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. 2012 Oct 1;75(1):115–170. doi: 10.3114/sim0012

Species concepts in Cercospora: spotting the weeds among the roses

JZ Groenewald 1,*, C Nakashima 2, J Nishikawa 3, H-D Shin 4, J-H Park 4, AN Jama 5, M Groenewald 1, U Braun 6, PW Crous 1,7,8
PMCID: PMC3713887  PMID: 24014899

Abstract

The genus Cercospora contains numerous important plant pathogenic fungi from a diverse range of hosts. Most species of Cercospora are known only from their morphological characters in vivo. Although the genus contains more than 5 000 names, very few cultures and associated DNA sequence data are available. In this study, 360 Cercospora isolates, obtained from 161 host species, 49 host families and 39 countries, were used to compile a molecular phylogeny. Partial sequences were derived from the internal transcribed spacer regions and intervening 5.8S nrRNA, actin, calmodulin, histone H3 and translation elongation factor 1-alpha genes. The resulting phylogenetic clades were evaluated for application of existing species names and five novel species are introduced. Eleven species are epi-, lecto- or neotypified in this study. Although existing species names were available for several clades, it was not always possible to apply North American or European names to African or Asian strains and vice versa. Some species were found to be limited to a specific host genus, whereas others were isolated from a wide host range. No single locus was found to be the ideal DNA barcode gene for the genus, and species identification needs to be based on a combination of gene loci and morphological characters. Additional primers were developed to supplement those previously published for amplification of the loci used in this study.

Taxonomic novelties:

New species - Cercospora coniogrammes Crous & R.G. Shivas, Cercospora delaireae C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora euphorbiae-sieboldianae C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora pileicola C. Nakash., Crous, U. Braun & H.D. Shin, Cercospora vignigena C. Nakash., Crous, U. Braun & H.D. Shin. Typifications: epitypifications - Cercospora alchemillicola U. Braun & C.F. Hill, Cercospora althaeina Sacc., Cercospora armoraciae Sacc., Cercospora corchori Sawada, Cercospora mercurialis Pass., Cercospora olivascens Sacc., Cercospora violae Sacc.; neotypifications - Cercospora fagopyri N. Nakata & S. Takim., Cercospora sojina Hara.

Key words: Cercospora apii complex, co-evolution, host jumping, host specificity, speciation

INTRODUCTION

Species of the genus Cercospora belong to one of the largest genera of hyphomycetes and were often linked to the teleomorph genus Mycosphaerella (Capnodiales, Mycosphaerellaceae; Stewart et al. 1999, Crous et al. 2000). The genus Mycosphaerella was shown to be polyphyletic (Crous et al. 2007), and subsequently split into numerous genera, correlating with its different anamorph states (Crous et al. 2009a, b). The genus Cercospora is now considered a holomorphic genus in its own right, with some species exhibiting the ability to form mycosphaerella-like teleomorphs (Corlett 1991, Crous et al. 2004b). Mycosphaerella s. str. on the other hand, is restricted to taxa that form Ramularia anamorphs (Verkley et al. 2004). As Mycosphaerella has been widely applied to more than 40 different genera, Crous et al. (2009b) expressed their preference to use the older, recently monographed (Braun 1998) anamorph-typified name Ramularia (1833) for this holomorphic clade, instead of the younger, confused teleomorph-typified generic name Mycosphaerella (1884). This is allowed under the new, changed Article 59 of the International Code for Nomenclature of algae, fungi, and plants (ICN) (Hawksworth 2011, Norvell 2011).

Species of Cercospora are commonly associated with leaf spots (Fig. 1), and have also been isolated from necrotic lesions of flowers, fruits and seeds or were associated with postharvest fruit rot disease (Silva & Pereira 2008) of hosts from across the world (Agrios 2005, To-Anun et al. 2011). The cercosporoid fungi have also been used as biocontrol agents (Morris & Crous 1994, Inglis et al. 2001, Tessman et al. 2001). Species of Cercospora were traditionally named after the host from which they were isolated, even to the extent that a species of Cercospora was described as new when found on a different host plant (Chupp 1954, Ellis 1971). The genus Cercospora was first erected by Fresenius for passalora-like fungi with pluriseptate conidia (in Fuckel 1863). Chupp’s (1954) monograph accepted 1 419 Cercospora species and proposed a broad concept for this genus based on whether hila were thickened or not, and whether conidia were pigmented, single or in chains. The number of Cercospora species doubled to more than 3 000 when Pollack (1987) published her annotated list of Cercospora names. Since then a combination of characters such as conidiomatal structure, mycelium, conidiophores, conidiogenous cells and conidia has been used to divide the genus into morphologically similar units. Crous & Braun (2003) used the structure of conidiogenous loci and hila as well as the absence or presence of pigmentation in conidiophores and conidia in their revision of names published in Cercospora and Passalora. They recognised 659 names in the genus Cercospora, with a further 281 names referred to as C. apii s. lat. The C. apii complex represented Cercospora species that were morphologically indistinguishable from C. apii (Ellis 1971, Crous & Braun 2003). In addition, Crous & Braun (2003) introduced the concept of “compound species” which consisted of morphologically indistinguishable species with different races (host range), genetically uniform or heterogeneous, with different degrees of biological specialisation. They also proposed that genetically and morphologically clearly distinguishable taxa should be treated as separate species, although the study was confounded by the general unavailability of Cercospora cultures for DNA analyses. Ex-type strains mostly do not exist as such isolates were neither designated nor preserved, for the majority of Cercospora species (Groenewald et al. 2010a). For most Cercospora species, a sexual stage (a mycosphaerella-like state) is not known; or has been reported, but not confirmed (Goodwin et al. 2001). The mating type genes of some apparently asexual Cercospora species were recently characterised, with the discovery that C. beticola, C. zeae-maydis and C. zeina were heterothallic, although only one mating type was present in populations of C. apii and C. apiicola (Groenewald et al. 2006b, 2010b). The two mating types of C. beticola were distributed approximately equally in the tested populations, indicating that these genes might indeed be active, indicative of cryptic sex. More recently a skewed distribution of mating types across sugar beet fields from different localities was report from Iran, with some fields having both mating types and others only the one or the other (Bakhshi et al. 2011). A further study conducted over a 3-yr period in the USA, also led to the conclusion that C. beticola has potential for sexual reproduction (Bolton et al. 2012).

Fig. 1.

Fig. 1.

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Foliar disease symptoms associated with Cercospora spp. A. C. achyranthis on Achyranthes japonica. B. C. dispori on Disporum viridescens. C. C. chinensis on Polygonatum humile. D. C. cf. flagellaris on Amaranthus patulus. E. C. capsici on Capsicum annuum. F. Cercospora sp. on Ajuga multiflora. G. Cercospora sp. on Cardamine leucanthe. H. C. cf. flagellaris on Celosia argentea var. cristata. I. C. zeina on Zea mays. J. C. beticola on Beta vulgaris. K. C. chrysanthemi on Chrysanthemum. L. C. apii on Apium. M. C. amoraciae on Rorippa indica. N. C. beticola on Chrysanthemum segetum. O. C. apiicola on Apium. P. C. ipomoeae on Persicaria thunbergii. Q. C. althaeina on Althaea rosea. R. C. zebrina on Trifolium repens. S. C. sojina on Glycine max. T. C. brunkii on Geranium nepalense.

Host specificity and speciation in Cercospora has not been studied extensively, but it is known that some species induce leaf spot symptoms when inoculated on other hosts, for example, C. beticola on all members of Beta (Chenopodiaceae) and other plant species (Weiland & Koch 2004) or C. apii and C. beticola isolated from disease symptoms on other hosts (Groenewald et al. 2006a). Cercospora caricis is used as a biological control agent of Cyperus rotundus (Cyperaceae), and Inglis et al. (2001) compared Brazilian isolates with an isolate from Florida, USA. The authors used RAPDs (Randomly Amplified Polymorphic DNA), RFLPs (Restriction Fragment Length Polymorphisms) with a telomeric probe and ITS sequencing and found that a cluster of isolates from the Brazilian cerrado region showed high genetic similarity, whereas similarity between this region and others in Brazil was less that 50 %. They also found that the ITS sequence analysis did not support a division in the Brazilian isolates (99 % similar sequences) but that it did separate the Florida isolate from the Brazilian isolates (96 % similar when included with the Brazilian isolates). They concluded that the isolate from Florida probably represented cryptic speciation but that larger sampling of isolates was required from different geographical areas to address this question. Host specificity for some species appears to operate at the strain level, as for C. rodmanii, in which the original strains of Conway (1976) were shown to be specific to water hyacinth, whereas strains identified by morphology and multi-locus sequence data as the same species, were able to infect beet and sugar beet (Montenegro-Calderón et al. 2011).

A number of molecular studies using ITS phylogenies confirmed that Cercospora taxa cluster in a well-supported monophyletic clade in Mycosphaerella (Stewart et al. 1999, Crous et al. 2000, 2009a, b, Goodwin et al. 2001, Pretorius et al. 2003), in contrast to other polyphyletic genera such as Septoria (Verkley et al. 2004; compared to the monophyletic Zymoseptoria, Quaedvlieg et al. 2011), Pseudocercospora, Passalora and Zasmidium (Crous et al. 2009b), to name but a few. The ITS region (ITS1, 5.8S rDNA and ITS2) lacks the resolution to distinguish between most Cercospora species (Groenewald et al. 2010a). For example, Goodwin et al. (2001) found a mean of 1.27 sequence changes over 18 taxa from 11 Cercospora species, and Pretorius et al. (2003) found a mean of 1.64 changes when they tested 25 taxa representing 11 Cercospora species. Both Goodwin et al. (2001) and Pretorius et al. (2003) observed more transitions than transversions. Only a limited number of studies utilising gene sequences other than ITS have been published thus far (for example Tessmann et al. 2001, Crous et al. 2004b, Groenewald et al. 2005, 2006a, 2010a, Montenegro-Calderón et al. 2011). Tessmann et al. (2001) found that 14 of the 431 aligned translation elongation factor 1-alpha characters were parsimony-informative, with only six of the 380 characters for beta-tubulin and 17 of the 309 histone H3 characters being parsimony-informative. The ITS region did not contain any differences when compared with the outgroup C. beticola. Crous et al. (2004b) used fixed nucleotide changes in aligned nucleotide characters (including alignment gaps) to discriminate C. acaciae-mangii from C. apii and C. beticola, and listed changes at none of 521 ITS characters (0 %), nine of 300 translation elongation factor 1-alpha characters (3 %), three of 209 actin characters (1.4 %), 10 of 312 calmodulin characters (3.2 %), and seven of 388 histone H3 characters (1.8 %). A total of 1 730 aligned characters were examined, of which 29 (1.68 %) were observed as fixed nucleotide changes. Using the same five loci, Groenewald et al. (2005) found 96 % similarity between C. apii and C. beticola for the calmodulin gene, with all other loci having identical sequences. Based on the differences in the calmodulin gene, distinctive AFLP banding patterns and different growth rates, the authors recognised C. apii s. str. and C. beticola s. str. as distinct species. Continuing with the same approach, Groenewald et al. (2006a) then proceeded to describe C. apiicola, a further distinct species thus far only isolated from Apium (Apiaceae). Both Groenewald et al. (2010a) and Montenegro-Calderón et al. (2011) used phylogenetic analyses of combined ITS, translation elongation factor 1-alpha, actin, calmodulin and histone H3 sequence alignments to study species boundaries and diversity in Cercospora. Groenewald et al. (2010a) concluded that although most loci tested could resolve a large number of species, the sum of the whole provided a better resolution compared to a subset of loci. In that study, the loci differed in their ability to resolve clades, with ITS and translation elongation factor 1-alpha performing worst (distinguishing three and 10 clades, respectively), while actin could distinguish 14 clades, calmodulin 13 clades and histone H3 12 clades compared to the 16 species clades recognised in the combined tree. Montenegro-Calderón et al. (2011) concluded that C. rodmanii could be distinguished from C. piaropi based on actin, calmodulin and histone H3, but that only calmodulin could clearly separate C. rodmanii from the other Cercospora species included in their study. These results illustrated that the phylogenetic approach using multi-locus sequences was one of the most effective ways to recognise different species of Cercospora. Although this approach is not suitable to recognise the true host range of a species without pathogenicity tests, it does provide a handle on the true identity of the strain being used.

Goodwin et al. (2001) attributed the short branch lengths observed for their ITS phylogeny to a relatively recent common ancestor that was able to, or acquired the ability to, produce cercosporin, a phytotoxic metabolite of polyketide origin (Daub & Ehrenshaft 2000). The ability to produce cercosporin probably allowed the Cercospora ancestor to rapidly expand its host range in a recent adaptive radiation (Goodwin et al. 2001). It has been suggested that this compound may enhance virulence (Upchurch et al. 1991), but it is not a universal pathogenicity factor as cercosporin is not produced by all species (Assante et al. 1977, examples cited by Goodwin et al. 2001, see also review by Weiland et al. 2010). Nutritional and environmental conditions influence the production of cercosporin, making it useless for application in Cercospora taxonomy (Jenns et al. 1989). Genomic studies in recent years attempt to understand the metabolic pathway used to produce cercosporin and C. nicotianae has become the model organism for these studies (e.g. Chung et al. 2003, Choquer et al. 2005, Chen et al. 2007, Amnuaykanjanasin & Daub 2009).

In an attempt to address some of the shortcomings highlighted in the previous paragraph, we have obtained diseased plant material and/or cultures from as many hosts and countries as possible over several years. We sequenced the ITS locus (including ITS1, 5.8S nrRNA gene and ITS2), as well as parts of four genomic protein coding genes, namely translation elongation-factor 1-alpha, actin, calmodulin and histone H3 for each culture. Our primary objective was to re-evaluate the species concept of known Cercospora species by consolidating the results of multi-locus phylogenetic analyses with morphological characteristics produced on host plants and different media. A secondary objective was to test whether Cercospora species, in general, were host-specific.

MATERIALS AND METHODS

Specimens and isolates

Dried specimens and cultures used in this study are maintained in herbaria and culture collections of Genebank, National Institute of Agrobiological Sciences, Japan, (MAFF), the Mycological Herbarium and Culture Collection, laboratory of Plant Pathology, Mie University, Japan (MUMH or MUCC) and the Centraalbureau voor Schimmelcultures (CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands), or the working collection of P.W. Crous (CPC), housed at CBS (Table 1). A global set of isolates (Table 1) was either obtained from personal culture collections, the culture collection of the CBS or recollected on diseased plant material, and grown in axenic culture. Symptomatic leaves with leaf spots were chosen for isolations of Cercospora spp. as explained in Crous (1998). To obtain ascospore isolates, excised lesions were placed in distilled water for approximately 2 h, after which they were placed on the bottom of Petri dish lids, over which the plate containing 2 % malt extract agar (MEA) (Crous et al. 1991, 2009c) was inverted. Germinating ascospores were examined after 24 h, and single-ascospore cultures established on MEA as explained by Crous (1998). Colonies were sub-cultured onto oatmeal agar (OA), V8-juice agar (V8), 2 % potato-dextrose agar (PDA) or MEA (Crous et al. 2009c) and incubated at 25 °C under continuous near-ultraviolet light, to promote sporulation.

Table 1.

Collection details and GenBank accession numbers of isolates included in this study.

Species Culture accession number(s)1 Host name or isolation source Host Family Country Collector GenBank accession numbers2
ITS TEF ACT CAL HIS
Cercospora achyranthis CBS 132613; CPC 10879 Achyranthes japonica Amaranthaceae South Korea: Jeju H.D. Shin JX143523 JX143277 JX143031 JX142785 JX142539
CPC 10091 Achyranthes japonica Amaranthaceae South Korea: Jeju H.D. Shin JX143524 JX143278 JX143032 JX142786 JX142540
Cercospora agavicola CBS 117292; CPC 11774 (TYPE) Agave tequilana var. azul Agavaceae Mexico: Penjamo V. Ayala-Escobar & Ma. de Jesús Yáñez-Morales AY647237 AY966897 AY966898 AY966899 AY966900
Cercospora alchemillicola CPC 5259 (TYPE) Alchemilla mollis Rosaceae New Zealand: Auckland C.F. Hill JX143525 JX143279 JX143033 JX142787 JX142541
Cercospora cf. alchemillicola CPC 5126 Oenothera fruticosa Onagraceae New Zealand: Auckland C.F. Hill JX143526 JX143280 JX143034 JX142788 JX142542
CPC 5127 Gaura lindheimeri Onagraceae New Zealand: Auckland C.F. Hill JX143527 JX143281 JX143035 JX142789 JX142543
Cercospora althaeina CBS 126.26; CPC 5066 Malva sp. Malvaceae – C. Killian JX143528 JX143282 JX143036 JX142790 JX142544
CBS 132609; CPC 10790 Althaea rosea Malvaceae South Korea: Suwon H.D. Shin JX143529 JX143283 JX143037 JX142791 JX142545
CBS 248.67; CPC 5117 (TYPE) Althaea rosea Malvaceae Romania: Fundulea O. Constantinescu JX143530 JX143284 JX143038 JX142792 JX142546
Cercospora apii CBS 110813; CPC 5110; 01-3 Moluccella laevis Lamiaceae USA: California S.T. Koike AY156918 DQ233345 DQ233371 DQ233397 DQ233423
CBS 110816; CPC 5111; 01-4 Moluccella laevis Lamiaceae USA: California S.T. Koike AY156919 DQ233346 DQ233372 DQ233398 DQ233424
CBS 114416; CPC 10925 Apium sp. Apiaceae Austria Institut fur Pflanzengesundheit AY840516 AY840483 AY840447 AY840414 AY840381
CBS 114418; CPC 10924 Apium graveolens Apiaceae Italy M. Meutri AY840517 AY840484 AY840448 AY840415 AY840382
CBS 114485; CPC 10923 Apium graveolens Apiaceae Italy M. Meutri AY840518 AY840485 AY840449 AY840416 AY840383
CBS 116455; CPC 11556 (TYPE) Apium graveolens Apiaceae Germany: Heilbron K. Schrameyer AY840519 AY840486 AY840450 AY840417 AY840384
CBS 116504; CPC 11579 Apium graveolens Apiaceae Germany: Heilbron K. Schrameyer AY840520 AY840487 AY840451 AY840418 AY840385
CBS 116507; CPC 11582 Apium graveolens Apiaceae Germany: Heilbron K. Schrameyer AY840521 AY840488 AY840452 AY840419 AY840386
CBS 119.25; B 42463; IHEM 3822; CPC 5086 Apium graveolens Apiaceae – L. J. Klotz AY179949 AY179915 AY840443 AY840410 AY840377
CBS 121.31; CPC 5073 Beta vulgaris Chenopodiaceae Austria: Wien E.W. Schmidt AY343371 AY343334 AY840444 AY840411 AY840378
CBS 127.31; CPC 5119 Beta vulgaris Chenopodiaceae Hungary E.W. Schmidt AY840514 AY840481 AY840445 AY840412 AY840379
CBS 132683; CPC 16663 Moluccella laevis Lamiaceae Zimbabwe S. Dimbi JX143531 JX143285 JX143039 JX142793 JX142547
CBS 152.52; IMI 077043; MUCL 16495; CPC 5063 Beta vulgaris Chenopodiaceae Netherlands: Bergen op Zoom G. van den Ende AY840515 AY840482 AY840446 AY840413 AY840380
CBS 252.67; CPC 5084 Plantago lanceolata Plantaginaceae Romania: Domnesti O. Constantinescu DQ233318 DQ233342 DQ233368 DQ233394 DQ233420
CBS 536.71; CPC 5087 Apium graveolens Apiaceae Romania: Bucuresti O. Constantinescu AY752133 AY752166 AY752194 AY752225 AY752256
CBS 553.71; IMI 161116; CPC 5083 Plumbago europaea Plumbaginaceae Romania: Hagieni O. Constantinescu DQ233320 DQ233344 DQ233370 DQ233396 DQ233422
CPC 18601 Apium graveolens Apiaceae USA: California S.T. Koike JX143532 JX143286 JX143040 JX142794 JX142548
CPC 5112 Moluccella laevis Lamiaceae New Zealand: Auckland C.F. Hill DQ233321 DQ233347 DQ233373 DQ233399 DQ233425
CPC 5260 Glebionis coronaria (≡ Chrysanthemum coronarium) Asteraceae New Zealand: Auckland C.F. Hill JX143533 JX143287 JX143041 JX142795 JX142549
MUCC 567; MUCNS 30; MAFF 238072 Apium graveolens Apiaceae Japan: Aichi T. Kobayashi JX143534 JX143288 JX143042 JX142796 JX142550
MUCC 573; MAFF 235978 Glebionis coronaria (≡ Chrysanthemum coronarium) Asteraceae Japan: Hokkaido – JX143535 JX143289 JX143043 JX142797 JX142551
MUCC 593 Apium graveolens Apiaceae Japan: Shizuoka M. Togawa JX143536 JX143290 JX143044 JX142798 JX142552
MUCC 923; MAFF 238299 Asparagus officinalis Asparagaceae Japan: Saga J. Yamaguchi JX143537 JX143291 JX143045 JX142799 JX142553
Cercospora apiicola CBS 116457; CPC 10267 (TYPE) Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840536 AY840503 AY840467 AY840434 AY840401
CBS 116458; CPC 10657 Apium graveolens Apiaceae South Korea: Kangnung H.D. Shin AY840537 AY840504 AY840468 AY840435 AY840402
CBS 132644; CPC 10248 Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840539 AY840506 AY840470 AY840437 AY840404
CBS 132651; CPC 10759 Apium graveolens Apiaceae South Korea: Namyangju H.D. Shin AY840544 AY840511 AY840475 AY840442 AY840409
CBS 132666; CPC 11642; GRE-4-2 Apium sp. Apiaceae Greece I. Vloutoglou DQ233341 DQ233367 DQ233393 DQ233419 DQ233441
CPC 10220 Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840538 AY840505 AY840469 AY840436 AY840403
CPC 10265 Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840540 AY840507 AY840471 AY840438 AY840405
CPC 10266 Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840541 AY840508 AY840472 AY840439 AY840406
CPC 10279 Apium sp. Apiaceae Venezuela: Caripe N. Pons AY840542 AY840509 AY840473 AY840440 AY840407
CPC 10666 Apium sp. Apiaceae South Korea: Kangnung H.D. Shin AY840543 AY840510 AY840474 AY840441 AY840408
CPC 11641; GRE-3-2 Apium sp. Apiaceae Greece I. Vloutoglou DQ233340 DQ233366 DQ233392 DQ233418 DQ233440
Cercospora armoraciae CBS 115060; CPC 5366 Gaura sp. Onagraceae New Zealand C.F. Hill JX143538 JX143292 JX143046 JX142800 JX142554
CBS 115394; CPC 5261 Nasturtium officinale (= Rorippa nasturtium-aquaticum) Brassicaceae New Zealand: Auckland C.F. Hill JX143539 JX143293 JX143047 JX142801 JX142555
CBS 115409; CPC 5359 Armoracia rusticana (= A. lapathifolia) Brassicaceae New Zealand: Manurewa C.F. Hill JX143540 JX143294 JX143048 JX142802 JX142556
CBS 132610; CPC 10811 Armoracia rusticana (= A. lapathifolia) Brassicaceae South Korea: Suwon H.D. Shin JX143541 JX143295 JX143049 JX142803 JX142557
CBS 132638; CPC 10100 Barbarea orthoceras Brassicaceae South Korea: Pocheon H.D. Shin JX143542 JX143296 JX143050 JX142804 JX142558
CBS 132654; CPC 11338 Turritis glabra (≡ Arabis glabra) Brassicaceae South Korea: Hoengseong H.D. Shin JX143543 JX143297 JX143051 JX142805 JX142559
CBS 132672; CPC 14612 Rorippa indica Brassicaceae South Korea: Jecheon H.D. Shin JX143544 JX143298 JX143052 JX142806 JX142560
CBS 250.67; CPC 5088 (TYPE) Armoracia rusticana (= A. lapathifolia) Brassicaceae Romania: Fundulea O. Constantinescu JX143545 JX143299 JX143053 JX142807 JX142561
CBS 258.67; CPC 5061 Cardaria draba Brassicaceae Romania: Fundulea O. Constantinescu JX143546 JX143300 JX143054 JX142808 JX142562
CBS 538.71; IMI 161109; CPC 5090 Berteroa incana Brassicaceae Romania: Hagieni O. Constantinescu JX143547 JX143301 JX143055 JX142809 JX142563
CBS 540.71; IMI 161110; CPC 5060 Cardaria draba Brassicaceae Romania: Hagieni O. Constantinescu JX143548 JX143302 JX143056 JX142810 JX142564
CBS 545.71; CPC 5056 Erysimum cuspidatum Brassicaceae Romania: Valea Mraconiei O. Constantinescu JX143549 JX143303 JX143057 JX142811 JX142565
CBS 555.71; IMI 161117; CPC 5082 Coronilla varia Fabaceae Romania: Hagieni O. Constantinescu JX143550 JX143304 JX143058 JX142812 JX142566
CPC 10133 Rorippa indica Brassicaceae South Korea: Wonju H.D. Shin JX143551 JX143305 JX143059 JX142813 JX142567
CPC 11364 Turritis glabra (≡ Arabis glabra) Brassicaceae South Korea: Hoengseong H.D. Shin JX143552 JX143306 JX143060 JX142814 JX142568
CPC 11530 Acacia mangium Fabaceae Thailand W. Himaman JX143553 JX143307 JX143061 JX142815 JX142569
MUCC 768 Armoracia rusticana (= A. lapathifolia) Brassicaceae Japan: Okinawa C. Nakashima JX143554 JX143308 JX143062 JX142816 JX142570
Cercospora beticola CBS 113069; CPC 5369 Spinacia sp. Chenopodiaceae Botswana: Gaborone L. Lebogang DQ233325 DQ233351 DQ233377 DQ233403 DQ233429
CBS 115478; CPC 5113 Limonium sinuatum Plumbaginaceae New Zealand: Auckland C.F. Hill DQ233326 DQ233352 DQ233378 DQ233404 DQ233430
CBS 116.47; CPC 5074 Beta vulgaris Chenopodiaceae Netherlands: Northwest Brabant G.E. Bunschoten AY752135 AY752168 AY752196 AY752227 AY752258
CBS 116454; CPC 11558 Beta vulgaris Chenopodiaceae Germany S. Mittler AY840526 AY840493 AY840457 AY840424 AY840391
CBS 116456; CPC 11557 (TYPE) Beta vulgaris Chenopodiaceae Italy: Ravenna V. Rossi AY840527 AY840494 AY840458 AY840425 AY840392
CBS 116501; CPC 11576 Beta vulgaris Chenopodiaceae Iran: Pakajik A.A. Ravanlou AY840528 AY840495 AY840459 AY840426 AY840393
CBS 116502; CPC 11577 Beta vulgaris Chenopodiaceae Germany S. Mittler AY840529 AY840496 AY840460 AY840427 AY840394
CBS 116503; CPC 11578 Beta vulgaris Chenopodiaceae Italy: Ravenna V. Rossi AY840530 AY840497 AY840461 AY840428 AY840395
CBS 116505; CPC 11580 Beta vulgaris Chenopodiaceae France: Longvic S. Garressus AY840531 AY840498 AY840462 AY840429 AY840396
CBS 116506; CPC 11581 Beta vulgaris Chenopodiaceae Netherlands M. Groenewald AY840532 AY840499 AY840463 AY840430 AY840397
CBS 117.47 Beta vulgaris Chenopodiaceae Czech Republic G.E. Bunschoten DQ233322 DQ233348 DQ233374 DQ233400 DQ233426
CBS 117556; CPC 10171 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill AY840534 AY840501 AY840465 AY840432 AY840399
CBS 122.31; CPC 5072 Beta vulgaris Chenopodiaceae Germany: Gmain E.W. Schmidt AY752136 AY752169 AY752197 AY752228 AY752259
CBS 123.31; CPC 5071 Beta vulgaris Chenopodiaceae Spain E.W. Schmidt AY840522 AY840489 AY840453 AY840420 AY840387
CBS 123907; CPC 14616 Goniolimon tataricum Plumbaginaceae Bulgaria S.G. Bobev FJ473422 FJ473427 FJ473432 FJ473437 FJ473442
CBS 123908; CPC 14620 Goniolimon tataricum Plumbaginaceae Bulgaria S.G. Bobev FJ473426 FJ473431 FJ473436 FJ473441 FJ473446
CBS 124.31; CPC 5070 Beta vulgaris Chenopodiaceae Romania: Hagieni E.W. Schmidt AY840523 AY840490 AY840454 AY840421 AY840388
CBS 125.31; CPC 5069 Beta vulgaris Chenopodiaceae – E.W. Schmidt AY840524 AY840491 AY840455 AY840422 AY840389
CBS 126.31; CPC 5064 Beta vulgaris Chenopodiaceae Germany: Klein Wanzleben E.W. Schmidt AY840525 AY840492 AY840456 AY840423 AY840390
CBS 132655; CPC 11341 Chrysanthemum segetum (= Ch. coronarium var. spatiosum) Asteraceae South Korea: Namyangju H.D. Shin DQ233332 DQ233358 DQ233384 DQ233410 DQ233434
CBS 132673; CPC 14617 Goniolimon tataricum Plumbaginaceae Bulgaria S.G. Bobev FJ473423 FJ473428 FJ473433 FJ473438 FJ473443
CBS 539.71; CPC 5062 Beta vulgaris Chenopodiaceae Romania: Bucuresti O. Constantinescu DQ233323 DQ233349 DQ233375 DQ233401 DQ233427
CBS 548.71; IMI 161115; CPC 5065 Malva pusilla Malvaceae Romania: Hagieni O. Constantinescu & G. Negrean DQ233324 DQ233350 DQ233376 DQ233402 DQ233428
CPC 10166 Beta vulgaris Chenopodiaceae New Zealand C.F. Hill DQ233329 DQ233355 DQ233381 DQ233407 DQ026471
CPC 10168 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill AY840533 AY840500 AY840464 AY840431 AY840398
CPC 10195 Beta vulgaris Chenopodiaceae New Zealand C.F. Hill DQ233330 DQ233356 DQ233382 DQ233408 DQ026472
CPC 10197 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill AY840535 AY840502 AY840466 AY840433 AY840400
CPC 10204 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill DQ233331 DQ233357 DQ233383 DQ233409 DQ233433
CPC 11344 Chrysanthemum segetum (= Ch. coronarium var. spatiosum) Asteraceae South Korea: Namyangju H.D. Shin DQ233333 DQ233359 DQ233385 DQ233411 DQ233435
CPC 12022 Beta vulgaris Chenopodiaceae Germany S. Mittler DQ233334 DQ233360 DQ233386 DQ233412 DQ233436
CPC 12027 Beta vulgaris Chenopodiaceae Germany S. Mittler DQ233335 DQ233361 DQ233387 DQ233413 DQ026468
CPC 12028 Beta vulgaris Chenopodiaceae Egypt M. Hasem DQ233336 DQ233362 DQ233388 DQ233414 DQ233437
CPC 12029 Beta vulgaris Chenopodiaceae Egypt M. Hasem DQ233337 DQ233363 DQ233389 DQ233415 DQ233438
CPC 12030 Beta vulgaris Chenopodiaceae Egypt M. Hasem DQ233338 DQ233364 DQ233390 DQ233416 DQ233439
CPC 12031 Beta vulgaris Chenopodiaceae Germany S. Mittler DQ233339 DQ233365 DQ233391 DQ233417 DQ026470
CPC 14618 Goniolimon tataricum Plumbaginaceae Bulgaria S.G. Bobev FJ473424 FJ473429 FJ473434 FJ473439 FJ473444
CPC 14619 Goniolimon tataricum Plumbaginaceae Bulgaria S.G. Bobev FJ473425 FJ473430 FJ473435 FJ473440 FJ473445
CPC 15623 Beta vulgaris Chenopodiaceae Mexico: Texcoco Ma. de Jesús Yáñez-Morales JX143555 JX143309 JX143063 JX142817 JX142571
CPC 18813 Beta vulgaris Chenopodiaceae USA: California S.T. Koike JX143556 JX143310 JX143064 JX142818 JX142572
CPC 5123 Apium graveolens Apiaceae New Zealand: Auckland C.F. Hill AY752134 AY752167 AY752195 AY752226 AY752257
CPC 5125 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill AY752137 AY752170 AY752198 AY752229 AY752260
CPC 5128 Beta vulgaris Chenopodiaceae New Zealand: Auckland C.F. Hill AY752138 AY752171 AY752199 AY752230 AY752261
CPC 5370 Spinacia sp. Chenopodiaceae Botswana: Gaborone L. Lebogang DQ233328 DQ233354 DQ233380 DQ233406 DQ233432
MUCC 568; MUCNS 320; MAFF 238206 Beta vulgaris Chenopodiaceae Japan: Chiba S. Uematsu JX143557 JX143311 JX143065 JX142819 JX142573
MUCC 569; MAFF 305036 Beta vulgaris Chenopodiaceae Japan: Hokkaido K. Goto JX143558 JX143312 JX143066 JX142820 JX142574
Cercospora cf. brunkii CBS 132657; CPC 11598 Geranium thunbergii (≡ G. nepalense var. thunbergii) Geraniaceae South Korea: Namyangju H.D. Shin JX143559 JX143313 JX143067 JX142821 JX142575
MUCC 732 Datura stramonium Solanaceae Japan: Wakayama C. Nakashima & I. Araki JX143560 JX143314 JX143068 JX142822 JX142576
Cercospora campi-silii CBS 132625; CPC 14585 Impatiens noli-tangere Balsaminaceae South Korea: Inje H.D. Shin JX143561 JX143315 JX143069 JX142823 JX142577
Cercospora canescens complex CBS 111133; CPC 1137 Vigna sp. Fabaceae South Africa: Potchefstroom S. van Wyk AY260065 DQ835084 DQ835103 DQ835130 DQ835157
CBS 111134; CPC 1138 Vigna sp. Fabaceae South Africa: Potchefstroom S. van Wyk AY260066 DQ835085 DQ835104 DQ835131 DQ835158
CBS 132658; CPC 11626; GHA-1-0 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143562 JX143316 JX143070 JX142824 JX142578
CBS 132659; CPC 11627; GHA-1-1 Dioscorea alata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143563 JX143317 JX143071 JX142825 JX142579
CBS 153.55; CPC 5059 Phaseolus lunatus (= Ph. limensis) Fabaceae USA: Georgia E.S. Luttrell JX143564 JX143318 JX143072 JX142826 JX142580
CPC 11628; GHA-2-1 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143565 JX143319 JX143073 JX142827 JX142581
CPC 11640; IMI 186563 Apium sp. Apiaceae USA – JX143566 JX143320 JX143074 JX142828 JX142582
CPC 15871 – Malvaceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143567 JX143321 JX143075 JX142829 JX142583
CPC 4408; Q 160 IS2 Citrus maxima Rutaceae South Africa: Tsipise K. Serfontein AY260067 DQ835086 DQ835105 DQ835132 DQ835159
CPC 4409 Citrus maxima Rutaceae South Africa: Tsipise K. Serfontein AY260068 DQ835087 DQ835106 DQ835133 DQ835160
Cercospora capsici CBS 118712 Lesions on calyx attached to fruit – Fiji P. Tyler GU214653 JX143322 JX143076 JX142830 JX142584
CBS 132622; CPC 14520 Capsicum annuum Solanaceae South Korea: Yanggu H.D. Shin JX143568 JX143323 JX143077 JX142831 JX142585
CPC 12307 Capsicum annuum Solanaceae South Korea: Hongcheon H.D. Shin GU214654 JX143324 JX143078 JX142832 JX142586
MUCC 574; MUCNS 810; MAFF 238227 Capsicum annuum Solanaceae Japan: Chiba S. Uematsu JX143569 JX143325 JX143079 JX142833 JX142587
Cercospora celosiae CBS 132600; CPC 10660 Celosia argentea var. cristata (≡ C. cristata) Amaranthaceae South Korea: Chuncheon H.D. Shin JX143570 JX143326 JX143080 JX142834 JX142588
Cercospora chenopodii CBS 132620; CPC 14237 Chenopodium cf. album Chenopodiaceae France: Ardeche P.W. Crous JX143571 JX143327 JX143081 JX142835 JX142589
Cercospora cf. chenopodii CBS 132594; CPC 10304 (TYPE) Chenopodium ficifolium Chenopodiaceae South Korea: Hongcheon H.D. Shin JX143572 JX143328 JX143082 JX142836 JX142590
CBS 132677; CPC 15599 Chenopodium sp. Chenopodiaceae Mexico: Montecillo Ma. de Jesús Yáñez-Morales JX143573 JX143329 JX143083 JX142837 JX142591
CPC 12450 Chenopodium ficifolium Chenopodiaceae South Korea: Hongcheon H.D. Shin JX143574 JX143330 JX143084 JX142838 JX142592
CPC 15763 Chenopodium sp. Chenopodiaceae Mexico: Montecillo Ma. de Jesús Yáñez-Morales JX143575 JX143331 JX143085 JX142839 JX142593
CPC 15859 Chenopodium sp. Chenopodiaceae Mexico: Purificacion Ma. de Jesús Yáñez-Morales JX143576 JX143332 JX143086 JX142840 JX142594
CPC 15862 Chenopodium sp. Chenopodiaceae Mexico: Purificacion Ma. de Jesús Yáñez-Morales JX143577 JX143333 JX143087 JX142841 JX142595
Cercospora chinensis CBS 132612; CPC 10831 Polygonatum humile Convallariaceae South Korea: Pyeongchang H.D. Shin JX143578 JX143334 JX143088 JX142842 JX142596
Cercospora cf. citrulina CBS 119395; CPC 12682 Musa sp. Musaceae Bangladesh: Western I. Buddenhagen EU514222 JX143335 JX143089 JX142843 JX142597
CBS 132669; CPC 12683 Musa sp. Musaceae Bangladesh: Western I. Buddenhagen EU514223 JX143336 JX143090 JX142844 JX142598
MUCC 576; MUCNS 300; MAFF 237913 Citrullus lanatus Cucurbitaceae Japan: Okinawa T. Kobayashion et al. JX143579 JX143337 JX143091 JX142845 JX142599
MUCC 577; MUCNS 254; MAFF 238205 Momordica charanthia Cucurbitaceae Japan: Kagoshima E. Imaizumi & C. Nomi JX143580 JX143338 JX143092 JX142846 JX142600
MUCC 584; MAFF 305757 Psophocarpus tetragonolobus Fabaceae Japan: Okinawa – JX143581 JX143339 JX143093 JX142847 JX142601
MUCC 588; MAFF 239409 Ipomoea pes-caprae Convolvulaceae Japan: Okinawa – JX143582 JX143340 JX143094 JX142848 JX142602
Cercospora coniogrammes CBS 132634; CPC 17017 (TYPE) Coniogramme japonica var. gracilis (≡ C. gracilis) Adiantaceae Australia: Queensland P.W. Crous JX143583 JX143341 JX143095 JX142849 JX142603
Cercospora corchori MUCC 585; MUCNS 72; MAFF 238191 (TYPE) Corchorus olitorius Tiliaceae Japan: Shimane T. Mikami JX143584 JX143342 JX143096 JX142850 JX142604
Cercospora cf. coreopsidis CBS 132598; CPC 10648 Coreopsis lanceolata Asteraceae South Korea: Seoul H.D. Shin JX143585 JX143343 JX143097 JX142851 JX142605
CPC 10122 Coreopsis lanceolata Asteraceae South Korea: Wonju H.D. Shin JX143586 JX143344 JX143098 JX142852 JX142606
Cercospora delaireae CBS 132595; CPC 10455; GV2 PPRI number: C558 (TYPE) Delairea odorata (= Senecio mikanioides) Asteraceae South Africa: Long TomcPass S. Neser JX143587 JX143345 JX143099 JX142853 JX142607
CPC 10627 Delairea odorata (= Senecio mikanioides) Asteraceae South Africa: Plettenberg Bay C.L. Lennox JX143588 JX143346 JX143100 JX142854 JX142608
CPC 10628 Delairea odorata (= Senecio mikanioides) Asteraceae South Africa: Plettenberg Bay C.L. Lennox JX143589 JX143347 JX143101 JX142855 JX142609
CPC 10629 Delairea odorata (= Senecio mikanioides) Asteraceae South Africa: Plettenberg Bay C.L. Lennox JX143590 JX143348 JX143102 JX142856 JX142610
Cercospora dispori CBS 132608; CPC 10773 Disporum viridescens Convallariaceae South Korea: Pyeongchang H.D. Shin JX143591 JX143349 JX143103 JX142857 JX142611
Cercospora cf. erysimi CBS 115059; CPC 5361 Erysimum mutabile Brassicaceae New Zealand: Manurewa C.F. Hill JX143592 JX143350 JX143104 JX142858 JX142612
Cercospora euphorbiaesieboldianae CBS 113306 (TYPE) Euphorbia sieboldiana Euphorbiaceae South Korea: Samcheok H.D. Shin JX143593 JX143351 JX143105 JX142859 JX142613
Cercospora fagopyri CBS 132623; CPC 14541 (TYPE) Fagopyrum esculentum Polygonaceae South Korea: Yangpyeong H.D. Shin JX143594 JX143352 JX143106 JX142860 JX142614
CBS 132640; CPC 10109 Fallopia dumentorum Polygonaceae South Korea: Yangpyeong H.D. Shin JX143595 JX143353 JX143107 JX142861 JX142615
CBS 132649; CPC 10725 Viola mandschurica Violaceae South Korea: Suwon H.D. Shin JX143596 JX143354 JX143108 JX142862 JX142616
CBS 132671; CPC 14546 Cercis chinensis Fabaceae South Korea: Yangpyeong H.D. Shin JX143597 JX143355 JX143109 JX142863 JX142617
MUCC 130 Cosmos bipinnata Asteraceae Japan: Ehime J. Nishikawa JX143598 JX143356 JX143110 JX142864 JX142618
MUCC 866 Hibiscus syriacus Malvaceae Japan: Ehime J. Nishikawa JX143599 JX143357 JX143111 JX142865 JX142619
Cercospora cf. flagellaris CBS 113127; RC3766; TX-18 Eichhornia crassipes Pontederiaceae USA: Texas D. Tessmann & R. Charudattan DQ835075 AF146147 DQ835121 DQ835148 DQ835175
CBS 115482; A207 Bs+; CPC 4410 Citrus sp. Rutaceae South Africa: Messina M.C. Pretorius AY260070 DQ835095 DQ835114 DQ835141 DQ835168
CBS 132637; CPC 10079 Trachelium sp. Campanulaceae Israel E. Tzul-Abad JX143600 JX143358 JX143112 JX142866 JX142620
CBS 132646; CPC 10681 Cichorium intybus Asteraceae South Korea: Suwon H.D. Shin JX143601 JX143359 JX143113 JX142867 JX142621
CBS 132648; CPC 10722 Amaranthus patulus Amaranthaceae South Korea: Namyangju H.D. Shin JX143602 JX143360 JX143114 JX142868 JX142622
CBS 132653; CPC 10884 Dysphania ambrosioides (≡ Chenopodium ambrosioides) Chenopodiaceae South Korea: Jeju H.D. Shin JX143603 JX143361 JX143115 JX142869 JX142623
CBS 132667; CPC 11643 Celosia argentea var. cristata (≡ C. cristata) Amaranthaceae South Korea: Hoengseong H.D. Shin JX143604 JX143362 JX143116 JX142870 JX142624
CBS 132670; CPC 14487 Sigesbeckia pubescens Asteraceae South Korea: Yanggu H.D. Shin JX143605 JX143363 JX143117 JX142871 JX142625
CBS 132674; CPC 14723 Phytolacca americana Phytolaccaceae South Korea: Jeju H.D. Shin JX143606 JX143364 JX143118 JX142872 JX142626
CBS 143.51; CPC 5055 Bromus sp. Poaceae – M.D. Whitehead JX143607 JX143365 JX143119 JX142873 JX142627
CPC 10124 Phytolacca americana Phytolaccaceae South Korea: Pocheon H.D. Shin JX143608 JX143366 JX143120 JX142874 JX142628
CPC 1051 Populus deltoides Salicaceae South Africa P.W. Crous AY260069 JX143367 JX143121 JX142875 JX142629
CPC 1052 Populus deltoides Salicaceae South Africa P.W. Crous JX143609 JX143368 JX143122 JX142876 JX142630
CPC 10684 Phytolacca americana Phytolaccaceae South Korea: Jinju H.D. Shin JX143610 JX143369 JX143123 JX142877 JX142631
CPC 4411; Q207 F5 Citrus sp. Rutaceae South Africa: Messina M.C. Pretorius AY260071 DQ835098 DQ835118 DQ835145 DQ835172
CPC 5441 Amaranthus sp. Amaranthaceae Fiji C.F. Hill JX143611 JX143370 JX143124 JX142878 JX142632
MUCC 127 Cosmos sulphureus Asteraceae Japan: Ehime J. Nishikawa JX143612 JX143371 JX143125 JX142879 JX142633
MUCC 735 Hydrangea serrata Hydrangeaceae Japan: Wakayama C. Nakashima & I. Araki JX143613 JX143372 JX143126 JX142880 JX142634
MUCC 831 Hydrangea serrata Hydrangeaceae Japan: Tokyo I. Araki & M. Harada JX143614 JX143373 JX143127 JX142881 JX142635
Cercospora cf. helianthicola MUCC 716 Helianthus tuberosus Asteraceae Japan: Wakayama C. Nakashima & I. Araki JX143615 JX143374 JX143128 JX142882 JX142636
Cercospora cf. ipomoeae CBS 132639; CPC 10102 Persicaria thunbergii Polygonaceae South Korea: Pocheon H.D. Shin JX143616 JX143375 JX143129 JX142883 JX142637
CBS 132652; CPC 10833 Ipomoea nil (= I. hederacea) Convolvulaceae South Korea: Chuncheon H.D. Shin JX143617 JX143376 JX143130 JX142884 JX142638
MUCC 442 Ipomoea aquatica Convolvulaceae Japan: Kagawa G. Kizaki JX143618 JX143377 JX143131 JX142885 JX142639
Cercospora kikuchii CBS 128.27; CPC 5068 (TYPE) Glycine soja Fabaceae Japan T. Matsumoto DQ835070 DQ835088 DQ835107 DQ835134 DQ835161
CBS 132633; CPC 16578 Glycine max Fabaceae Argentina – JX143619 JX143378 JX143132 JX142886 JX142640
CBS 135.28; CPC 5067 Glycine soja Fabaceae Japan H.W. Wollenweber DQ835071 DQ835089 DQ835108 DQ835135 DQ835162
MUCC 590; MAFF 305040 Glycine soja Fabaceae Japan: Kagoshima H. Kurata JX143620 JX143379 JX143133 JX142887 JX142641
Cercospora lactucae-sativae CBS 132604; CPC 10728 Ixeris chinensis subsp. strigosa (≡ Ixeris strigosa) Asteraceae South Korea: Chuncheon H.D. Shin JX143621 JX143380 JX143134 JX142888 JX142642
CPC 10082 Ixeris chinensis subsp. strigosa (≡ Ixeris strigosa) Asteraceae South Korea: Chuncheon H.D. Shin JX143622 JX143381 JX143135 JX142889 JX142643
MUCC 570; MUCN S463; MAFF 238209 Lactuca sativa Asteraceae Japan: Chiba C. Nakashima JX143623 JX143382 JX143136 JX142890 JX142644
MUCC 571; MUCNS 214; MAFF 237719 Lactuca sativa Asteraceae Japan: Chiba S. Uematsu JX143624 JX143383 JX143137 JX142891 JX142645
Cercospora cf. malloti MUCC 575; MUCNS 582; MAFF 237872 Cucumis melo Cucurbitaceae Japan: Okinawa K. Uehara JX143625 JX143384 JX143138 JX142892 JX142646
MUCC 787 Mallotus japonicus Euphorbiaceae Japan: Okinawa C. Nakashima & T. Akashi JX143626 JX143385 JX143139 JX142893 JX142647
Cercospora mercurialis CBS 549.71 Mercurialis annua Euphorbiaceae Romania: Cheia O. Constantinescu JX143627 JX143386 JX143140 JX142894 JX142648
CBS 550.71 (TYPE) Mercurialis perennis Euphorbiaceae Romania: Cheia O. Constantinescu JX143628 JX143387 JX143141 JX142895 JX142649
CBS 551.71 Mercurialis ovata Euphorbiaceae Romania: Hagieni O. Constantinescu & G. Negrean JX143629 JX143388 JX143142 JX142896 JX142650
Cercospora cf. modiolae CPC 5115 Modiola caroliniana Malvaceae New Zealand C.F. Hill JX143630 JX143389 JX143143 JX142897 JX142651
Cercospora cf. nicotianae CBS 131.32; CPC 5076 Nicotiana tabacum Solanaceae Indonesia: Medan H. Diddens & A. Jaarsveld DQ835073 DQ835099 DQ835119 DQ835146 DQ835173
CBS 132632; CPC 15918 Glycine max Fabaceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143631 JX143390 JX143144 JX142898 JX142652
CBS 570.69; CPC 5075 Nicotiana tabacum Solanaceae Nigeria S.O. Alasoadura DQ835074 DQ835100 DQ835120 DQ835147 DQ835174
Cercospora olivascens CBS 253.67; IMI 124975; CPC 5085 (TYPE) Aristolochia clematidis Aristolochiaceae Romania: Cazanele Dunarii O. Constantinescu JX143632 JX143391 JX143145 JX142899 JX142653
Cercospora cf. physalidis CBS 765.79 Solanum tuberosum Solanaceae Peru L.J. Turkensteen JX143633 JX143392 JX143146 JX142900 JX142654
Cercospora pileicola CBS 132607; CPC 10749 (TYPE) Pilea pumila (= P. mongolica) Urticaceae South Korea: Dongducheon H.D. Shin JX143634 JX143393 JX143147 JX142901 JX142655
CBS 132647; CPC 10693 Pilea hamaoi (≡ P. pumila var. hamaoi) Urticaceae South Korea: Hoengseong H.D. Shin JX143635 JX143394 JX143148 JX142902 JX142656
CPC 11369 Pilea pumila (= P. mongolica) Urticaceae South Korea: Hongcheon H.D. Shin JX143636 JX143395 JX143149 JX142903 JX142657
Cercospora polygonacea CBS 132614; CPC 11318 Persicaria longiseta (≡ P. blumei) Polygonaceae South Korea: Cheongju H.D. Shin JX143637 JX143396 JX143150 JX142904 JX142658
Cercospora punctiformis CBS 132626; CPC 14606 Cynanachum wilfordii Asclepiadaceae South Korea: Bonghwa H.D. Shin JX143638 JX143397 JX143151 JX142905 JX142659
Cercospora cf. resedae CBS 118793 Reseda odorata Resedaceae New Zealand: Auckland C.F. Hill JX143639 JX143398 JX143152 JX142906 JX142660
CBS 257.67; CPC 5057 Helianthemum sp. Cistaceae Romania: Bucuresti O. Constantinescu DQ233319 DQ233343 DQ233369 DQ233395 DQ233421
Cercospora cf. richardiicola CBS 132627; CPC 14680 Ajuga multiflora Lamiaceae South Korea: Incheon H.D. Shin JX143640 JX143399 JX143153 JX142907 JX142661
MUCC 128 Tagetes erecta Asteraceae Japan: Ehime J. Nishikawa JX143641 JX143400 JX143154 JX142908 JX142662
MUCC 132 Osteospermum sp. Asteraceae Japan: Shizuoka J. Nishikawa JX143642 JX143401 JX143155 JX142909 JX142663
MUCC 138 Fuchsia ×hybrida Onagraceae Japan: Shizuoka J. Nishikawa JX143643 JX143402 JX143156 JX142910 JX142664
MUCC 578; MAFF 238210 Zantedeschia sp. Araceae Japan: Ehime J. Nishikawa JX143644 JX143403 JX143157 JX142911 JX142665
MUCC 582; MAFF 238880 Gerbera hybrida Asteraceae Japan: Shizuoka J. Takeuchi JX143645 JX143404 JX143158 JX142912 JX142666
Cercospora ricinella CBS 132605; CPC 10734 Ricinus communis Euphorbiaceae South Korea: Chuncheon H.D. Shin JX143646 JX143405 JX143159 JX142913 JX142667
CPC 10104 Ricinus communis Euphorbiaceae South Korea: Chuncheon H.D. Shin JX143647 JX143406 JX143160 JX142914 JX142668
Cercospora rodmanii CBS 113123; RC3660; 28-1 Eichhornia crassipes Pontederiaceae Brazil: Rio Verde R. Charudattan DQ835076 AF146136 DQ835122 DQ835149 DQ835176
CBS 113124; RC2867 Eichhornia crassipes Pontederiaceae Mexico: Carretero R. Charudattan DQ835077 AF146137 DQ835123 DQ835150 DQ835177
CBS 113125; RC4101; 400 Eichhornia crassipes Pontederiaceae Zambia M. Morris DQ835078 AF146146 DQ835124 DQ835151 DQ835178
CBS 113126; RC3409; 62-2 Eichhornia crassipes Pontederiaceae Brazil: Oroco R. Charudattan DQ835079 AF146138 DQ835125 DQ835152 DQ835179
CBS 113128; RC394; WH83 Eichhornia crassipes Pontederiaceae USA: Florida R. Charudattan DQ835080 AF146142 DQ835126 DQ835153 DQ835180
CBS 113129; RC397; WH9-BR Eichhornia crassipes Pontederiaceae USA: Florida K. Conway DQ835081 AF146143 DQ835127 DQ835154 DQ835181
CBS 113130; RC393; WHK Eichhornia crassipes Pontederiaceae USA: Florida R. Charudattan DQ835082 AF146144 DQ835128 DQ835155 DQ835182
CBS 113131; RC395; WHV Eichhornia crassipes Pontederiaceae Venezuela: Maracay R. Charudattan DQ835083 AF146148 DQ835129 DQ835156 DQ835183
Cercospora rumicis CPC 5439 Rumex sanguineus Polygonaceae New Zealand: Manurewa C.F. Hill JX143648 JX143407 JX143161 JX142915 JX142669
Cercospora senecioniswalkeri CBS 132636; CPC 19196 Senecio walkeri Asteraceae Laos P. Phengsintham JX143649 JX143408 JX143162 JX142916 JX142670
Cercospora cf. sigesbeckiae CBS 132601; CPC 10664 Sigesbeckia glabrescens Asteraceae South Korea: Chuncheon H.D. Shin JX143650 JX143409 JX143163 JX142917 JX142671
CBS 132606; CPC 10740 Paulownia coreana Scrophulariaceae South Korea: Namyangju H.D. Shin JX143651 JX143410 JX143164 JX142918 JX142672
CBS 132621; CPC 14489 Sigesbeckia pubescens Asteraceae South Korea: Yanggu H.D. Shin JX143652 JX143411 JX143165 JX142919 JX142673
CBS 132641; CPC 10117 Persicaria orientalis (= P. cochinchinensis) Polygonaceae South Korea: Chuncheon H.D. Shin JX143653 JX143412 JX143166 JX142920 JX142674
CBS 132642; CPC 10128 Pilea pumila (= P. mongolica) Urticaceae South Korea: Hongcheon H.D. Shin JX143654 JX143413 JX143167 JX142921 JX142675
CBS 132675; CPC 14726 Malva verticillata Malvaceae South Korea: Yanggu H.D. Shin JX143655 JX143414 JX143168 JX142922 JX142676
MUCC 587; MUCNS 197; MAFF 237690 Begonia sp. Begoniaceae Japan: Chiba S. Uematsu JX143656 JX143415 JX143169 JX142923 JX142677
MUCC 589; MAFF 305039 Glycine max Fabaceae Japan: Saitama H. Kurata JX143657 JX143416 JX143170 JX142924 JX142678
MUCC 849 Dioscorea tokoro Dioscoreaceae Japan: Tokyo I. Araki JX143658 JX143417 JX143171 JX142925 JX142679
Cercospora sojina CBS 132018; CPC 12322 Glycine soja Fabaceae South Korea: Hoengseong H.D. Shin GU214655 JX143418 JX143172 JX142926 JX142680
CBS 132615; CPC 11353 (TYPE) Glycine soja Fabaceae South Korea: Hongcheon H.D. Shin JX143659 JX143419 JX143173 JX142927 JX142681
CBS 132684; CPC 17971; CCC 173-09, 09-495 Glycine max Fabaceae Argentina F. Scandiani JX143660 JX143420 JX143174 JX142928 JX142682
CPC 11420 Glycine soja Fabaceae South Korea: Hongcheon H.D. Shin JX143661 JX143421 JX143175 JX142929 JX142683
CPC 17964; CCC 155-09, 09-285-5 Glycine max Fabaceae Argentina F. Scandiani JX143662 JX143422 JX143176 JX142930 JX142684
CPC 17965; CCC 156-09, 09-285-4 Glycine max Fabaceae Argentina F. Scandiani JX143663 JX143423 JX143177 JX142931 JX142685
CPC 17966; CCC 157-09, 09-285-3 Glycine max Fabaceae Argentina F. Scandiani JX143664 JX143424 JX143178 JX142932 JX142686
CPC 17967; CCC 158-09, 09-285-1 Glycine max Fabaceae Argentina F. Scandiani JX143665 JX143425 JX143179 JX142933 JX142687
CPC 17968; CCC 159-09, 09-285-7 Glycine max Fabaceae Argentina F. Scandiani JX143666 JX143426 JX143180 JX142934 JX142688
CPC 17969; CCC 167-09, 09-881 Glycine max Fabaceae Argentina N. Formento JX143667 JX143427 JX143181 JX142935 JX142689
CPC 17970; CCC 172-09, 09-320 Glycine max Fabaceae Argentina F. Scandiani JX143668 JX143428 JX143182 JX142936 JX142690
CPC 17972; CCC 174-09, Glycine max Fabaceae Argentina S. Piubello JX143669 JX143429 JX143183 JX142937 JX142691
CPC 17973; CCC 176-09, 09-882 Glycine max Fabaceae Argentina N. Formento JX143670 JX143430 JX143184 JX142938 JX142692
CPC 17974; CCC 177-09, 09-2488-1 Glycine max Fabaceae Argentina F. Scandiani JX143671 JX143431 JX143185 JX142939 JX142693
CPC 17975; CCC 178-09, 09-1438-2 Glycine max Fabaceae Argentina F. Scandiani JX143672 JX143432 JX143186 JX142940 JX142694
CPC 17976; CCC 179-09, 09-2591 Glycine max Fabaceae Argentina F. Scandiani JX143673 JX143433 JX143187 JX142941 JX142695
CPC 17977; CCC 180-09, 09-2520 Glycine max Fabaceae Argentina F. Scandiani JX143674 JX143434 JX143188 JX142942 JX142696
Cercospora sp. A CBS 132631; CPC 15872 Chenopodium sp. Chenopodiaceae Mexico Ma. de Jesús Yáñez-Morales JX143675 JX143435 JX143189 JX142943 JX142697
Cercospora sp. B CBS 132602; CPC 10687 Ipomoea purpurea Convolvulaceae South Korea: Kangnung H.D. Shin JX143676 JX143436 JX143190 JX142944 JX142698
Cercospora sp. C CBS 132629; CPC 15841 – Compositae Mexico: Montecillo Ma. de Jesús Yáñez-Morales JX143677 JX143437 JX143191 JX142945 JX142699
Cercospora sp. D CBS 132630; CPC 15856 – – Mexico Ma. de Jesús Yáñez-Morales JX143678 JX143438 JX143192 JX142946 JX142700
Cercospora sp. E CBS 132628; CPC 15632 Unidentified wild plant – Mexico: Montecillo Ma. de Jesús Yáñez-Morales JX143679 JX143439 JX143193 JX142947 JX142701
CPC 15801 Unidentified wild plant – Mexico: Montecillo Ma. de Jesús Yáñez-Morales JX143680 JX143440 JX143194 JX142948 JX142702
Cercospora sp. F CBS 132618; CPC 12062 Zea mays Poaceae South Africa P. Caldwell DQ185071 DQ185083 DQ185095 DQ185107 DQ185119
Cercospora sp. G CBS 115518; CPC 5360 Bidens frondosa Asteraceae New Zealand: Kopuku C.F. Hill JX143681 JX143441 JX143195 JX142949 JX142703
CPC 5438 Salvia viscosa Lamiaceae New Zealand: Manurewa C.F. Hill JX143682 JX143442 JX143196 JX142950 JX142704
Cercospora sp. H CBS 115205; CPC 5116 Dichondra repens Convolvulaceae New Zealand C.F. Hill JX143683 JX143443 JX143197 JX142951 JX142705
CPC 11620 Chamelaucium uncinatum Myrtaceae Argentina S. Wolcan JX143684 JX143444 JX143198 JX142952 JX142706
Cercospora sp. I CBS 114815; CPC 5364 Deutzia purpurascens Hydrangeaceae New Zealand: Manurewa C.F. Hill JX143685 JX143445 JX143199 JX142953 JX142707
CBS 114816; CPC 5363 Deutzia ×rosea (= D. gracilis × purpurascens) Hydrangeaceae New Zealand: Manurewa C.F. Hill JX143686 JX143446 JX143200 JX142954 JX142708
CBS 114817; CPC 5365 Fuchsia procumbens Onagraceae New Zealand: Manurewa C.F. Hill JX143687 JX143447 JX143201 JX142955 JX142709
CBS 114818; CPC 5362 Deutzia crenata Hydrangeaceae New Zealand: Manurewa C.F. Hill JX143688 JX143448 JX143202 JX142956 JX142710
CBS 115117 Archontophoenix cunninghamiana Arecaceae (Palmae) New Zealand: Whangarei C.F. Hill JX143689 JX143449 JX143203 JX142957 JX142711
CBS 115121 Gunnera tinctoria Gunneraceae New Zealand: Mt Albert C.F. Hill JX143690 JX143450 JX143204 JX142958 JX142712
CBS 132597; CPC 10615 Coreopsis verticillata Asteraceae New Zealand: Manurewa C.F. Hill JX143691 JX143451 JX143205 JX142959 JX142713
CBS 132643; CPC 10138 Ajuga multiflora Lamiaceae South Korea: Suwon H.D. Shin JX143692 JX143452 JX143206 JX142960 JX142714
CPC 10616 Coreopsis verticillata Asteraceae New Zealand: Manurewa C.F. Hill JX143693 JX143453 JX143207 JX142961 JX142715
CPC 5440 Nicotiana sp. Solanaceae New Zealand: Manurewa C.F. Hill JX143694 JX143454 JX143208 JX142962 JX142716
Cercospora sp. J MUCC 541 Antirrhinum majus Plantaginaceae Japan: Aichi M.Matsusaki JX143695 JX143455 JX143209 JX142963 JX142717
Cercospora sp. K CBS 132603; CPC 10719 Ipomoea coccinea (≡ Quamoclit coccinea) Convolvulaceae South Korea: Namyangju H.D. Shin JX143696 JX143456 JX143210 JX142964 JX142718
CPC 10094 Ipomoea coccinea (≡ Quamoclit coccinea) Convolvulaceae South Korea: Namyangju H.D. Shin JX143697 JX143457 JX143211 JX142965 JX142719
CPC 12391 Ipomoea coccinea (≡ Quamoclit coccinea) Convolvulaceae South Korea: Namyangju H.D. Shin JX143698 JX143458 JX143212 JX142966 JX142720
Cercospora sp. L CBS 115477; CPC 5114 Crepis capillaris Asteraceae New Zealand C.F. Hill JX143699 JX143459 JX143213 JX142967 JX142721
Cercospora sp. M CBS 132596; CPC 10553 Acacia mangium Fabaceae Thailand: Sanamchaikhet K. Pongpanich JX143700 AY752175 AY752203 AY752234 AY752265
Cercospora sp. N CBS 132619; CPC 12684 Musa sp. Musaceae Bangladesh: Western I. Buddenhagen EU514224 JX143460 JX143214 JX142968 JX142722
Cercospora sp. O CBS 132635; CPC 18636 Musa sp. Musaceae Thailand: Mae Klang Loung P.W. Crous JX143701 JX143461 JX143215 JX142969 JX142723
Cercospora sp. P CBS 112649; CPC 3946 Citrus sp., leaf spot Rutaceae Swaziland M.C. Pretorius AY260072 DQ835090 DQ835109 DQ835136 DQ835163
CBS 112722; CPC 3947 Citrus sp., leaf spot Rutaceae Swaziland M.C. Pretorius AY260073 DQ835091 DQ835110 DQ835137 DQ835164
CBS 112728; CPC 3949 Citrus × sinensis (≡ C. aurantium var. sinensis) Rutaceae South Africa: Komatipoort M.C. Pretorius AY260076 DQ835092 DQ835111 DQ835138 DQ835165
CBS 112730; CPC 3948 Citrus × sinensis (≡ C. aurantium var. sinensis) Rutaceae South Africa: Komatipoort M.C. Pretorius AY260075 DQ835093 DQ835112 DQ835139 DQ835166
CBS 112894; CPC 3950 Citrus × sinensis (≡ C. aurantium var. sinensis) Rutaceae South Africa: Komatipoort M.C. Pretorius AY260077 DQ835094 DQ835113 DQ835140 DQ835167
CBS 113996; CPC 5326 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143702 JX143462 JX143216 JX142970 JX142724
CBS 115413; CPC 5328 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143703 JX143463 JX143217 JX142971 JX142725
CBS 115609; CPC 3945 Citrus sp., leaf spot Rutaceae Swaziland M.C. Pretorius AY260074 DQ835096 DQ835115 DQ835142 DQ835169
CBS 116365; CPC 10526 (TYPE) Acacia mangium Fabaceae Thailand M.J. Wingfield AY752141 AY752176 AY752204 AY752235 AY752266
CBS 132645; CPC 10527 Acacia mangium Fabaceae Thailand M.J. Wingfield AY752142 AY752177 AY752205 AY752236 AY752267
CBS 132660; CPC 11629; GHA-4-0 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143704 JX143464 JX143218 JX142972 JX142726
CBS 132662; CPC 11635; PNG-009 Dioscorea nummularia Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143705 JX143465 JX143219 JX142973 JX142727
CBS 132664; CPC 11637; PNG-022 Dioscorea rotundata Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143706 JX143466 JX143220 JX142974 JX142728
CBS 132665; CPC 11638; PNG-023 Dioscorea bulbifera Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143707 JX143467 JX143221 JX142975 JX142729
CBS 132680; CPC 15827 Ricinus communis Euphorbiaceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143708 JX143468 JX143222 JX142976 JX142730
CPC 10552 Acacia mangium Fabaceae Thailand K. Pongpanich JX143709 AY752174 AY752202 AY752233 AY752264
CPC 11630; GHA-4-3 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143710 JX143469 JX143223 JX142977 JX142731
CPC 11631; GHA-5-0 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143711 JX143470 JX143224 JX142978 JX142732
CPC 11632; GHA-7-4 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143712 JX143471 JX143225 JX142979 JX142733
CPC 11633; GHA-8-4 Dioscorea rotundata Dioscoreaceae Ghana S. Nyako & A.O. Danquah JX143713 JX143472 JX143226 JX142980 JX142734
CPC 4001 Citrus ×sinensis (≡ C. aurantium var. sinensis) Rutaceae Swaziland M.C. Pretorius AY343372 AY343335 DQ835116 DQ835143 DQ835170
CPC 4002 Citrus ×sinensis (≡ C. aurantium var. sinensis) Rutaceae Swaziland M.C. Pretorius DQ835072 DQ835097 DQ835117 DQ835144 DQ835171
CPC 5262 Hibiscus sabdariffa Malvaceae New Zealand: Auckland (imported from Fiji) C.F. Hill JX143714 JX143473 JX143227 JX142981 JX142735
CPC 5327 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143715 JX143474 JX143228 JX142982 JX142736
MUCC 771 Coffea arabica Rubiaceae Japan: Okinawa C. Nakashima JX143716 JX143475 JX143229 JX142983 JX142737
Cercospora sp. Q CBS 113997; CPC 5325 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143717 JX143476 JX143230 JX142984 JX142738
CBS 115410; CPC 5331 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143718 JX143477 JX143231 JX142985 JX142739
CBS 115411; CPC 5332 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143719 JX143478 JX143232 JX142986 JX142740
CBS 115412; CPC 5333 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143720 JX143479 JX143233 JX142987 JX142741
CBS 115536; CPC 5329 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143721 JX143480 JX143234 JX142988 JX142742
CBS 115537; CPC 5330 Cajanus cajan Fabaceae South Africa: Nelspruit L. van Jaarsveld JX143722 JX143481 JX143235 JX142989 JX142743
CBS 132656; CPC 11536 Acacia mangium Fabaceae Thailand K. Pongpanich JX143723 JX143482 JX143236 JX142990 JX142744
CBS 132661; CPC 11634; PNG-002 Dioscorea rotundata Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143724 JX143483 JX143237 JX142991 JX142745
CBS 132663; CPC 11636; PNG-016 Dioscorea esculenta Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143725 JX143484 JX143238 JX142992 JX142746
CBS 132679; CPC 15807 Phaseolus vulgaris Fabaceae Mexico Ma. de Jesús Yáñez-Morales JX143726 JX143485 JX143239 JX142993 JX142747
CBS 132681; CPC 15844 Euphorbia sp. Euphorbiaceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143727 JX143486 JX143240 JX142994 JX142748
CBS 132682; CPC 15850 Taraxacum sp. Asteraceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143728 JX143487 JX143241 JX142995 JX142749
CPC 10550 Acacia mangium Fabaceae Thailand K. Pongpanich AY752139 AY752172 AY752200 AY752231 AY752262
CPC 10551 Acacia mangium Fabaceae Thailand K. Pongpanich AY752140 AY752173 AY752201 AY752232 AY752263
CPC 11539 Acacia mangium Fabaceae Thailand K. Pongpanich JX143729 JX143488 JX143242 JX142996 JX142750
CPC 11639; PNG-037 Dioscorea rotundata Dioscoreaceae Papua New Guinea J. Peters & A.N. Jama JX143730 JX143489 JX143243 JX142997 JX142751
CPC 15875 Euphorbia sp. Euphorbiaceae Mexico: Tamaulipas Ma. de Jesús Yáñez-Morales JX143731 JX143490 JX143244 JX142998 JX142752
Cercospora sp. R CBS 114644 Myoporum laetum Myoporaceae New Zealand: Grey Lynn C.F. Hill JX143732 JX143491 JX143245 JX142999 JX142753
Cercospora sp. S CBS 132599; CPC 10656 Crepidiastrum denticulatum (≡ Youngia denticulata) Asteraceae South Korea: Yangpyeong H.D. Shin JX143733 JX143492 JX143246 JX143000 JX142754
Cercospora vignigena CBS 132611; CPC 10812 (TYPE) Vigna unguiculata (= V. sinensis) Fabaceae South Korea: Jeongeup H.D. Shin JX143734 JX143493 JX143247 JX143001 JX142755
CPC 1134 Vigna unguiculata (= V. sinensis) Fabaceae South Africa: Potchefstroom S. van Wyk JX143735 JX143494 JX143248 JX143002 JX142756
MUCC 579; MAFF 237635 Vigna unguiculata (= V. sinensis) Fabaceae Japan: Gumma K. Kishi JX143736 JX143495 JX143249 JX143003 JX142757
Cercospora violae CBS 251.67; CPC 5079 (TYPE) Viola tricolor Violaceae Romania: Cazanele Dunarii O. Constantinescu JX143737 JX143496 JX143250 JX143004 JX142758
CPC 5368 Viola odorata Violaceae New Zealand C.F. Hill JX143738 JX143497 JX143251 JX143005 JX142759
MUCC 129 Viola sp. Violaceae Japan: Kochi J. Nishikawa JX143739 JX143498 JX143252 JX143006 JX142760
MUCC 133 Viola tricolor Violaceae Japan: Nagano J. Nishikawa JX143740 JX143499 JX143253 JX143007 JX142761
MUCC 136 Viola tricolor Violaceae Japan: Shizuoka J. Nishikawa JX143741 JX143500 JX143254 JX143008 JX142762
Cercospora zeae-maydis CBS 117755; YA-03; A358 Zea mays Poaceae USA: Indiana B. Fleener DQ185072 DQ185084 DQ185096 DQ185108 DQ185120
CBS 117756; DE-97; A359 Zea mays Poaceae USA: Indiana B. Fleener DQ185073 DQ185085 DQ185097 DQ185109 DQ185121
CBS 117757; JV-WI-02; A360 (TYPE) Zea mays Poaceae USA: Wisconsin B. Fleener DQ185074 DQ185086 DQ185098 DQ185110 DQ185122
CBS 117758; JH-IA-04; A361 Zea mays Poaceae USA: Iowa B. Fleener DQ185075 DQ185087 DQ185099 DQ185111 DQ185123
CBS 117759; UC-TN-99; A362 Zea mays Poaceae USA: Tennessee B. Fleener DQ185076 DQ185088 DQ185100 DQ185112 DQ185124
CBS 117760; NH-PA-99; A363 Zea mays Poaceae USA: Pennsylvania B. Fleener DQ185077 DQ185089 DQ185101 DQ185113 DQ185125
CBS 117761; PR-IN-99; A364 Zea mays Poaceae USA: Indiana B. Fleener DQ185078 DQ185090 DQ185102 DQ185114 DQ185126
CBS 117762; DEXTER-MO-00; A365 Zea mays Poaceae USA: Missouri B. Fleener DQ185079 DQ185091 DQ185103 DQ185115 DQ185127
CBS 117763; RENBECK-IA-99; A367 Zea mays Poaceae USA: Iowa B. Fleener DQ185080 DQ185092 DQ185104 DQ185116 DQ185128
CBS 132668; CPC 12225; CHME 52 Zea mays Poaceae China: Liaoning Province – JX143742 JX143501 JX143255 JX143009 JX142763
CBS 132678; CPC 15602 Zea mays Poaceae Mexico: Tlacotepec Ma. de Jesús Yáñez-Morales JX143743 JX143502 JX143256 JX143010 JX142764
Cercospora zebrina CBS 108.22; CPC 5091 Medicago arabica (= M. maculata) Fabaceae – E.F. Hopkins JX143744 JX143503 JX143257 JX143011 JX142765
CBS 112723; CPC 3957 Trifolium repens Fabaceae Canada: Ottawa K.A. Seifert AY260079 JX143504 JX143258 JX143012 JX142766
CBS 112736; CPC 3958 Trifolium repens Fabaceae Canada: Ottawa K.A. Seifert AY260080 JX143505 JX143259 JX143013 JX142767
CBS 112893; CPC 3955 Trifolium pratense Fabaceae Canada: Ottawa K.A. Seifert AY260078 JX143506 JX143260 JX143014 JX142768
CBS 113070; CPC 5367 Trifolium repens Fabaceae New Zealand: Blockhouse Bay C.F. Hill JX143745 JX143507 JX143261 JX143015 JX142769
CBS 114359; CPC 10901 Hebe sp. Scrophulariaceae New Zealand C.F. Hill JX143746 JX143508 JX143262 JX143016 JX142770
CBS 118789; WAC 5106 Trifolium subterraneum Fabaceae Australia M.J. Barbetti JX143747 JX143509 JX143263 JX143017 JX142771
CBS 118790; IMI 262766; WA 2030; WAC 7973 Trifolium subterraneum Fabaceae Australia M.J. Barbetti JX143748 JX143510 JX143264 JX143018 JX142772
CBS 118791; IMI 264190; WA2054; WAC7993 Trifolium cernuum Fabaceae Australia M.J. Barbetti JX143749 JX143511 JX143265 JX143019 JX142773
CBS 129.39; CPC 5078 Trifolium subterraneum Fabaceae USA: Wisconsin – JX143750 JX143512 JX143266 JX143020 JX142774
CBS 132650; CPC 10756 Trifolium repens Fabaceae South Korea: Namyangju H.D. Shin JX143751 JX143513 JX143267 JX143021 JX142775
CBS 137.56; CPC 5118 Hedysarum coronarium Fabaceae Italy – JX143752 JX143514 JX143268 JX143022 JX142776
CBS 537.71; IMI 161108; CPC 5089 Astragalus spruneri Fabaceae Romania: Hagieni O. Constantinescu JX143753 JX143515 JX143269 JX143023 JX142777
CPC 5437 Lotus pedunculatus Fabaceae New Zealand: Auckland C.F. Hill JX143754 JX143516 JX143270 JX143024 JX142778
CPC 5473 Jacaranda mimosifolia Bignoniaceae New Zealand C.F. Hill JX143755 JX143517 JX143271 JX143025 JX142779
Cercospora zeina CBS 118820; CPC 11995 (TYPE) Zea mays Poaceae South Africa: Pietermaritzburg P. Caldwell DQ185081 DQ185093 DQ185105 DQ185117 DQ185129
CBS 132617; CPC 11998 Zea mays Poaceae South Africa: Pietermaritzburg P. Caldwell DQ185082 DQ185094 DQ185106 DQ185118 DQ185130
Cercospora cf. zinniae CBS 132624; CPC 14549 Zinnia elegans Asteraceae South Korea: Yangpyeong H.D. Shin JX143756 JX143518 JX143272 JX143026 JX142780
CBS 132676; CPC 15075 – – Brazil: Valverde A.C. Alfenas JX143757 JX143519 JX143273 JX143027 JX142781
MUCC 131 Zinnia elegans Asteraceae Japan: Shizuoka J. Nishikawa JX143758 JX143520 JX143274 JX143028 JX142782
MUCC 572; MUCNS 215; MAFF 237718 Zinnia elegans Asteraceae Japan: Chiba S. Uematsu JX143759 JX143521 JX143275 JX143029 JX142783
Septoria provencialis CBS 118910; CPC 12226 Eucalyptus sp. Myrtaceae France P.W. Crous DQ303096 JX143522 JX143276 JX143030 JX142784
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CBS: CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands; CPC: Culture collection of Pedro Crous, housed at CBS; IHEM: Collection of the Laboratorium voor Microbiologie en Microbiele Genetica, Rijksuniversiteit, Ledeganckstraat 35, B-9000, Gent, Belgium; IMI: International Mycological Institute, CABI-Bioscience, Egham, Bakeham Lane, U.K.; Lynfield: Private culture collection and herbarium of Frank Hill, New Zealand; MAFF: Ministry of Agticulture, Forestry and Fisheries, Tsukuba, Ibaraki, Japan; MUCC: Culture Collection, Laboratory of Plant Pathology, Mie University, Tsu, Mie Prefecture, Japan; MUCL: Université Catholique de Louvain, Louvain-la-Neuve, Belgium; MUCNS: Active cultures & specimens of Chiharu Nakashima, housed at Mie University; MUMH: Mycologicl Herbarium of Mie University, Tsu, Mie, Japan; PPRI: Plant Protection Research Institute, Pretoria, South Africa; WAC: Department of Agriculture Western Australia Plant Pathogen Collection, Perth, Australia.

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ITS: internal transcribed spacers and intervening 5.8S nrDNA; TEF: translation elongation factor 1-alpha; ACT: actin; CAL: calmodulin; HIS: histone H3.

DNA extraction, amplification and phylogeny

Genomic DNA was isolated from fungal mycelium grown on the agar plates following the protocol of Lee & Taylor (1990) or the UltraClean™ Microbial DNA Isolation Kit (Mo Bio Laboratories, Inc., Solana Beach, CA, USA). All isolates were sequenced with five genomic loci. The primers ITS5 or ITS1 and ITS4 (White et al. 1990) were used to amplify the internal transcribed spacers areas as well as the 5.8S rRNA gene (ITS) of the nrDNA operon. Part of the actin gene (ACT) was amplified using the primer set ACT-512F and ACT-783R (Carbone & Kohn 1999) and part of the translation elongation factor 1-a gene (EF) using the primer set EF1-728F and EF1-986R (Carbone & Kohn 1999). The primer set CAL-228F and CAL-737R (Carbone & Kohn 1999) was used to amplify part of the calmodulin gene (CAL) whereas the primer set CylH3F and CylH3R (Crous et al. 2004c) was used to amplify part of the histone H3 gene (HIS). Additional degenerate primers were developed from sequences obtained from GenBank as alternative forward and reverse primers for some of the loci during the course of the study (Table 2); however, these were rarely used but based on their degenerate design could be of use to the broader scientific community. The protocols and conditions outlined by Groenewald et al. (2005) were followed for standard amplification and subsequent sequencing of the loci.

Table 2.

Details of primers used and/or developed for this study and their relation to selected published primers. The start and end positions of the primers are derived using the GenBank accession shown next to the locus name as reference in the 5’-3’ direction. See Crous et al. (2009a) for information on additional ITS primers.

Name Sequence (5’ - 3’) Orientation %GC %GC Tm (°C) Start End Reference
Actin (Hypocrea orientalis GenBank accession JQ238613)
ACT-512F ATG TGC AAG GCC GGT TTC GC Forward 60.0 51.4 244 263 Carbone & Kohn (1999)
ACT-783R TAC GAG TCC TTC TGG CCC AT Reverse 55.0 47.6 544 563 Carbone & Kohn (1999)
ACT1Fd GCY GCB CTC GTY ATY GAC AAT GG Forward 57.2 45.7 - 50.6 - 54.7 16 38 This study, see also Aveskamp et al. (2009)
ACT1Rd CRT CGT ACT CCT GCT TBG AGA TCC AC Reverse 54.5 48.3 - 50.3 - 51.8 1537 1562 This study
ACT2Fd GTA TCG TBC TBG ACT CYG GTG AYG GTG Forward 56.8 48.1 - 52.2 - 55.4 854 880 This study
ACT2Rd ARR TCR CGD CCR GCC ATG TC Reverse 61.7 45.1 - 50.9 - 58.1 940 956 This study, see also Quaedvlieg et al. (2011)
Beta-tubulin (Gibberella zeae GenBank accession FJ214662)
Bt1a TTC CCC CGT CTC CAC TTC TTC ATG Forward 54.2 50.1 1091 1114 Glass & Donaldson (1995)
Bt1b GAC GAG ATC GTT CAT GTT GAA CTC Reverse 45.8 45.1 1603 1626 Glass & Donaldson (1995)
Bt2a GGT AAC CAA ATC GGT GCT GCT TTC Forward 50.0 48.2 163 186 Glass & Donaldson (1995)
Bt2b ACC CTC AGT GTA GTG ACC CTT GGC Reverse 58.0 52.1 617 640 Glass & Donaldson (1995)
CYLTUB1F AAA TTG GTG CTG CTT TCT GG Forward 45.0 43.5 170 189 This study
CYLTUB1R AGT TGT CGG GAC GGA AGA G Reverse 57.9 46.6 563 581 Crous et al. (2004c)
T1 AAC ATG CGT GAG ATT GTA AGT Forward 38.1 41.5 1 17 O’Donnell & Cigelnik (1997)
TUB1Fd CAN MAT GMG KGA RAT CGT RGT Forward 47.6 36.8 - 44.5 - 51.9 1 14 This study
TUB1Rd RGC VTC YTG GTA YTG CTG GTA Reverse 53.2 43.2 - 47.4 - 51.0 1633 1652 This study
TUB2Fd GTB CAC CTY CAR ACC GGY CAR TG Forward 59.4 46.1 - 51.4 - 56.4 74 96 This study
TUB2Rd TCA CCA GTG TAC CAA TGM ARG AAA GCC Reverse 48.1 48.3 - 50.1 - 52.0 1545 1565 This study
TUB3Fd AAA THG GTG CYG CHT TCT GG Forward 50.8 42.5 - 45.9 - 50.5 170 189 This study
TUB3Rd TCV GWG TTS AGY TGA CCN GGG Reverse 60.3 46.1 - 50.5 -54.0 1039 1059 This study
TUB4Fd GGH GCY GGH AAC AAC TGG GC Forward 65.8 48.3 - 52.2 - 57.7 600 618 This study
TUB4Rd CCR GAY TGR CCR AAR ACR AAG TTG TC Reverse 50.0 44.4 - 49.4 - 54.4 581 606 This study
Calmodulin (Colletotrichum gloeosporioides GenBank accession HM575363)
CAL-228F GAG TTC AAG GAG GCC TTC TCC C Forward 59.1 49.2 2 23 Carbone & Kohn (1999)
CAL-737R CAT CTT TCT GGC CAT CAT GG Reverse 50.0 43.4 439 458 Carbone & Kohn (1999)
CAL1Rd GCA TCA TRA GYT RGA CRA ACT CG Reverse 47.8 41.0 - 45.4 - 49.7 747 769 This study
CAL2Rd TGR TCN GCC TCD CGG ATC ATC TC Reverse 58.0 47.5 - 50.8 - 54.9 647 669 This study
Histone H3 (Talaromyces stipitatus GenBank accession XM_002478391)
CYLH3F AGG TCC ACT GGT GGC AAG Forward 61.1 47.6 28 45 Crous et al. (2004c)
CYLH3R AGC TGG ATG TCC TTG GAC TG Reverse 55.0 46.6 361 380 Crous et al. (2004c)
H3-1a ACT AAG CAG ACC GCC CGC AGG Forward 66.7 54.2 10 30 Glass & Donaldson (1995)
H3-1b GCG GGC GAG CTG GAT GTC CTT Reverse 66.7 54.5 367 387 Glass & Donaldson (1995)
HIS1Rd RCG RAG RCG ACG GGC Reverse 76.7 45.4 - 50.0 - 54.6 382 396 This study
HIS2Rd GGA TGG TRA CAC GCT TRG CGT G Reverse 59.1 47.9 - 50.5 - 53.1 240 361 This study
ITS (Magnaporthe grisea GenBank accession AB026819)
ITS1 TCC GTA GGT GAA CCT GCG G Forward 63.2 49.5 2162 2180 White et al. (1990)
ITS4 TCC TCC GCT TAT TGA TAT GC Reverse 45.0 41.6 2685 2704 White et al. (1990)
ITS5 GGA AGT AAA AGT CGT AAC AAG G Forward 40.9 40.8 2138 2159 White et al. (1990)
V9G TTA CGT CCC TGC CCT TTG TA Forward 45.0 42.8 2002 2021 de Hoog & Gerrits van den Ende (1998)
Translation elongation factor 1-alpha (Sordaria macrospora GenBank accession X96615)
CylEF-R2 CAT GTT CTT GAT GAA RTC ACG Reverse 40.5 39.2 - 40.2 - 41.1 783 803 Crous et al. (2004c)
EF-1 ATG GGT AAG GAR GAC AAG AC Forward 47.5 41.2 - 42.3 - 43.4 190 209 O’Donnell et al. (1998)
EF-2 GGA RGT ACC AGT SAT CAT GTT Reverse 45.2 41.6 - 42.6 -43.7 798 818 O’Donnell et al. (1998)
EF-22 AGG AAC CCT TAC CGA GCT C Reverse 57.9 46.2 578 596 O’Donnell et al. (1998)
EF1-1567R ACH GTR CCR ATA CCA CCR ATC TT Reverse 47.1 43.1 - 47.2 - 52.0 1254 1276 Designed by S. Rehner (www.aftol.org/pdfs/EF1primer.pdf)
Translation elongation factor 1-alpha (Sordaria macrospora GenBank accession X96615)
EF1-2218R ATG ACA CCR ACR GCR ACR GTY TG Reverse 54.3 45.6 - 50.4 - 55.1 1782 1804 Designed by S. Rehner (www.aftol.org/pdfs/EF1primer.pdf)
EF1-526F GTC GTY GTY ATY GGH CAY GT Forward 51.7 40.0 - 45.6 - 52.2 220 239 Designed by S. Rehner (www.aftol.org/pdfs/EF1primer.pdf)
EF1-728F CAT CGA GAA GTT CGA GAA GG Forward 50.0 42.2 306 325 Carbone & Kohn (1999)
EF1-986R TAC TTG AAG GAA CCC TTA CC Reverse 45.0 40.9 584 603 Carbone & Kohn (1999)
EF1Fd GTC GTT ATC GGC CAC GTC G Forward 63.2 48.5 223 241 This study
EF1Rd CGG MCT TGG TGA CCT TGC C Reverse 65.8 48.8 - 50.4 - 52.0 1836 1852 This study
EF2Fd GAT CTA CCA GTG CGG TGG Forward 61.1 45.4 273 290 This study
EF2Rd GGT GCA TYT CSA CGG ACT TGA C Reverse 56.8 48.2 - 49.1 - 49.9 1356 1377 This study
EF3Fd GAG CGT GAG CGT GGT ATC AC Forward 60.0 48.1 632 651 This study
EF3Rd GGT ACG CTK GTC RAT ACC ACC Reverse 57.1 45.5 - 47.5 - 49.6 286 306 This study
EF4Fd GGT GCA TYT CSA CGG ACT TGA C Forward 56.8 48.2 - 49.1 - 49.9 1356 1377 This study
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Sequences of Septoria provencialis (isolate CPC 12226) were used as outgroup based on availability and phylogenetic relationship with Cercospora (Crous et al. 2004b, 2006b). The Cercospora sequences were assembled and added to the outgroup sequences using Sequence Alignment Editor v. 2.0a11 (Rambaut 2002), and manual adjustments for improvement were made by eye where necessary. Gaps present in the ingroup taxa and longer than 10 characters were coded as a single event for all analyses (see TreeBASE).

Neighbour-joining analyses using the HKY85 substitution model were applied to each data partition individually to check the stability and robustness of each species clade under each data set using PAUP v. 4.0b10 (Swofford 2003) (data not shown, discussed under the species notes where applicable). Alignment gaps were treated as missing data and all characters were unordered and of equal weight. Any ties were broken randomly when encountered. The robustness of the trees obtained was evaluated by 1 000 bootstrap replications (Hillis & Bull 1993).

MrModeltest v. 2.2 (Nylander 2004) was used to determine the best nucleotide substitution model settings for each data partition. Based on the results of the MrModeltest, a model-optimised phylogenetic re-construction was performed for the aligned combined data set to determine species relationships using MrBayes v. 3.2.0 (Ronquist & Huelsenbeck 2003). The heating parameter was set at 0.3 and the Markov Chain Monte Carlo (MCMC) analysis of four chains was started in parallel from a random tree topology and lasted until the average standard deviation of split frequencies came below 0.05. Trees were saved each 1 000 generations and the resulting phylogenetic tree was printed with Geneious v. 5.5.4 (Drummond et al. 2011). New sequences generated in this study were deposited in NCBI’s GenBank nucleotide database (www.ncbi.nlm.nih.gov; Table 1) and the alignment and phylogenetic tree in TreeBASE (www.treebase.org).

Isolates of Cercospora sp. Q were screened with five more loci to test whether additional loci could distinguish cryptic taxa within this species. This species was selected based on the intraspecific variation present in Fig. 2 (part 5) and also the range of host species and countries represented. The primer set GDF1 and GDR1 (Guerber et al. 2003) was used to amplify part of the glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene, primer set NMS1 and NMS2 (Li et al. 1994) for part of the mitochondrial small subunit rRNA gene and part of the chitin synthase (CHS) gene was amplified using the primers CHS-79F and CHS-354R (Carbone & Kohn 1999). Part of the gene encoding for a mini-chromosome maintenance protein (MCM7) was amplified using primers Mcm7-709for, Mcm7-1348rev, Mcm7-1447rev (Schmitt et al. 2009) and part of the beta-tubulin gene using mainly the primers T1, Bt2b and TUB3Rd (see Table 2 for references).

Fig. 2.

Fig. 2.

Fig. 2.

Fig. 2.

Fig. 2.

Fig. 2.

Fig. 2.

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(Part 1). Consensus phylogram (50 % majority rule) of 5 994 trees resulting from a Bayesian analysis of the combined 5-gene sequence alignment using MrBayes v. 3.2.0. Bayesian posterior probabilities are indicated with colour-coded branches and numbers (see legend) and the scale bar represents the expected changes per site. Species clades are indicated in coloured blocks and species names in black text. Hosts and countries of origin are indicated in green and blue text, respectively. The tree was rooted to Septoria provencialis (strain CPC 12226).

Taxonomy

Morphological descriptions are based on structures in vivo, with morphological structures in vitro noted where relevant. Structures were mounted in clear lactic acid, and 30 measurements (× 1 000 magnification) determined wherever possible, with the extremes of spore measurements given in parentheses. Observations were made with a Zeiss V20 Discovery stereo-microscope, and with a Zeiss Axio Imager 2 light microscope using differential interference contrast (DIC) illumination and an AxioCam MRc5 camera and software. Colony colours (surface and reverse) were assessed on different culture media at 25 °C in the dark, using the colour charts of Rayner (1970). All isolates obtained in this study are maintained in culture collections (Table 1). Nomenclatural novelties and descriptions were deposited in MycoBank (www.MycoBank.org; Crous et al. 2004a).

RESULTS

DNA phylogeny

Amplification products and gene sequences of similar size to that reported previously (Groenewald et al. 2005, 2010a) were obtained. The resulting concatenated alignment contains 361 taxa (including the outgroup taxon), and 471, 263, 199, 240 and 347 characters (including alignment gaps) were used in the ITS, TEF, ACT, CAL and HIS partitions, respectively. Based on the results of MrModeltest, the following priors were set in MrBayes for the different partitions: all partitions had dirichlet base frequencies and GTR+G models with gamma-distributed rates were implemented for ITS, ACT and CAL, and HKY+G with gamma-distributed rates for TEF while HIS required HKY+I+G with inverse gamma-distributed rates. The final aligned combined data set contained 361 ingroup taxa with a total of 1 305 characters and Septoria provencialis (isolate CPC 12226) served as the outgroup taxon. From this alignment 1 520 characters were used for the Bayesian analysis; these contained 588 unique site patterns (48, 172, 111, 125 and 132 for ITS, TEF, ACT, CAL and HIS, respectively). The Bayesian analysis lasted 3 995 000 generations and the consensus trees and posterior probabilities were calculated from the 5 994 trees left after discarding 1 998 trees (the first 1 000 generations) for burn-in (Fig. 2).

The ITS region has limited resolution for almost all species in Cercospora and therefore the results of the other gene regions were particularly useful for comparison of clade stability. Neighbour-joining analyses using the HKY85 substitution model were applied to each data partition to check the stability and robustness of each species clade under the different partitions (data not shown). The ITS region was only able to distinguish C. zeina and C. zeae-maydis from the rest of the included species. The TEF region was able to distinguish 33 of the 73 species clades and especially failed for Cercospora sp. M-Q (including C. cf. sigesbeckiae and C. cf. richardiicola; spanning most of Fig. 2 part 4 and the upper half of part 5), whereas ACT distinguished 43 of the 73 species clades and especially failed for Cercospora sp. G-I (Fig. 2 part 1) and including C. cf. flagellaris and C. alchemillicola/C. cf. alchemillicola. The ACT region also accounted for most of the variation observed for Cercospora sp. Q. The CAL region was able to distinguish 34 of the 73 species clades but especially failed for Cercospora sp. M, P and Q (including C. kikuchii, C. cf. sigesbeckiae, C. cf. richardiicola and C. rodmanii; spanning middle of Fig. 2 part 4), as well as a group consisting predominantly of C. armoraciae, C. capsici, C. zebrina and C. violae (Fig. 2 part 3). Although the locus was able to separate C. beticola and C. apii, it could not distinguish C. cf. brunkii and C. cf. resedae from C. apii. The HIS region distinguished 46 of the 73 species clades and especially failed for Cercospora sp. G-I (Fig. 2 part 1) and Cercospora sp. M, P and Q (including C. kikuchii, C. cf. richardiicola and C. rodmanii; spanning middle of Fig. 2 part 4). The HIS region also accounted for most of the variation observed for C. armoraciae and was responsible for the split of C. beticola into two clades. No single gene region was found which could reliably distinguish all species and, irrespective of which locus was used, occurrences of the same sequence(s) shared between multiple species were observed. If data for ITS is not taken into consideration, the remaining four loci always distinguish the following 18 species: C. agavicola, C. apiicola, C. coniogramme, C. cf. erysimi, C. euphorbiae-sieboldianae, C. helianthicola, C. mercurialis, C. olivascens, C. pileicola, C. senecionis-walkeri, C. violae, C. zeae-maydis, C. zeina, Cercospora sp. A, Cercospora sp. C, Cercospora sp. D, Cercospora sp. J, Cercospora sp. R. Some species are only distinguished based on a single locus and these results are discussed under the species notes, where applicable.

Evaluation of additional loci

Isolates of Cercospora sp. Q were compared using the five loci used for the combined phylogeny and five additional loci as explained in the Materials and Methods. The results are summarised in Table 3 and detailed per locus below:

Table 3.

Results from screening Cercospora sp. Q strains with additional loci. The percentage similarity was calculated relative to strain CPC 5325, for which sequences were generated for all loci. The number of nucleotides used for the calculation of the similarity is shown in front of the percentage. For abbreviations of loci see Table 1 and in addition: GAPDH: partial glyceraldehyde-3-phosphate dehydrogenase gene; mtSSU: partial mitochondrial small rRNA gene; CHS: partial chitin synthase gene; TUB: partial beta-tubulin gene; Mcm7: partial gene encoding a mini-chromosome maintenance protein.

Original name Culture accession
number(s)		 Host name Percentage similarity and allele group (I-VI) designation per locus
 GenBank accession numbers
GAPDH mtSSU CHS TUB Mcm7 (GAPDH, mtSSU, CHS, TUB, Mcm7)
Cercospora apii CBS 113997; CPC 5325 Cajanus cajan 979 nt I 573 nt I 299 nt I 597 nt I 501 nt I JX142521, JX142504, JX142487, JX142478, JX142473
Cercospora apii CBS 115410; CPC 5331 Cajanus cajan 966 nt (100 %) I 573 nt (100 %) I 299 nt (100 %) I 597 nt (99 %) I – JX142522, JX142505, JX142488, JX142479, –
Cercospora apii CBS 115411; CPC 5332 Cajanus cajan 966 nt (100 %) I 573 nt (100 %) I 299 nt (100 %) I 597 nt (99 %) III – JX142523, JX142506, JX142489, JX142480, –
Cercospora apii CBS 115412; CPC 5333 Cajanus cajan 966 nt (100 %) I 573 nt (100 %) I 299 nt (100 %) I 322 nt (9,9 %) III – JX142524, JX142507, JX142490, JX142481, –
Cercospora apii CBS 115536; CPC 5329 Cajanus cajan 970 nt (95 %) V 573 nt (100 %) I 299 nt (99 %) II 597 nt (99 %) II – JX142525, JX142508, JX142491, JX142482, –
Cercospora apii CBS 115537; CPC 5330 Cajanus cajan 970 nt (95 %) V 573 nt (100 %) I 299 nt (99 %) II 597 nt (99 %) II – JX142526, JX142509, JX142492, JX142483, –
Cercospora acaciae-mangii CPC 10550 Acacia mangium 979 nt (100 %) I 573 nt (100 %) I 299 nt (99 %) II 450 nt (99 %) I 501 nt (99 %) II JX142533, JX142516, JX142499, JX142484, JX142475
Cercospora acaciae-mangii CPC 10551 Acacia mangium 979 nt (99 %) I 573 nt (100 %) I 299 nt (99 %) II – 501 nt (99 %) III JX142534, JX142517, JX142500, –, JX142476
Cercospora sp. 2 CBS 132656; CPC 11536 Acacia mangium 961 nt (96 %) III 573 nt (100 %) I 299 nt (99 %) II – – JX142527, JX142510, JX142493, –, –
Cercospora sp. 2 CPC 11539 Acacia mangium 958 nt (96 %) III 573 nt (100 %) I 299 nt (99 %) II – – JX142535, JX142518, JX142501, –, –
Cercospora dioscoreaepyrifoliae CBS 132661; CPC 11634; PNG-002 Dioscorea rotundata 970 nt (95 %) VI 573 nt (100 %) I 298 nt (99 %) II – 458 nt (99 %) III JX142528, JX142511, JX142494, –, JX142474
Cercospora dioscoreaepyrifoliae CBS 132663; CPC 11636; PNG-016 Dioscorea esculenta 969 nt (96 %) IV 573 nt (100 %) I 299 nt (99 %) II – – JX142529, JX142512, JX142495, –, –
Cercospora dioscoreaepyrifoliae CPC 11639; PNG-037 Dioscorea rotundata 969 nt (95 %) VI 573 nt (100 %) I 299 nt (99 %) II – – JX142536, JX142519, JX142502, –, –
Cercosporoid CBS 132679; CPC 15807 Phaseolus vulgaris 954 nt (100 %) I 573 nt (100 %) I 299 nt (99 %) III – – JX142530, JX142513, JX142496, –, –
Cercospora sp. CBS 132681; CPC 15844 Euphorbia sp. 956 nt (96 %) III 573 nt (100 %) I 299 nt (99 %) III – – JX142531, JX142514, JX142497, –, –
Cercospora sp. CBS 132682; CPC 15850 Taraxacum sp. 960 nt (100 %) I 573 nt (100 %) I 299 nt (99 %) II – – JX142532, JX142515, JX142498, –, –
Cercospora sp. CPC 15875 Euphorbia sp. 955 nt (99 %) II 573 nt (100 %) I 299 nt (99 %) III 597 nt (99 %) III – JX142537, JX142520, JX142503, JX142485, –
Septoria provencialis (outgroup) CBS 118910; CPC 12226 Eucalyptus sp. 885 nt (87 %) – – 502 nt (82 %) 499 nt (81 %) JX142538, –, –, JX142486, JX142477
Number of identical sequences (excl. outgroup): 6 of 17 17 of 17 4 of 17 0 of 8 0 of 4
Cercospora apii CBS 113997; CPC 5325 Cajanus cajan 481 nt I 306 nt I 221 nt I 312 nt I 378 nt I JX143717, JX143476, JX143230, JX142984, JX142738
Cercospora apii CBS 115410; CPC 5331 Cajanus cajan 481 nt (100 %) I 280 nt (100 %) I 194 nt (100 %) I 280 nt (100 %) I 378 nt (100 %) I JX143718, JX143477, JX143231, JX142985, JX142739
Cercospora apii CBS 115411; CPC 5332 Cajanus cajan 481 nt (100 %) I 280 nt (100 %) I 194 nt (100 %) I 280 nt (100 %) I 378 nt (100 %) I JX143719, JX143478, JX143232, JX142986, JX142740
Cercospora apii CBS 115412; CPC 5333 Cajanus cajan 481 nt (100 %) I 280 nt (100 %) I 194 nt (100 %) I 280 nt (100 %) I 378 nt (100 %) I JX143720, JX143479, JX143233, JX142987, JX142741
Cercospora apii CBS 115536; CPC 5329 Cajanus cajan 481 nt (100 %) I 280 nt (100 %) I 194 nt (100 %) I 278 nt (100 %) I 378 nt (98 %) III JX143721, JX143480, JX143234, JX142988, JX142742
Cercospora apii CBS 115537; CPC 5330 Cajanus cajan 481 nt (100 %) I 280 nt (100 %) I 194 nt (100 %) I 280 nt (100 %) I 378 nt (98 %) III JX143722, JX143481, JX143235, JX142989, JX142743
Cercospora acaciae-mangii CPC 10550 Acacia mangium 481 nt (99 %) II 306 nt (100 %) I 221 nt (99 %) II 312 nt (100 %) I 377 nt (99 %) IV AY752139, AY752172, AY752200, AY752231, AY752262
Cercospora acaciae-mangii CPC 10551 Acacia mangium 481 nt (99 %) II 306 nt (100 %) I 221 nt (99 %) IV 305 nt (100 %) I 377 nt (100 %) I AY752140, AY752173, AY752201, AY752232, AY752263
Cercospora sp. 2 CBS 132656; CPC 11536 Acacia mangium 473 nt (99 %) III 306 nt (100 %) I 221 nt (99 %) IV 312 nt (100 %) I 378 nt (99 %) IV JX143723, JX143482, JX143236, JX142990, JX142744
Cercospora sp. 2 CPC 11539 Acacia mangium 481 nt (99 %) III 306 nt (100 %) I 221 nt (99 %) IV 312 nt (100 %) I 378 nt (98 %) V JX143729, JX143488, JX143242, JX142996, JX142750
Cercospora dioscoreaepyrifoliae CBS 132661; CPC 11634; PNG-002 Dioscorea rotundata 481 nt (99 %) III 284 nt (100 %) I 221 nt (99 %) II 297 nt (100 %) I 378 nt (99 %) VI JX143724, JX143483, JX143237, JX142991, JX142745
Cercospora dioscoreaepyrifoliae CBS 132663; CPC 11636; PNG-016 Dioscorea esculenta 481 nt (99 %) III 306 nt (100 %) I 221 nt (99 %) II 303 nt (100 %) I 378 nt (99 %) VI JX143725, JX143484, JX143238, JX142992, JX142746
Cercospora dioscoreaepyrifoliae CPC 11639; PNG-037 Dioscorea rotundata 481 nt (99 %) II 306 nt (100 %) I 221 nt (99 %) II 303 nt (100 %) I 378 nt (99 %) II JX143730, JX143489, JX143243, JX142997, JX142751
Cercosporoid CBS 132679; CPC 15807 Phaseolus vulgaris 481 nt (99 %) II 294 nt (99 %) II 220 nt (99 %) III 312 nt (100 %) I 376 nt (99 %) VI JX143726, JX143485, JX143239, JX142993, JX142747
Cercospora sp. CBS 132681; CPC 15844 Euphorbia sp. 481 nt (99 %) III 294 nt (99 %) II 220 nt (99 %) III 312 nt (99 %) II 376 nt (100 %) I JX143727, JX143486, JX143240, JX142994, JX142748
Cercospora sp. CBS 132682; CPC 15850 Taraxacum sp. 481 nt (99 %) II 294 nt (99 %) II 220 nt (99 %) III 312 nt (100 %) I 377 nt (100 %) VI JX143728, JX143487, JX143241, JX142995, JX142749
Cercospora sp. CPC 15875 Euphorbia sp. 481 nt (99 %) III 294 nt (99 %) II 220 nt (99 %) III 312 nt (100 %) I 378 nt (99 %) VI JX143731, JX143490, JX143244, JX142998, JX142752
Septoria provencialis (outgroup) CBS 118910; CPC 12226 Eucalyptus sp. 483 nt (98 %) 317 nt (75 %) 227 nt (87 %) 329 nt (81 %) 386 nt (93 %) DQ303096, JX143522, JX143276, JX143030, JX142784
Number of identical sequences (excl. outgroup): 6 of 17 13 of 17 6 of 17 16 of 17 7 of 17
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ITS — Three allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at only two positions in the second internal transcribed spacer (transitions at positions 451 and 453 compared to the sequence of isolate CPC 5325). Although allele group I was confined to isolates from Cajanus (Fabaceae), the other two groups were intermixed amongst the remaining host genera.

TEF — Two allele groups are identified based on sequence identity. The variation in this locus is based on a single nucleotide change (transitions at position 289 compared to the sequence of isolate CPC 5325). Although allele group I was confined to isolates from Acacia (Fabaceae), Cajanus, and Dioscorea (Dioscoreaceae), the other group represents the remaining host genera.

ACT — Four allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at three positions (transitions at positions 143, 166 and 173 compared to the sequence of isolate CPC 5325). Allele group I was confined to isolates from Cajanus, and allele group II is mainly limited to Dioscorea (except for one isolate from Acacia), allele group IV is limited to the remaining isolates from Acacia, and the remaining host genera belong to allele group III.

CAL — Two allele groups are identified based on sequence identity. The variation in this locus is based on a single nucleotide change (a transition at position 76 compared to the sequence of isolate CPC 5325). This single nucleotide change only occurred in isolate CPC 15844; the rest of the isolates had identical CAL sequences.

HIS — Six allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at 10 positions (transitions at positions 106, 112, 148, 149, 178, 205, 238, 301 and 364, as well as a transversion at position 245 compared to the sequence of isolate CPC 5325). Allele group II differs from allele group I by a unique change of C to T at position 364 and allele group V differs from allele group IV by a unique change of A to T at position 245. Even if allele group I and II and group IV and V are taken as combined groups, isolates from different hosts are intermixed and no clear association of host with allele group, as with the loci mentioned above, is possible.

GAPDH — Six allele groups are identified based on sequence identity. The variation in this locus is based on numerous nucleotide changes (transitions at positions 44, 48-49, 52-53, 56, 63-69, 110, 122, 149, 158, 206, 257, 287, 329, 335, 395, 440, 479, 530, 533, 566, 593, 596, 608, 647, 650, 674, 720, 731, 740, 747, 780, 789, 791-792, 794, 804-806, 808-809, 811-812, 817, 821-822, 824, 830, 834, 837, 839-840, 842-844, 846, 848, 852, 856, 874, 922 and 958, transversions at positions 49, 66, 233, 767, 785, 787-789, 792, 795, 797, 798, 806, 810-811, 814, 818-819, 821, 831, 833, 843, 848-849, 865 and 883, indels at positions 67, 101 and 803, as well as another indel spanning 801-811, compared to the sequence of isolate CPC 5325). Allele group II differs from allele group I by a unique change of C to T at position 530. This locus represents the largest number of nucleotide substitutions of all the loci included for Cercospora sp. Q in this study, and therefore has high potential for species discrimination. However, if each allele group is accepted as a distinct species, it would result in a huge proliferation of taxa within this group.

mtSSU — Only one allele group is identified based on sequence identity. No variation was observed over the 573 nucleotides sequences for the selected isolates.

CHS — Three allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at only three positions (transitions at positions 91, 100 and 217 compared to the sequence of isolate CPC 5325). Allele group I includes four of the six isolates from Cajanus and allele group III includes the isolates from Phaseolus (Fabaceae) and Euphorbia (Euphorbiaceae); the remaining isolates belong to allele group II.

TUB — This locus failed to amplify easily, even when several different primer combinations were tested. Three allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at six positions (transitions at positions 147 and 396, transversions at positions 172, 189, 213 and 591 compared to the sequence of isolate CPC 5325). The majority of sequences were obtained for the isolates from Cajanus, and these isolates end up belonging into all three allele groups.

Mcm7 — This locus failed to amplify easily, even when both available primer combinations were tested. Three allele groups are identified based on sequence identity. The variation in this locus is based on nucleotide changes at six positions (transitions at positions 60, 86, 263, 365 and 470, and a transversion at position 89, compared to the sequence of isolate CPC 5325). Due to the small number of successful sequences, a clear conclusion cannot be drawn from this dataset and it was not possible to distinguish between the isolates from Acacia and Dioscorea.

TAXONOMY

In this paper, a polyphasic approach was taken and species are discussed and/or described with consideration to the following factors:

Phylogenetic analyses: Based on the clustering and support in the Bayesian tree obtained from the combined ITS, TEF, ACT, CAL and HIS alignment (Fig. 2). All genes were also assessed individually (data not shown; discussed where applicable in the species notes).

Morphological characteristics: A few morphological characteristics effectively distinguished species (Fig. 3). These are: conidiophores (uniform, irregular, attenuated, truncate, long or short obconically truncate), conidiogenous cells (terminal, intercalary), loci (apical, lateral, circumspersed (all around the conidiogenous cell; Hennebert & Sutton 1994); uni-local (single, terminal locus), multi-local (multiple loci); thickness, absence of protuberant loci), and conidia (dimensions, shape, hilum morphology).

Fig. 3.

Fig. 3.

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Overview of morphological structures. A. Fasciculate conidiophores situated on a stroma. B. Conidiophores reduced to uni-local conidiogenous cells. C. Conidiophores arising from a weakly developed stroma. D. Fasciculate conidiophore with flexuous conidiophores. E. Conidiophores arising from external mycelium. F. Thickened, darkened and somewhat refractive conidial loci (arrows). G. Conidiogenous cells with multi-local loci. H. Fascicle erumpent through stoma. I. Cylindrical conidium with obtuse apex. J. Filiform conidium. K, L. Acicular, undulate conidia with subobtusely rounded apices, and truncate bases. M-O. Obclavate conidia with subobtusely rounded apices and obconically truncate bases. P. Subcylindical conidium with long obconically truncate base.

A diagnostic characteristic of species with wide host ranges was circumspersed loci on tenuous conidiophores, whereas the species with narrow host ranges had a few distinct apical or lateral loci on moderately thick-walled to thick-walled conidiophores. These characteristics were preserved, even when the fungus was cultivated on agar medium.

The Bayesian analysis resulted in 73 species clades mapped onto the phylogenetic tree (Fig. 2); 34 of these were assigned to an existing species name, 15 more were morphologically similar to existing species but names could not be applied without doubt (indicated with “cf.” in the species name, see species notes below), a further 19 could not be named unequivocally (“Cercospora spp. A-S”) and novel species are introduced below for the remaining five clades.

Cercospora achyranthis Syd. & P. Syd., Ann. Mycol. 7: 171. 1909.

Caespituli amphigenous, mainly hypophyllous. Mycelium internal. Stromata lacking or composed of a few brown cells, intraepiderimal or substomatal. Conidiophores thick-walled, dark brown, arising from internal hyphae or a few brown cells, solitary, or in loose fascicles (2-5), straight, sinuous to distinctly geniculate, flexuous, almost uniform in width, somewhat wider at the apex, often constricted at septa and proliferating point, conical at the apex, simple, sometimes branched, 31-340 × 4.5-6 μm, 2-20-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, multi-local; loci distinctly thickened, darkened, slightly to distinctly protuberant, apical or formed on shoulders caused by geniculation, 2-3 μm diam. Conidia solitary, subhyaline, acicular, cylindrical to cylindro-obclavate, straight to slightly curved, long obconically truncated and thickened at the base, obtuse at the apex, rarely constricted at the septa, 33-172 × 3.5-8 μm, 3-20-septate.

Specimens examined: South Korea, Jeju, on Achyranthes japonica (Amaranthaceae), 14 Sep. 2002, H.D. Shin, CBS H-20983, CPC 10088-10091; on A. japonica, 13 Nov. 2003, H.D. Shin, CBS H-20984, CBS 132613 =CPC 10879, CPC 10880-10881.

Notes: This species is characterised by conidiophores with a thickened, dark brown wall, vary in shape, often constricted at septa, and conical at the apex, sometimes branched, and longer than in most other species (31-340 × 4.5-6 μm, 2-20-septate). The conidia of C. achyranthis are not hyaline, but subhyaline to pale olivaceous and have rather small hila (ca. 2 μm wide), which are reminiscent of the genus Passalora. Nevertheless, it is a true Cercospora. Cercospora achyranthis is supported by ACT. The TEF and CAL phylogenies fail to discriminate C. sojina (also with subhyaline conidia and small hila) from C. achyranthis. On the HIS phylogeny, it is indistinguishable from C. polygonaceae, to which it is also a sister taxon in the combined tree (Fig. 2 part 2). The name C. achyranthis is based on Japanese material, and fresh collections from Japan would be required to designate an epitype for this taxon.

Cercospora agavicola Ayala-Escobar, Mycotaxon 93: 117. 2005.

Specimen examined: Mexico, State of Guanajuato, Penjamo, on Agave tequilana var. azul (Agavaceae), Jan. 2003, V. Ayala-Escobar and Ma. de Jesús Yáñez-Morales, holotype CHAPA # 166, isotype HAL 1839 F, culture ex-type CBS 117292 =CPC 11774.

Notes: Cercospora agavicola is characterised by large stromata and consistently cylindrical conidia, often with swollen tips (Ayala-Escobar et al. 2005). In this study using a larger dataset, it is also clear that C. agavicola, which is supported by TEF, ACT, CAL and HIS regions, is genetically distinct from the other Cercospora species studied. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. cf. coreopsidis.

Cercospora alchemillicola U. Braun & C.F. Hill, Mycol. Progr. 1: 19. 2002.

Specimens examined: New Zealand, Auckland, Western Springs Gardens, on Alchemilla mollis (Rosaceae), 23 Jul. 2000, C.F. Hill, Lynfield 236 (holotype HAL, isotype PDD 73031); on A. mollis, C.F. Hill, Lynfield 564, epitype designated here CBS H-20985, culture ex-epitype CPC 5259.

Notes: Sequences from New Zealand on hosts of Onagraceae (Gaura, isolate CPC 5127, and Oenothera, isolate CPC 5126) are slightly distinct from that derived from Alchemilla (Rosaceae). The collections on Onagraceae (C. cf. alchemillicola) are also morphologically different from C. alchemillicola, and represent an undescribed species. The three isolates are identical to one another on the TEF, ACT, CAL and HIS phylogenies but also to some other species, e.g. to Cercospora sp. I, C. cf. physalidis and C. celosiae based on the TEF phylogeny, and Cercospora sp. I and C. cf. physalidis based on the ACT phylogeny. A similar mix is observed in the HIS phylogeny with Cercospora sp. I and C. celosiae and in the CAL phylogeny with Cercospora spp. M, O, P, Q and C. cf. sigesbeckiae. In the combined tree (Fig. 2 part 4), the three isolates represent sister taxa.

Cercospora cf. alchemillicola

Specimens examined: New Zealand, Auckland City, Albert Park, on Gaura lindheimeri (Onagraceae), C.F. Hill, Lynfield 545, CPC 5127; on Oenothera fruticosa (Onagraceae), C.F. Hill, Lynfield 541, CPC 5126.

Notes: Cercospora on Gaura and Oenothera in New Zealand cannot be distinguished on the individual gene trees from C. alchemillicola (see species notes under that species above) described from New Zealand on Alchemilla mollis (Braun & Hill 2002). We consider the latter two isolates to represent a distinct species, which cannot be formally named due to the absence of good specimens. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. alchemillicola.

Cercospora althaeina Sacc., Michelia 1: 269. 1878.

  • = Cercospora kellermanii Bubák, J. Mycol. 9: 3. 1903.

  • = Cercospora althaeina var. praecincta Davis, Trans. Wisconsin Acad. Sci. 18: 260. 1915.

    • ≡ Cercospora praecincta (Davis) Chupp, A monograph of the fungus genus Cercospora: 376. 1954.

  • = Cercospora ramularia Siemaszko, Izv. Kavkazsk. Muz.12: 28. 1919, and Arch. Nauk Biol. Towarz. Nauk. Warszawsk. 1: 49. 1923.

    • ≡Cercosporina ramularia (Siemaszko) Sacc., Syll. Fung. 25: 910. 1931.

  • = Cercospora althaeina var. althaeae-officinalis Săvul. & Sandu, Hedwigia 73: 127. 1933.

  • = Cercospora althaeicola J.M. Yen & S.K. Sun, Cryptog. Mycol. 4: 189. 1983.

Leaf spots distinct, angular to irregular, mostly vein-limited, olivaceous-brown, sometimes greyish brown with dark brown margin, centre becoming pale grey with black dots (= stroma with conidiophores). Caespituli amphigenous, mostly epiphyllous. Mycelium internal. Stromata well-developed, emerging through stomatal openings or erumpent through the cuticle. Conidiophores in divergent fascicles (6-12), pale olivaceous-brown at the base, paler upwards, 0-3-septate, straight to mildly curved, 32-90 × 4-6.5 μm, conically narrowed at the apex; loci 1.5-2 μm wide, conspicuous, apical or on shoulders formed by geniculation. Conidia solitary, obclavate-cylindrical to filiform, not acicular, straight to mildly curved, hyaline, 1-10-septate, obtuse at the apex, subtruncate or obconically truncate at the base, 40-140 × 3.5-5 μm (adapted from Shin & Kim 2001).

Specimens examined: Italy, Selva, on Althaea rosea, 1876, holotype in PAD. Romania, Fundulea, on A. rosea, O. Constantinescu, epitype designated here CBS H-9811, culture ex-epitype CBS 248.67 = CPC 5117. Unknown, on Malva sp. (Malvaceae), C. Killian, CBS 126.26 = CPC 5066, (as C. malvacearum). South Korea, Suwon, on Althaea rosea (Malvaceae), 14 Oct. 2003, H.D. Shin, CBS H-20986, CBS 132609 =CPC 10790.

Notes: A true Cercospora s. str. close to C. apii s. lat., but distinguished by obclavate-cylindrical conidia with obconically truncate bases (Crous & Braun 2003). Although only weakly supported as distinct from C. armoraciae, we suspect that the isolate from Malva sp. represents a different taxon. Further isolates and pathogenicity studies are needed to test this hypothesis. The species is distinguished in the TEF and ACT phylogenies but cannot be distinguished from C. zebrina, Cercospora sp. L and C. rumicis based on the CAL phylogeny. In the HIS phylogeny the three isolates are not identical to any other species but the isolate from Malva sp. clusters distinct from the two A. rosea isolates which form a sister clade to C. chenopodii. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. zebrina.

Cercospora apii Fresen., emend. Groenewald et al. Phytopathology 95: 954. 2005.

Caespituli amphigenous. Mycelium internal. Stromata lacking or small, up to 32 μm diam, brown, substomatal or intraepidermal. Conidiophores arising from upper part of stromata or internal hyphae, solitary to 2-8, in loose to dense fascicles, brown, paler towards the apex, simple, mildly sinuous, moderately thick-walled to thick-walled, straight or once abruptly geniculate caused by sympodial proliferation, slightly curved, uniform in width, wider at the base, short conically truncate or truncate at the apex, 12.5-160 × 5-8 μm. Conidiogenous cells integrated, terminal or intercalary, proliferating sympodially, chiefly uni-local; loci distinctly thickened, not or slightly protuberant, 2-4 μm diam, apical or formed on the shoulder caused by sympodial proliferation. Conidia solitary, hyaline, cylindro-obclavate when shorter, longer conidia usually acicular, straight to slightly curved, subacute to obtuse at the apex, truncate to obconically truncate and thickened at the base, 35-120 × 3.5-5 μm, 3-10-septate.

Specimens examined: Austria, Wien, on Beta vulgaris (Chenopodiaceae), Jun. 1931, E.W. Schmidt, CBS 121.31 = CPC 5073; on Apium sp. (Apiaceae), 28 Aug. 2003, Institut fur Pflanzengesundheit, CBS 114416 =CPC 10925. Germany, Landwirtschaftsamt, Heilbron, on Apium graveolens (Apiaceae), K. Schrameyer, culture ex-type CBS 116455 =CPC 11556; CBS 116504 =CPC 11579; CBS 116507 =CPC 11582. Hungary, on B. vulgaris, Jun. 1931, E.W. Schmidt, CBS 127.31 = CPC 5119. Italy, on A. graveolens, M. Meutri, CBS 114418 =CPC 10924; CBS 114485 =CPC 10923. Japan, Aichi, on A. graveolens, 1 Nov. 1995, T. Kobayashi, MUCC 567 = MAFF 238072 = MUCNS 30 (named as C. apii s. str.); Shizuoka, on A. graveolens, 8 Jun. 2007, M. Togawa, MUMH 10802, MUCC 593; Saga, on Asparagus officinalis (Asparagaceae), 20 Sep. 1999, J. Yamaguchi, MUMH 11400, MUCC 923 = MAFF 238299; Hokkaido, on Glebionis coronaria (≡ Chrysanthemum coronarium) (Asteraceae), Aug. 1989, MUCC 573 = MAFF 235978. Netherlands, Bergen op Zoom, on B. vulgaris, Sep. 1951, G. van den Ende, CBS 152.52 = IMI 077043 = MUCL 16495 = CPC 5063. New Zealand, Auckland, on Glebionis coronaria (≡ Chrysanthemum coronarium), C.F. Hill, Lynfield 566, CPC 5260; on Moluccella laevis (Lamiaceae), C.F. Hill, Lynfield 516, CPC 5112. Romania, Hagieni, distr. Constanta, on Plumbago europaea (Plumbaginaceae), 13 Jun. 1970, O. Constantinescu, CBS 553.71 = IMI 161116 = CPC 5083 (as C. plumbaginea); Bucuresti, on A. graveolens, 2 Oct. 1969, O. Constantinescu, CBS H-9812, CBS 536.71 = CPC 5087; Domnesti, on Plantago lanceolata (Plantaginaceae), 3 Aug. 1965, O. Constantinescu, CBS 252.67 = CPC 5084. Unknown, on A. graveolens, Mar. 1925, L.J. Klotz, CBS 119.25 = B 42463 = IHEM 3822 = CPC 5086. USA, California, on M. laevis, S.T. Koike, CBS 110816 =CPC 5111; CBS 110813 =CPC 5110; California, on A. graveolens, 27 Sep. 2010, S.T. Koike, CPC 18601. Zimbabwe, on M. laevis, 13 May 2009, S. Dimbi, CBS 132683 =CPC 16663.

Notes: Various investigators have demonstrated that great variation in the size and shape of conidiophores and conidia (conidiophores: 25-300 × 3.5-9 μm, rarely branched, conidia: 25-315 × 3-6 μm, cylindrical, filiform to acicular) is induced by changes in environmental conditions, especially humidity. Crous & Braun (2003) pointed out these morphological ambiguities, and introduced a concept of Cercospora apii s. lat., for taxa morphologically indistinguishable from Cercospora apii on A. graveolens. Cercospora apii s. str., which is phylogenetically distinct, is characterised in that its conidiophores are almost uniform in width, moderately thick-walled or thick-walled, short obconically truncate at the apex, and with a few loci on integrated conidiogenous cells, and long-cylindrical to cylindrical-obclavate to often acicular conidia with truncate or obconically truncate basal ends and subacute to obtuse apices.

According to Crous & Braun (2003), the host plants of C. apii s. str. are found in more than 86 genera of several plant families. Groenewald et al. (2006a) concluded that C. apii s. str., which is mainly isolated from celery, has a wide host range, because numerous isolates of C. apii s. lat. originating from various host plants have similar nucleotide sequences to the type strain of C. apii s. str.

In principle, the phylogenetic split observed between C. beticola and C. apii is only supported by the CAL sequences, and for the other genes these two taxa cluster as a large unresolved clade. Groenewald et al. (2005) showed that these two species are also distinguished by their AFLP fingerprints and growth conditions, suggesting that they were operational species units with a different ecology. These results indicate that in many cases morphologically identical species occurring on different hosts in fact represent different species. The situation is complicated in that there are several species with wide host ranges. Other species can colonise dead material of non-hosts, facilitating what has been described as a pogostick hypothesis (Crous & Groenewald 2005), until they locate their ideal hosts on which they are primary pathogens. In the present study it was further found that the CAL phylogeny fails to distinguish C. apii s. str. from C. cf. brunkii and C. cf. resedae, which are sister taxa in the combined tree (Fig. 2 part 5).

Cercospora apiicola M. Groenew., Crous & U. Braun, Mycologia 98: 281. 2006.

Leaf spots amphigenous, subcircular to irregular, 3-10 mm diam, medium brown, with a raised or inconspicuous, indefinite margin, not surrounded by a border of different colour. Caespituli amphigenous, but primarily hypophyllous. Stromata lacking to well-developed, 30-60 μm diam, medium brown. Conidiophores in fascicles (4-10), moderately dense, arising from stromata, emerging through stomata or erumpent through the cuticle, subcylindrical, upper part geniculate-sinuous, unbranched, 1-3-septate, 25-70 × 4-6 μm, medium brown, becoming pale brown towards the apex, smooth, wall somewhat thickened. Conidiogenous cells integrated, terminal, 15-30 × 4-5 μm, occasionally unilocal, usually multilocal, sympodial; loci subcircular, planate, thickened, darkened, refractive, 2.5-3 μm wide. Conidia solitary, cylindrical when small, obclavate-cylindrical when mature, not acicular, (50-)80-120(-150) × (3-) 4-5 μm, 1-6(-18)-septate; apex subobtuse, base obconically subtruncate; hila 2-2.5 μm wide, thickened, darkened, refractive.

Specimens examined: Greece, on Apium graveolens, 2000, I. Vloutoglou, CBS 132666 =CPC 11642; CPC 11641. South Korea, Kangnung, on A. graveolens, 20 Sep. 2003, H.D. Shin, CPC 10666; Namyangju, on A. graveolens, 30 Sep. 2003, CBS 116458 =CPC 10657; on A. graveolens, 22 Oct. 2003, H.D. Shin, CBS 132651 =CPC 10759. Venezuela, La Guanota, Caripe, Edo. Monagas, 1050 m.s.n.m., on Apium sp., 23 Jul. 2002, N. Pons, holotype CBS H-18473, culture ex-type CBS 116457 =CPC 10267; CBS 132644 =CPC 10248; CPC 10220; CPC 10265-10266; CPC 10279; CPC 10666.

Notes: Morphologically C. apiicola differs from C. apii s. str. in having multiple conidiogenous loci and long conically truncate conidiogenous cells (Groenewald et al. 2006a). It has a high degree of phylogenetic independence from other species of C. apii s. lat. supported by TEF, ACT, CAL and HIS regions. It is also clearly distinct from C. apii in the combined tree (Fig. 2 part 2 vs. part 5).

Cercospora armoraciae Sacc., Nuovo Giorn. Bot. Ital. 8: 188. 1876.

  • =?Cercospora cheiranthi Sacc., Nuovo Giorn. Bot. Ital. 8: 187. 1876.

  • = Cercospora nasturtii Pass., Hedwigia 16: 124. 1877.

  • = Cercospora nasturtii subsp. barbareae Sacc., Michelia 2: 557. 1882.

    • ≡Cercospora barbareae (Sacc.) Chupp, Farlowia 1: 579. 1944.

  • = Cercospora bizzozeriana Sacc. & Berl., Malpighia 2: 248, 1888.

  • = Cercospora atrogrisea Ellis & Everh., Proc. Acad. Nat. Sci. Phiadelphia 45: 464. 1894.

  • = Cercospora bizzozeriana var. drabae Sausa da Câmara, Revista Agron. (Lisbon) 1: 25. 1903.

  • = Cercospora berteroae Hollós, Ann. Mus. Nat. Hung. 5: 468. 1907.

  • = Cercospora drabae Bubák & Kabát, Hedwigia 52: 362. 1912.

    • ≡Cercosporina drabae (Bubák & Kabát) Sacc., Syll. Fung. 25: 900. 1931.

  • = Cercospora camarae Curzi, Atti Ist. Bot. Univ., Pavia, III, 2: 101. 1925.

  • = Cercospora cardamines Losa (as “cardaminae”), Anales Jard. Bot. Madrid 6: 453. 1946.

  • == Cercospora lepidii Niessl, unknown, in herb., HBG fide Chupp (1954, p. 180).

Caespituli amphigenous. Mycelium internal. Stromata lacking to well-developed, up to 60 μm diam, brown, substomatal or intraepidermal. Conidiophores arising from internal hyphae or a few brown cells, cylindrical, solitary, or in loose to divergent fascicles (2-30), pale to pale brown, paler towards apex, moderately thick-walled, simple, straight to strongly geniculate, irregular in width, often narrowed with successive geniculation, truncate or conically truncate at the tip, sometimes constricted at septa, 13-135 × 2.5-7.5 μm, 0-7-septate. Conidiogenous cells integrated, terminal, intercalary, proliferating sympodially, uni-local to multi-local (1-3); loci conspicuous, apical or on shoulder of conidiogenous cells caused by geniculation, rarely lateral, distinctly thickened, somewhat protuberant, refractive or darkened, 1.8-3.5 μm diam. Conidia solitary, hyaline, straight to mildly curved, cylindrical, cylindro-obclavate to acicular, obconically truncate or truncate, distinctly thickened at the base, obtuse at the apex, 15-125 × 2.5-6 μm, 1-11-septate.

Specimens examined: Italy, Venice, on Armoracia rusticana (= A. lapathifolia) (Brassicaceae), Treviso, Sep. 1874, (syntype Mycoth. Ven. 282, in B, HBG, S). Japan, Okinawa, on A. rusticana (= A. lapathifolia), 19 Nov. 2007, C. Nakashima, MUMH 10820, MUCC 768. New Zealand, Auckland, Grey Lynn, on Nasturtium officinale (= Rorippa nasturtium-aquaticum) (Brassicaceae), 14 Apr. 2002, C.F. Hill, Lynfield 576, CBS H-20988, CBS 115394 =CPC 5261 (named as C. nasturtii); Manurewa, on A. rusticana (= A. lapathifolia), C.F. Hill, Lynfield 622, CBS 115409 =CPC 5359 (as C. armoraciae); on Gaura sp. (Onagraceae), C.F. Hill, Lynfield 634, CBS 115060 =CPC 5366. Romania, Fundulea, on A. rusticana (= A. lapathifolia), O. Constantinescu, epitype designated here CBS H-20987, culture ex-epitype CBS 250.67 = CPC 5088; Fundulea, on Cardaria draba (Brassicaceae), O. Constantinescu, CBS 258.67 = CPC 5061 (as C. bizzozeriana); Hagieni, on Berteroa incana (Brassicaceae), O. Constantinescu, CBS 538.71 = IMI 161109 = CPC 5090 (as C. berteroae); Hagieni, on C. draba, O. Constantinescu, CBS 540.71 = IMI 161110 = CPC 5060 (as C. bizzozeriana); Hagieni, on Coronilla varia (Fabaceae), O. Constantinescu, CBS 555.71 = IMI 161117 = CPC 5082 (as C. rautensis); Valea Mraconiei, on Erysimum cuspidatum (Brassicaceae), O. Constantinescu, CBS 545.71 = CPC 5056 (as C. erysimi). South Korea, Hoengseong, on Turritis glabra (≡ Arabis glabra) (Brassicaceae), 23 Jun. 2004, H.D. Shin, CBS H-20989, CBS 132654 =CPC 11338 (as C. nasturtii); CPC 11364 (as C. nasturtii); Jecheon, on Rorippa indica (Brassicaceae), 19 Oct. 2007, H.D. Shin, CBS 132672 =CPC 14612 (as C. nasturtii); Pocheon, on Barbarea orthoceras (Brassicaceae), 23 Oct. 2002, H.D. Shin, CBS H-20990, CBS 132638 =CPC 10100 (named as C. nasturtii); Wonju, on R. indica, 18 Oct. 2002, H.D. Shin, CBS H-20991, CPC 10133 (as C. nasturtii); Suwon, on A. rusticana (= A. lapathifolia), 14 Oct. 2003, H.D. Shin, CBS H-20992, CBS 132610 =CPC 10811 (as C. armoraciae). Thailand, on Acacia mangium (Fabaceae), W. Himaman, CPC 11530.

Notes: See also C. capsici. Cercospora armoraciae is supported by the HIS phylogeny. In the TEF phylogeny it is part of a larger clade intermixed with C. zebrina, Cercospora sp. L, C. rumicis, C. violae and C. althaeina; in ACT the C. armoraciae clade contains some intraspecific variation and also includes C. rumicis. In the CAL phylogeny, it is a sister clade to C. zebrina, but it contains isolates from C. capsici. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. capsici. Morphological characteristics of the C. armoraciae clade include conidiophores that are often narrowed, with successive geniculation, conically truncate at the apex, and with distinctly thickened and somewhat protuberant loci, and conidia that are cylindro-obclavate to acicular.

In this study, most Cercospora species on Brassicaceae having indistinguishable morphological characteristics are listed as synonyms under C. armoraciae. This treatment was proposed previously (Crous & Braun 2003). Davis (1929) pointed out that similar forms on Brassicaceae, namely C. nasturtii, C. armoraciae, C. cheiranthi, etc., were likely conspecific. The results of this study support his prediction. Cercospora stanleyae Chupp ex U. Braun & Crous (Crous & Braun 2003) is tentatively maintained as a separate species due to morphological differences. Cercospora brassicicola differs from C. armoraciae in that the former has long conidiophores (up to 500 μm in length), and is pathogenic to Brassica. In addition, Cercospora thlaspi “thlaspiae” differs from C. armoraciae in that the former has long conidiophores (to 400 μm in length) and acicular conidia (40-300 × 2-4 μm).

Cercospora beticola Sacc., emend. Groenewald et al., Phytopathology 95: 954. 2005.

Caespituli hypophyllous. Mycelium internal. Stromata lacking to well-developed, up to 60 μm diam, intraepidermal or substomatal, brown to dark brown. Conidiophores solitary to 2-18 in loose fascicles, slightly divergent, brown, paler towards apex, moderately thick-walled, cylindrical, almost uniform in width, simple, geniculate, 16-200(-450) × 4-6 μm, 1-6-septate, truncate at the apex, sometimes constricted at septa. Conidiogenous cells terminal or intercalary, proliferating sympodially, with 1-2 loci; loci distinctly thickened, not protuberant, apical or formed on shoulder of conidiogenous cells caused by geniculation and lateral, 2.5-3(-4) μm. Conidia solitary, filiform to acicular, straight to mildly curved, rarely cylindro-obclavate, truncate at the base, acute to subacute at the tip, 27-250 × 2-5 μm, 3-28-septate.

Description of caespituli on V8 medium; MUCC 568 (MAFF 238206): Conidiophores solitary to loosely fasciculate, brown, paler towards the apex, uniform in width, smooth, moderately thick-walled, straight to slightly sinuous, short conically truncate at the tip, 50-148 × 3-5 μm, multi-septate. Conidiogenous cells integrated, terminal; loci moderately thickened, apical, uni-local, 2-3 μm in width. Conidia hyaline, cylindrical to cylindro-obclavate; short obconical, slightly thickened and truncate or obconically truncate at the base, acute at the apex, 40-88 × 3-6 μm, 3-14-septate.

Specimens examined: Botswana, Gaborone, on Spinacia sp. (Chenopodiaceae), L. Lebogang, CPC 5369-5370. Bulgaria, on Goniolimon tataricum (Plumbaginaceae), S.G. Bobev, CBS 123907 =CPC 14616; CBS 123908 =CPC 14620; CBS 132673 =CPC 14617; CPC 14618-14619. Czech Republic, on Beta vulgaris, Sep. 1947, G.E. Bunschoten, CBS 117.47. Egypt, on B. vulgaris, 15 Apr. 2004, M. Hasem, CPC 12028-12030. France, Longvic, on B. vulgaris, S. Garressus, CBS 116505 =CPC 11580. Germany, on B. vulgaris, S. Mittler, CPC 12031; CPC 12027; CPC 12022; CBS 116502 =CPC 11577; CBS 116454 =CPC 11558; on B. vulgaris, Jun. 1931, E.W. Schmidt, CBS 122.31 = CPC 5072; CBS 126.31 = CPC 5064. Iran, Pakajik, on B. vulgaris, A.A. Ravanlou, CBS 116501 =CPC 11576. Italy, Ravenna, on B. vulgaris, 10 Jul. 2003, V. Rossi, culture ex-epitype CBS 116456 =CPC 11557; CBS 116503 =CPC 11578. Japan, Chiba, on B. vulgaris, 30 May 1998, S. Uematsu, MUCNS 320 = MUCC 568 = MAFF 238206; Hokkaido, on B. vulgaris, 1955, K. Goto, MUCC 569 = MAFF 305036. South Korea, Namyangju, on Chrysanthemum segetum (= Ch. coronarium var. spatiosum) (Asteraceae), 24 Jun. 2004, H.D. Shin, CBS 132655 =CPC 11341 (named as C. chrysanthemi); 27 Jul. 2004, H.D. Shin, CPC 11344 (named as C. chrysanthemi). Mexico, Texcoco, on B. vulgaris, 20 Oct. 2008, Ma. de Jesús Yáñez-Morales, CPC 15623. Netherlands, on B. vulgaris, M. Groenewald, CBS 116506 =CPC 11581; Northwest Brabant, on B. vulgaris, Nov. 1947, G.E. Bunschoten, CBS 116.47 = CPC 5074. New Zealand, Auckland, on Limonium sinuatum (Plumbaginaceae), 25 Feb. 2002, C.F. Hill, Lynfield 533, CBS 115478 =CPC 5113 (named as C. statices); on B. vulgaris, C.F. Hill, CPC 5128; Lynfield 539, CPC 5125; CPC 10197; CPC 10204; CPC 10168; CBS 117556 =CPC 10171; CPC 10168; on Apium graveolens, C.F. Hill, Lynfield 537a, CPC 5123. Romania, Bucuresti, on B. vulgaris, 17 Oct. 1966, O. Constantinescu, CBS 539.71 = CPC 5062; Hagieni, on Malva pusilla (Malvaceae), 15 Jul. 1970, O. Constantinescu & G. Negrean, CBS H-9847, CBS H-9849, CBS 548.71 = IMI 161115 = CPC 5065; on B. vulgaris, Jun. 1931, E.W. Schmidt, CBS 124.31 = CPC 5070. Spain, on B. vulgaris, Jun. 1931, E.W. Schmidt, CBS 123.31 = CPC 5071. Unknown, on B. vulgaris, Jun. 1931, E.W. Schmidt, CBS 125.31 = CPC 5069. USA, California, on B. vulgaris, S.T. Koike, CPC 18813.

Notes: Cercospora beticola is the causal agent of Cercospora leaf spot on B. vulgaris, which is one of the most common and destructive sugar beet diseases (Weiland & Koch 2004). Despite its importance as a plant pathogen, its actual host range remains unclear.

Initial phylogenetic analyses on the genus Cercospora employed ITS sequences to reveal phylogenetic relationships within the genus (Stewart et al. 1999, Goodwin et al. 2001, Pretorius et al. 2003). These analyses failed to discriminate all species due to the limited resolution provided by the ITS locus. Groenewald et al. (2005, 2006a) subsequently succeeded in using multi-locus sequence data from five gene regions to distinguish Cercospora species. They also expanded the host range of C. beticola. Although isolates of C. beticola have been isolated from diverse hosts, these isolates appear to have been colonising non-hosts as saprobes or secondary invaders (Crous & Groenewald 2005), and proof of their pathogenicity has not been confirmed.

Results from the phylogenetic analyses using CAL and combined multi-locus data set divide C. beticola and C. apii s. str. into two different clades, with C. beticola splitting further into two subclades (also see Fig. 2 part 6) based on sequence changes in HIS, probably due to intraspecific variation. The combined data clearly show that C. apii s. str. and C. beticola are related sibling species, although C. beticola must be retained as a separate species.

Cercospora cf. brunkii

Caespituli amphigenous. Mycelium internal. Stromata lacking or composed of few dark brown cells, intraepidermal or substomatal. Conidiophores brown to dark brown, paler at the apex, 2-6 in loose fascicles, moderately thick-walled, straight or 1-2 times geniculate caused by sympodial proliferation, uniform in width, mildly attenuated at the apex, short obconically truncate or truncate at the apex, 30-160 × 4.5-5.5 μm, 0-9-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, rarely percurrently, uni- or multi-local (2-5); loci distinctly thickened, often dispersed on whole conidiophores, darkened, apical and lateral, 2-3 μm diam. Conidia solitary, hyaline, acicular, straight or slightly curved, thickened and truncate at the base, acute at the apex, 27-110 × 1.5-4 μm, indistinctly multi-septate, 0-9-septate.

Specimens examined: Japan, Wakayama, on Datura stramonium (Solanaceae), 30 Oct. 2007, C. Nakashima & I. Araki, MUMH 10858, MUCC 732. South Korea, Namyangju, on Geranium thunbergii (≡ G. nepalense var. thunbergii) (Geraniaceae), 30 Sep. 2004, H.D. Shin, CBS H-20993, CBS 132657 =CPC 11598.

Notes: This species is basal to C. apii s. str. Fresh collections from Geranium (Geraniaceae) are needed from the USA (type locality of C. brunkii) to determine if the latter name can be applied to this species. The two isolates representing this species are never supported in their own clade; in the TEF and ACT phylogenies they are intermixed with C. cf. flagellaris, in the CAL phylogeny with C. apii and in the HIS phylogeny with C. kikuchii, C. cf. richardiicola and Cercospora spp. P and Q. These different shared alleles are the likely cause for their separate position in the combined phylogeny (Fig. 2 part 5).

Cercospora campi-silii Speg., Michelia 2: 171. 1880.

    • ≡ Cercosporidium campi-silii (Speg.) X.J. Liu & Y.L. Guo, Acta Mycol. Sin. 1: 94. 1982.

    • ≡ Passalora campi-silii (Speg.) Poonam Srivast., J. Living World 1: 114. 1994, nom. inval.

    • ≡ Passalora campi-silii (Speg.) U. Braun, Mycotaxon 55: 228. 1995.

  • = Cercospora impatientis Bäumler, Verh. K. K. Zool.-Bot. Ges. Wien 38: 717. 1888.

Leaf spots angular to irregular, 1-3 mm diam, center greyish to pallid, surrounded by purplish brown to dark brown border lines, but brown to greyish brown without definite borders on the abaxial surface. Caespituli hypophyllous, but also epiphyllous in later stage of disease development. Stromata lacking or composed of a few brown cells. Conidiophores arising in fascicles of 5-12(-18), loose to moderately dense, emerging through stomata or occasionally erumpent through the cuticle, subcylindrical, 2-5 times geniculate, sometimes abruptly geniculate, unbranched, 2-4-septate, 40-110 × 4-5.5 μm, pale brown to olivaceous-brown. Conidiogenous cells integrated, terminal, sympodial, multi-local; loci subcircular, thickened, darkened, 2.5-3 μm wide. Conidia solitary, obclavate-cylindrical to elliptical, 25-60 × 4.5-6 μm, (1-)3(-6)-septate, subhyaline, apex obtuse, base obconically subtruncate; hila ca. 2 μm wide, thickened, darkened.

Specimen examined: South Korea, Inje, on Impatiens noli-tangere (Balsaminaceae), 29 Sep. 2007, H.D. Shin, CBS 132625 =CPC 14585.

Notes: Although C. campi-silii was transferred from Cercospora to Passalora based on its pale olivaceous conidia (Braun 1995b), as in the case of C. sojina, these taxa are best retained in Cercospora, which is fully supported by their phylogenetic position within Cercospora. Cercospora campi-silii is separated based on the TEF, ACT and HIS phylogenies in the present study. Only the CAL phylogeny failed to distinguish it from C. sojina and C. achyranthis. On the combined tree (Fig. 2 part 2), it is a sister taxon to C. sojina. Cercospora campi-silii was described from Europe and examination of European material is necessary to determine similarity with Korean collections.

Cercospora canescens complex

Cultures examined: Ghana, on leaves of Dioscorea rotundata (Dioscoreaceae), 2000, S. Nyako & A.O. Danquah, CBS 132658 =CPC 11626 = GHA-1-0 (as C. dioscoreae-pyrifoliae); CPC 11628 = GHA-2-1; on leaves of Dioscorea alata, 2000, S. Nyako & A.O. Danquah, CBS 132659 =CPC 11627 = GHA-1-1. Mexico, Tamaulipas, unidentified Malvaceae host, 30 Oct. 2008, Ma. de Jesús Yáñez-Morales, CPC 15871. South Africa, Northwest Province, Potchefstroom, on Vigna sp. (Fabaceae), S. van Wyk, CBS 111133 =CPC 1137; CBS 111134 =CPC 1138; Tsipise, Limpopo Province, on Citrus maxima (Rutaceae) fruit spot, K. Serfontein, CPC 4408-4409. USA, Georgia, on Phaseolus lunatus (= Ph. limensis) (Fabaceae), E.S. Luttrell, CBS 153.55 = CPC 5059 (as C. canescens); on Apium sp., CPC 11640 = IMI 186563.

Notes: Morphologically the present clade represents isolates that correspond with the description of C. canescens, which was originally described from Phaseolus in the USA. It is possible that as more isolates are added, the lower subclade, which represents hosts in other families, may eventually split off as a distinct taxon. Epitype material from the USA is necessary to fix the application of the name C. canescens. The material on Ph. lunatus (= Ph. limensis) could be used in this sense, but C. canescens is a complicated species complex. More isolates from the USA are necessary to resolve this issue. A sequence of an isolate on Phaseolus from Mexico (CPC 15807) clusters in “Cercospora sp. Q”, which might be C. canescens. The C. canescens complex is supported as a distinct clade in the ACT and CAL phylogenies. The TEF sequence of isolate CPC 15871 splits off from the rest of the isolates to cluster with C. cf. coreopsidis. In the HIS phylogeny, the isolates occur in four distinct but related clades (C. mercurialis occurs in an intermediate position between these clades). These four clades correspond to the intraspecific variation observed for this species in Fig. 2 (part 1).

Cercospora capsici Heald & F.A. Wolf, Mycologia 3: 15. 1911.

Leaf spots circular to subcircular, more or less concentric, 2-10 mm diam. Caespituli amphigenous, appearing greyish brown in case of abundant sporulation. Mycelium internal. Stromata rudimentary, composed of a few swollen cells. Conidiophores straight to mildly curved, not branched, in divergent fascicles (3-15), mildly geniculate, 30-120 × 3-6 μm, 0-6-septate. Conidiogenous cells integrated, terminal, lateral, proliferating sympodially; loci distinct, slightly protuberant, apical and formed on shoulder caused by geniculation, 2-3 μm wide. Conidia solitary, hyaline, acicular, straight to mildly curved, 64-180 × 4-5.5 μm, 2-12-septate, subacute at the apex, obconically truncate at the base (adapted from Shin & Kim 2001).

Description of caespituli on V8 medium; MUCC 574 (MAFF 238227): Conidiophores solitary, pale brown to brown, irregular in width, wider at the base, smooth, moderately thick-walled, sinuous-geniculate, simple, conically truncated at the tip, 20-130.5 × 3.5-5 μm, multi-septate. Conidiogenous cells integrated, terminal; loci distinctly thickened, apical, 2-2.5 μm in width. Conidia solitary, hyaline, cylindro-obclavate to acicular, distinctly thickened and long obconically truncated at the base, obtuse to acute at the apex, 105-200 × 2.5-4.5 μm, 9-18-septate.

Specimens examined: Fiji, unknown host, fungus fruiting on lesions on calyx attached to fruit, 17 Aug. 2005, P. Tyler, CBS 118712. Japan, Chiba, on Capsicum annuum (Solanaceae), 1 Oct. 1999, S. Uematsu, MUCC 574 = MAFF 238227 = MUCNS 810. South Korea, Hongcheon, on C. annuum, 29 Aug. 2005, H.D. Shin, CBS H-20994, CPC 12307; Yanggu, on C. annuum, 28 Sep. 2007, H.D. Shin, CBS H-20995, CBS 132622 =CPC 14520.

Notes: See also C. armoraciae. This species is supported in the TEF (related to Cercospora sp. J and C. chenopodii), ACT (related to Cercospora sp. J and C. zebrina and C. armoraciae) and HIS (related to Cercospora spp. C and D) phylogenies and is part of the larger C. armoraciae clade based on CAL. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. armoraciae. Morphological characteristics of this species on the host plant and in culture are almost similar to C. armoraciae. In addition, acicular conidia are formed in culture. The application of the name C. capsici to this clade is only tentative, since the latter species was described from the USA. North American cultures and sequences are needed to confirm their identity.

Several species of Cercospora occur on solanaceous host plants. Of these, C. physalidis has been shown to form a species complex. Braun & Mel’nik (1997) concluded many species of Cercospora apii s. lat. on solanaceous hosts, including C. capsici, were synonymous with C. physalidis based on their morphological characteristics. Based on the results of pathogenicity tests (C. Nakashima, unpubl. data), phylogeny, and morphology (cylindrical to obclavate, rarely acicular conidia, and conidiophores that narrow at the upper portion), C. capsici must be separated from the C. physalidis complex. Likewise, other taxa in this complex such as C. lycii, C. nicandrae, C. sciadophila, C. solanacea, and C. solani, which consistently have obclavate-cylindrical conidia, must be re-examined.

Cercospora celosiae Syd., Ann. Mycol. 27: 430. 1929.

Leaf spots amphigenous, scattered to confluent, distinct, subcircular to irregular, small to fairly large, 1-7 mm diam, pale brown to brown, surrounded by a dark brown border. Caespituli amphigenous. Stromata small, rudimentary to slightly developed, composed of several brown, swollen hyphal cells. Conidiophores 3-20 in loose fascicles, emerging through stomata or erumpent through the cuticle, olivaceous-brown throughout, or paler upwards, 0-5-septate, straight to slightly curved, 1-5 times mildly geniculate, sometimes once abruptly geniculate, not branched, 25-200 × 4.5-6 μm; loci conspicuous, apical or on shoulders of conidiogenous cells caused by geniculation. Conidia solitary, acicular to filiform, sometimes shorter ones obclavate-cylindrical, straight to mildly curved, hyaline, 2-14-septate, slightly constricted at the septa, subacute to subobtuse at the apex, obconically truncate to subtruncate at the base, 40-150 × 3-5 μm; hilum conspicuously thickened, darkened, and non-protuberant

Specimen examined: South Korea, Chuncheon, on Celosia argentea var. cristata (≡ C. cristata) (Amaranthaceae), 7 Oct. 2003, H.D. Shin, CBS H-20996, CBS 132600 =CPC 10660.

Notes: The isolate representing C. celosiae is not supported as a separate clade; in the TEF, ACT, CAL and HIS phylogenies it is intermixed with predominantly Cercospora sp. I and C. alchemillicola / C. cf. alchemillicola, which is also evident from its position basal to Cercospora sp. I in the combined phylogeny (Fig. 2 part 1). Authentic material from China is required to determine if C. celosiae should be merged with what is presently treated as Cercospora sp. I.

Cercospora chenopodii Fresen., Beitr. Mykol.: 92. 1863. Fig. 4

Fig. 4.

Fig. 4.

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Cercospora chenopodii (CBS 132620 =CPC 14237). A. Leaf spots. B. Close-up of lesion. C-F. Conidiophores. G-I. Conidia. Scale bars = 10 μm.

  • = Ramularia dubia Riess, Hedwigia 1: pl. 4, fig. 9. 1854.

    • ≡ Cercospora dubia (Riess) G. Winter, Fungi Eur. Exs., Ed. nov., Cent. 28, No. 2780. 1882 and Hedwigia 22: 10. 1883, nom. illeg., homonym of C. dubia Speg., 1880.

    • ≡ Cercospora dubia (Riess) Bubák, Ann. Mycol. 6: 29. 1908, nom. illeg., homonym of C. dubia Speg., 1880.

    • ≡ Cercosporidium dubium (Riess) X.J. Liu & Y.L. Guo, Acta Mycol. Sin. 1: 95. 1982.

    • ≡ Passalora dubia (Riess) Poonam Srivast., J. Living World 1: 115. 1994, comb. inval.

    • ≡ Passalora dubia (Riess) U. Braun, Mycotaxon 55: 231. 1995.

  • = Cercospora chenopodii Cooke, Grevillea 12: 22. 1883, nom. illeg., homonym of C. chenopodii Fresen., 1863.

  • = Cercospora dubia var. urbica Roum., Rev. Mycol. 15: 15. 1893.

  • = Cercospora dubia var. atriplicis Bondartsev, Trudy Glavn. Bot. Sada 26: 51. 1910.

  • = Cercospora atriplicis Lobik, Mat. po Fl. Faun. Obsled. Terskogo Okruga: 52. 1928.

  • = Cercospora chenopodii var. micromaculata Dearn., Mycologia 21: 329. 1929.

  • = Cercospora penicillata f. chenopodii Fuckel, Fungi Rhen. Exs., Fasc. II, No. 119. 1863, nom. nud.

  • = Cercospora chenopodii var. atriplicis patulae Thüm., in herb.

  • = Cercospora bondarzevii Henn., in herb. B.

Specimen examined: France, Ardeche, N44°22’39.8” E4°26’9.1”, on Chenopodium cf. album (Chenopodiaceae) next to river, 31 Aug. 2007, P.W. Crous, CBS H-20997, CBS 132620 =CPC 14237.

Notes: Cercospora chenopodii was transferred to the genus Passalora as P. dubia by Braun (1995a) based on broadly obclavate conidia with visible large loci. The conidia of this species are hyaline, and best retained in Cercospora, which has been confirmed by results of molecular sequence analyses. The species is supported as distinct in the TEF, ACT and HIS phylogenies; in the CAL phylogeny it cannot be distinguished from C. cf. chenopodii. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. cf. chenopodii. Also see C. cf. chenopodii.

Cercospora cf. chenopodii Fig. 5.

Fig. 5.

Fig. 5.

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Cercospora cf. chenopodii (CPC 10304). A. Leaf spots. B. Close-up of lesion. C-E. Fasciculate conidiophores. F-I. Conidia. Scale bars = 10 μm.

Leaf spots amphigenous, subcircular, circular, 3-8 mm diam, greyish brown to pale brown. Mycelium internal, consisting of septate, branched, smooth, pale brown hyphae. Caespituli in fascicles (10-40), amphigenous, brown, dense, becoming divergent, up to 150 μm wide and 50 μm high. Conidiophores aggregated in dense fascicles arising from the upper cells of a moderately developed brown stroma; conidiophores olivaceous-brown to brown, 2-5-septate, 1-2 times geniculate in upper part, at times apically swollen, not branched, 60-135 × 4-7 μm. Conidiogenous cells terminal, unbranched, pale brown, smooth, tapering to flat-tipped apical loci, proliferating sympodially, 20-40 × 4-6 μm; loci thickened, darkened, refractive, 2-4 μm diam. Conidia solitary, smooth, cylindrical to obclavate, straight to slightly curved, hyaline, (0-)2-4(-5)-septate, apex obtuse, base obconically truncate, (25-)40-65(-80) × (5-)6-7.5(-9) μm; hila thickened, darkened, refractive, 2-3 μm diam.

Culture characteristics: Colonies erumpent, spreading, with sparse aerial mycelium, and lobate, smooth margins, and folded surface; reaching 10 mm after 2 wk. On MEA iron-grey with patches of dirty white, reverse fuscous-black to greyish sepia. On OA and PDA surface mouse-grey, with patches of pale mouse-grey, reverse olivaceous-grey.

Specimens examined: Mexico, Montecillo, Chenopodium sp. (Chenopodiaceae), 9 Oct. 2008, Ma. de Jesús Yáñez-Morales, CBS 132677 =CPC 15599; CPC 15763; Purificacion, Chenopodium sp., 12 Oct. 2008, Ma. de Jesús Yáñez-Morales, CPC 15859; CPC 15862. South Korea, Hongcheon, on Chenopodium ficifolium (Chenopodiaceae), 4 Oct. 2002, H.D. Shin, CBS H-20998, culture CBS 132594 =CPC 10304; Hongcheon, on C. ficifolium, 27 Oct. 2005, H.D. Shin, CBS H-20999, CPC 12450.

Notes: The chief difference between C. chenopodii and C. cf. chenopodii lies in the denser fascicles observed in the former species. Otherwise, the two species are barely distinguishable, and the latter species has to be considered a cryptic taxon. In the TEF phylogeny these two species are clearly distinct, although the isolates of C. cf. chenopodii are intermixed with those of C. delaireae, C. ricinella and Cercospora sp. K. The ACT and HIS phylogenies separate C. cf. chenopodii from the other species included in this study, although the CAL phylogeny could not distinguish C. chenopodii and C. cf. chenopodii. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. chenopodii. See the species notes for C. chenopodii. We refrain from describing this species as new until more isolates for C. chenopodii can be sequenced to determine the intraspecific variation.

Cercospora chinensis F.L. Tai, Bull. Chin. Bot. Soc. 2: 49. 1936.

Caespituli amphigenous. Mycelium internal. Stromata lacking to small, up to 30 μm diam, dark brown, intraepidermal or substomatal. Conidiophores solitary to 2-5 in loose fascicles, simple, sometimes branched, thick-walled, dark brown, paler towards the apex, mainly straight, loosely geniculate, almost uniform in width, conically truncated and somewhat wider at the apex, 61-100 × 5-6 μm, 3-6-septate. Conidiogenous cells integrated, proliferating sympodially or rarely percurrently, terminal and intercalary, multi-local; loci thickened, not protuberant, apical, lateral, 2.5-3 μm diam. Conidia solitary, hyaline, acicular to cylindro-obclavate, slightly curved, obconically truncate or subtruncate, and thickened at the base, acute at the apex, 60-210 × 3.5-5 μm, 2-16-septate.

Specimen examined: South Korea, Pyeongchang, on Polygonatum humile (Convallariaceae), 20 Sep. 2003, H.D. Shin, CBS H-21000, CBS 132612 =CPC 10831.

Notes: See the notes for C. dispori below. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. dispori and C. corchori.

Cercospora cf. citrulina

Caespituli amphigenous. Mycelium internal. Stromata lacking or small, up to 20 μm, pale brown. Conidiophores pale to pale brown, paler towards the apex, irregular in width, wider at the base, narrowed successive geniculation at the apex, sinuous-geniculate to well geniculate above the middle, thin-walled when young, darker and moderately thickened in mature conidiophores, solitary or in loose fascicles (2-14), simple, truncate at the apex, 50-86 × 2.5-5 μm, 0-3-septate. Conidiogenous cells integrated, terminal, rarely intercalary, proliferating sympodially, multi-local; loci distinct, thickened, apical or on shoulder caused by geniculation, slightly protuberant, 2.5-3 μm diam. Conidia solitary, hyaline, cylindrical, filiform to acicular, straight to slightly curved, truncate to long obconically truncate and distinctly thickened at the base, apex subacute, 40-134 × 3-4 μm, multi-septate.

Specimens examined: Bangladesh (western part), on Musa sp. (Musaceae), I. Buddenhagen, CBS 119395 =CPC 12682; CBS 132669 =CPC 12683. Japan, Kagoshima, on Momordica charanthia (Cucurbitaceae), 20 Oct. 1997, E. Imaizumi & C. Nomi, MUCC 577 = MAFF 238205 = MUCNS 254 (as C. citrullina); Okinawa, on Citrullus lanatus (Cucurbitaceae), 6 Mar. 1998, T. Kobayashion et al., MUMH 11402, MUCC 576 = MUCNS 300 = MAFF 237913 (as C. citrullina); on Psophocarpus tetragonolobus (Fabaceae), MUCC 584 = MAFF 305757 (as C. psophocarpicola); on Ipomoea pes-caprae (Convolvulaceae), MUCC 588 = MAFF 239409 (as C. ipomoeae).

Notes: This clade is supported by the TEF, ACT and CAL phylogenies. In the HIS phylogeny, the clade is split into the two sister clades visible in the combined tree, and may eventually be shown to be a species complex. In the HIS phylogeny, MUCC 584, MUCC 576 and MUCC 577 are clustering sister to C. chinensis and C. dispori whereas the remaining isolates are sister to C. vignigena. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. cf. helianthicola.

This taxon is distinguished from other species based on several morphological characteristics. Sporulation is mainly observed at the apex of conidiophores; slightly protuberant loci are formed on shoulders caused by geniculation; the width of conidiogenous cells immediately behind the fertile region is generally narrower, and conidiogenous cells are truncate at the apex. An isolate obtained from Ipomoea pes-caprae (MUCC 588) is located in this clade (Fig. 2 part 5). It was not possible to examine its morphology in this study and thus it is not clear whether or not this fungus was saprobic. An isolate identified as C. psophocarpicola (MUCC 584), is also located in this clade. There is no morphological basis to divide C. psophocarpicola and other isolates in this clade into different species. Besides, the pathogenicity of MUCC 584 to Psophocarpus (Fabaceae) was confirmed (Ohnuki et al. 1989), thus showing that this species was not saprobic. Moreover, the four Japanese isolates examined in this study were obtained from the same subtropical islands in Japan. On the other hand, two isolates named as “C. hayi” from Musa sp. were also located in this clade. According to Crous et al. (2004b), several species of Cercospora are known to be able to colonise Musa. From the distribution of this taxon, it is natural that this species also colonised Musa (Musaceae), which grows in the same region.

Cercospora coniogrammes Crous & R.G. Shivas, sp. nov. MycoBank MB800653. Fig. 6.

Fig. 6.

Fig. 6.

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Cercospora coniogrammes (CBS 132634 =CPC 17017). A. Leaf spots. B. Close-up of lesion. C-F. Weakly developed fascicles, showing conidiophores with sympodial proliferation and multi-local loci. G-I. Cylindrical to acicular conidia. Scale bars = 10 μm.

Etymology: Named after the host genus from which it was collected, Coniogramme.

Leaf spots amphigenous, subcircular to angular, 1-3 mm diam, grey to pale brown, surrounded by a broad brown margin, up to 4 mm diam. Mycelium internal. Caespituli predominantly epiphyllous. Conidiophores aggregated in loose fascicles (2-6), arising from the upper cells of a brown, weakly developed stroma, up to 20 μm diam, brown, finely verruculose in lower part, 3-7-septate, subcylindrical, straight to geniculate-sinuous, unbranched, 60-120 × 5-7 μm. Conidiogenous cells integrated, terminal, unbranched, brown, smooth, tapering to flat-tipped loci, proliferating sympodially, 15-35 × 3-5 μm, with numerous tightly aggregated apical loci, proliferating sympodially; loci distinct, thickened and darkened, protruding, 2-2.5 μm diam. Conidia solitary, hyaline, cylindrical to acicular, straight or slightly curved, apex subobtuse, base truncate, (30-)50-85(-120) × (2-)3(-3.5) μm, 1-6-septate, thin-walled, smooth; hila thickened, darkened, refractive, 1.5-2 μm diam.

Culture characteristics: Colonies spreading, flat, with sparse aerial mycelium, folded surface and even margins, reaching 25 mm after 2 wk. On OA blood-red in centre, red at margin. On MEA grey-olivaceous in centre, smoke-grey at margins, olivaceous-grey in reverse. On PDA umber to chestnut in centre, bay at margin, umber in reverse.

Specimen examined: Australia, Queensland, Brisbane, on Coniogramme japonica var. gracilis (≡ C. gracilis) (Adiantaceae), holotype CBS H-21001, Aug. 2009, P.W. Crous, culture ex-type CBS 132634 =CPC 17017.

Notes: The numerous, tightly aggregated loci on the conidiogenous cells, and cylindrical to acicular conidia are characteristic of this species. This species is supported on the TEF, ACT, CAL and HIS phylogenies and is basal in the combined tree (Fig. 2 part 1).

Cercospora corchori Sawada, Trans. Nat. Hist. Soc. Formosa 26: 179. 1916.

Caespituli amphigenous. Mycelium internal. Stromata lacking to small, substomatal or intraepidermal, pale brown to brown, 16-25 μm diam. Conidiophores arising from upper part of stromata or internal hyphae, in loose fascicles (5-10), moderately thick-walled, pale brown to brown, uniform in width, sometimes attenuated at the apex, sinuous-geniculate, sparsely septate, conically truncate at the apex, 20-83 × 4-5 μm. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, multi-local; loci distinct, thickened and darkened, apical or formed on the shoulder caused by the geniculation, 1-3 μm diam. Conidia hyaline to subhyaline, cylindro-obclavate to acicular, straight or slightly curved, truncate and thickened at the base, acute at the apex, 30-128 × 2.5-5 μm, 4-13-septate.

Description of caespituli on MEA; MUCC 585 (= MAFF 238191): Conidiophores solitary, brown, uniform in width, smooth, moderately thick-walled, slightly curved, simple, conically truncated at the apex, 130-230 × 3.5-4.5 μm, multi-septate. Conidiogenous cells integrated, terminal; loci moderately thickened, apical, 2.5-2.5 μm in width.

Specimens examined: Japan, Shimane, on Corchorus olitorius (Tiliaceae), 27 Aug. 1997, T. Mikami (epitype designated here - TFM:FPH-8114), culture ex-epitype MUCC 585 = MAFF 238191 = MUCNS 72. Taiwan, Taipei, on C. olitorius, 30 Jul. 1909, K. Sawada, (isotype - TNS-F-220392).

Notes: Cercospora corchori, which is known as the causal agent of a seed-borne disease, is distinguished from other species in that conidiophores are uniform in width, and conically truncate at the apex. Moreover, the species is supported by the ACT, CAL and HIS phylogenies. In the TEF phylogeny, it clusters on a longer branch in a clade with isolates of Cercospora sp. K and C. lactucae-sativae. In the combined tree (Fig. 2 part 5), it is a sister taxon to Cercospora spp. R and S.

Cercospora cf. coreopsidis

Leaf spots distinct (characteristic for this species), circular to subcircular, initially pale brown, later centre grey to dirty grey with raised greyish brown margins. Caespituli amphigenous. Mycelium internal. Stromata lacking or small, up to 30 μm in diam, intraepidermal or substomatal, brown. Conidiophores solitary, or up to 2-9 in loose fascicles, irregular in width, slightly attenuated at the apex, somewhat wider at mid cells, pale brown, thick-walled, paler towards the apex, conically truncate at the apex, geniculate at the upper portion, tortuous, 30-156 × 4-5.5 μm, 1-7-septate. Conidiogenous cells integrated, intercalary, terminal, proliferating sympodially, multi-local; loci thickened, darkened, not protuberant, flat, apical, lateral, rarely circumspersed, 1.5-2 μm. Conidia solitary, hyaline, filiform to acicular, straight to curved, truncated and thickened at the base, tip acute, 40-90(-180) × (1.5-)3-5 μm, indistinctly 7-10-septate.

Specimen examined: South Korea, Seoul, Coreopsis lanceolata (Asteraceae), 17 Sep. 2003, H.D. Shin, CBS H-21002, CBS 132598 =CPC 10648; Wonju, on C. lanceolata, 18 Oct. 2002, H.D. Shin, CPC 10122.

Notes: The description of the present species is based on Korean specimens. Many species of Cercospora have latent pathogenicity to asteraceous plants. Although these results show that the identification of Cercospora species on these plants is difficult based on the host plant, the isolates originating from Coreopsis must be treated as a host-specific species in having an independent phylogenetic position, which is supported by the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. agavicola.

On the other hand, C. beticola, which has also been known from Bidens (Asteraceae), was also reported from Coreopsis (Asteraceae) (Thaung 1984). Morphological differences between these species were not observed. The identification of the Korean collections as C. cf. coreopsidis is only tentative and must be proven on the base of sequences derived from North American isolates, which are not yet available.

Cercospora delaireae C. Nakash., Crous, U. Braun & H.D. Shin, sp. nov. MycoBank MB800654. Fig. 7.

Fig. 7.

Fig. 7.

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Cercospora delaireae (CBS 132595 =CPC 10455). A. Leaf spots. B. Close-up of lesion. C-F. Conidiophores giving rise to conidia. G, H. Conidia. Scale bars = 10 μm.

Etymology: Named after the host genus from which it was collected, Delairea.

Leaf spots amphigenous, subcircular to angular, grey-brown to brown, 3-7 μm diam, surrounded by a large, brown border, 7-15 mm diam. Caespituli amphigenous, mainly hypophyllous. Mycelium internal. Stromata lacking or composed of few brown cells, substomatal or intraepidermal. Conidiophores solitary or in loose fascicles (2-4), pale brown to brown, irregular in width, narrowed at upper portion, moderately thick-walled, smooth, straight or abruptly once geniculate, truncate at the tip, 20-120 × 5-6.5 μm, 1-9-septate. Conidiogenous cells integrated, terminal, rarely intercalary, proliferating sympodially, 20-60 × 4-6 μm, usually unilocal, rarely multi-local; loci apical or formed on the shoulder due to sympodial proliferation, 2-4 μm diam, thickened and darkened. Conidia solitary, hyaline, filiform to acicular, truncate at the base, tip acute, (55-)80-150(-200) × (3.5-)4(-5) μm, 3-15-septate, thin-walled, smooth; hila thickened, darkened, 2-4 μm diam.

Culture characteristics: Colonies erumpent, spreading, with sparse to moderate aerial mycelium, and smooth, lobed margin and folded surface; reaching 20 mm diam after 2 wk. On MEA surface dirty white to salmon with patches of olivaceous-grey; reverse iron-grey in centre, salmon in outer region. On PDA surface dirty white with patches of pale mouse-grey, and red, diffuse pigment surrounding culture; reverse olivaceous-grey, but with prominent red pigment. On OA spreading, flat, lacking aerial mycelium, with lobate, smooth margins; surface red with diffuse red pigment surrounding colony; reverse red.

Specimens examined: South Africa, Eastern Cape Province, Plettenberg Bay, on Delairea odorata (= Senecio mikaniodes) (Asteraceae), C.L. Lennox, CPC 10627-10629; Mpumalanga, Long Tom Pass, on D. odorata (= Senecio mikanioides), 16 Jun. 2003, S. Neser, holotype CBS H-21004, culture ex-type CBS 132595 =CPC 10455.

Notes: Cercospora delaireae must be regarded as a new species based on its distinct phylogenic position (Fig. 2 part 2). In the individual gene trees it is distinguished in the ACT, CAL and HIS phylogenies; in the TEF phylogeny it cannot be distinguished from C. cf. chenopodii. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. ricinella. It appears to be specific to Delairea odorata (= Senecio mikanioides) (Cape-ivy), and should be further evaluated as possible biocontrol agent of this host. Delairea odorata is an invasive perennial vine problematic in coastal riparian areas and is reported as being toxic to animals and fish. Stem, rhizome and stolon fragments resprout if left in the ground after treatment (for further information see <www.cal-ipc.org/ip/management/plant_profiles/Delairea_odorata.php>).

Cercospora dispori Togashi & Maki, Trans. Sapporo Nat. Hist. Soc. 17: 98. 1942.

Caespituli amphigenous. Mycelium internal. Stromata lacking to small, up to 40 μm diam, dark brown, intraepidermal or substomatal. Conidiophores solitary, or up to 2-10 in loose fascicles, thick-walled, dark brown, paler towards the apex, straight or sinuous-geniculate, almost uniform in width, conically truncate at the apex, 45-100 × 3.5-5.5 μm, 1-7-septate. Conidiogenous cells integrated, proliferating sympodially or rarely percurrently, terminal and intercalary, multi-local; loci thickened, not protuberant, apical, lateral. Conidia solitary, hyaline, acicular to cylindrical, slightly curved, obconically truncate or subtruncate, and thickened at the base, acute or obtuse at the apex, 30-85(-200) × 3.5-5 μm, 2-12-septate, thin-walled, smooth.

Specimens examined: Japan, Fukuoka, on Disporum smilacinum var. ramosum (Convallariaceae), 22 Sep. 1940, Y. Maki & T. Katsuki, holotype in SAPA? (specimen could not be located). South Korea, Pyeongchang, on Disporum viridescens (Convallariaceae), 20 Sep. 2003, H.D. Shin, CBS 132608 =CPC 10773; CPC 10774-10775.

Notes: Cercospora chinensis and C. dispori are distinguished from other C. apii s. lat. species in that their conidiophores are uniform in width, thick-walled, dark coloured and conically truncate at the apex. In this study, C. chinensis and C. dispori occur on Convallariaceae, and cluster together in a well-supported clade. On the individual gene trees, these two species (represented by isolates CPC 10831 and CPC 10773) rarely cluster and are both on long branches in the phylogenetic analyses. In the TEF phylogeny, C. dispori cannot be distinguished from C. apii / C. beticola whereas C. chinensis is a sister taxon to C. pileicola. In the ACT phylogeny, C. chinensis cannot be distinguished from C. apii / C. beticola and C. dispori is a sister taxon to the C. apii / C. beticola clade. In the CAL phylogeny the two species are indistinguishable and they are related to C. lactucae-sativae. In the HIS phylogeny the two species are sister taxa related to C. citrullina. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. chinensis. Based on morphological characteristics, there is a difference between the two species in that the conidiophores of C. chinensis are sometimes branched. Thus, these two species are retained as separate taxa.

Cercospora cf. erysimi

Specimen examined: New Zealand, Manurewa, on Erysimum mutabile (Brassicaceae), 5 Dec. 2002, C.F. Hill, Lynfield 625, CBS 115059 =CPC 5361.

Notes: This species is phylogenetically supported by TEF, ACT, CAL and HIS. A collection on Erysimum (Brassicaceae) from Europe (isolate CPC 5056) clusters within C. armoraciae. The latter could also be the “true C. erysimi”, which is still unclear. The type of C. erysimi is from North America. Thus, fresh material is needed from North America to resolve the application of the name “C. erysimi”. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. cf. modiolae and Cercospora sp. E.

Cercospora euphorbiae-sieboldianae C. Nakash., Crous, U. Braun & H.D. Shin, sp. nov. MycoBank MB800655. Fig. 8.

Fig. 8.

Fig. 8.

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Cercospora euphorbiae-sieboldianae (CBS 113306). A. Leaf spots. B. Close-up of lesion. C, D. Fasciculate conidiophores. E. Conidiophore giving rise to conidium. F-I. Conidia. Scale bars = 10 μm.

Etymology: Named after the host from which it was collected, Euphorbia sieboldiana.

Leaf spots amphigenous, subcircular to irregular, 3-15 mm diam, coalenscing, up to 25 mm diam, brown to greyish brown, becoming whitish grey in centre, with blackish margins on upper surface, and greyish white to grey on lower surface. Mycelium internal. Caespituli amphigenous. Stromata small to well-developed, intraepidermal to substomatal, brown to dark brown, 20-125 μm. Conidiophores loose to densely fasciculate in fascicles of 3-40, pale brown to brown, paler towards the apex, irregular in width, somewhat constricted at the proliferating point, conically truncate at the apex, 0-2-septate, straight or sinuous to geniculate due to sympodial proliferation, simple, rarely branched, 15-170 × 4.5-8 μm. Conidiogenous cells integrated, terminal, rarely intercalary, proliferating sympodially, 50-70 × 4-5 μm, multi-local; loci distinctly thickened, darkened, apical or formed on the shoulder, rarely lateral, 3-4.5 μm diam. Conidia solitary, hyaline to subhyaline, solitary, straight to slightly curved, obclavate to obclavate-cylindric, obconically truncated at the base, acute to obtuse at the apex, often beak-like at the apex, 38-130 × 5.5-8(-12) μm, (4-)3-6(-12)-septate, thin-walled, smooth; hila thickened, darkened, 3-4.5 μm diam.

Culture characteristics: Colonies erumpent, spreading, with sparse aerial mycelium and smooth, even margins, reaching 30 mm diam after 2 wk at 25 °C in the dark. On MEA surface grey-olivaceous, reverse iron-grey. On PDA surface and reverse olivaceous-grey. Colonies forming spermatogonia in culture on both media.

Specimen examined: South Korea, Samcheok, on Euphorbia sieboldiana (Euphorbiaceae), 8 May 2003, H.D. Shin, holotype CBS H-21005, culture ex-type CBS 113306.

Notes: This species is phylogenetically distinguishable from its closest relatives in the TEF, ACT, CAL and HIS phylogenies. It is related to C. polygonaceae (TEF), C. senecionis-walkeri (ACT), C. vignigena (CAL) and C. punctiformis (HIS); therefore it is distinct from the other species occurring on Euphorbiaceae included in this study. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. punctiformis. It is morphologically well distinguished from species of the C. apii complex and other species of Cercospora by its unusually broadly obclavate-cylindrical conidia (5.5-8(-12) μm) with few septa and rather broad loci and hila (3-4.5 μm).

Cercospora fagopyri K. Nakata & S. Takim., J. Agric. Exp. Stat. Gov. Gen. Chosen 15: 29. 1928.

  • = Cercospora fagopyri Abramov, in Lavrov, Opred. rastit. paras. kul’t. i dikor. polezn. rast. Sibiri, Vyp. I: 22. 1932, nom. nud.

    • ≡ Cercospora fagopyri Abramov, in Vasilevsky & Karakulin, Fungi imperfecti parasitici. 1. Hyphomycetes: 321. 1937, nom. illeg. (homonym).

  • = Cercospora fagopyri Chupp & A.S. Mull., Bol. Soc. Venez. Ci.. Nat. 8: 44. 1942, nom. illeg. (homonym).

Caespituli caulogenous, or amphigenous on leaves. Mycelium internal. Stromata intraepidermal or substomatal, pale brown, small to well-developed, 25-60 μm diam. Conidiophores pale brown, solitary, or in loose to dense fascicles (2-20), sinuously geniculate, rarely geniculate due to sympodial proliferation, usually irregular in width, frequently constricted due to proliferation, attenuated at the tip, truncate at the apex, multi-septate, 20-120 × 3.5-5.5 μm, 0-5-septate. Conidiogenous cells integrated, mainly terminal, rarely intercalary, proliferating sympodially, multi-local; loci thickened and darkened, apical and formed on the shoulder caused by sympodial proliferation, sometimes lateral, sometimes protuberant, 1.5-2.5 μm. Conidia solitary, hyaline, cylindrical to acicular, straight or slightly curved, long obconically truncate or truncate at the thickened and darkened base, obtuse or acute at the apex, 20-100 × 3-4 μm, 3-20-septate, thin-walled, smooth.

Description of caespituli on V8; (MUCC 130): Caespituli dimorphic, either small (common), or large (rarely observed; described in parenthesis). Conidiophores solitary to loosely fasciculate, arising from hyphae, subhyaline to pale brown, irregular in width, smooth, meager and thin-walled, sinuous-geniculate to geniculate (straight to geniculate), unbranched, truncated at the tip, 15-500 × 3-5 μm, multi-septate. Conidiogenous cells integrated, terminal or intercalary, proliferating sympodially, multi-local (uni-local); loci moderately thickened, apical, protuberant (not protuberant), 1.25-3 μm in width. Conidia solitary, hyaline, filiform to acicular, slightly thickened and obconically truncate (truncate) at the base, acute at the apex, 45.5-187 × 2-4.5 μm, 3-16-septate.

Specimens examined: Japan, Ehime, on Cosmos bipinnata (Asteraceae), 16 Oct. 2004, J. Nishikawa, MUMH 11394, MUCC 130; on Hibiscus syriacus (Malvaceae), MUCC 866. South Korea, Suwon, on Viola mandshurica (Violaceae), 14 Oct. 2003, H.D. Shin, CBS H-21006, CBS 132649 =CPC 10725; Yangpyeong, on Cercis chinensis, (Fabaceae), 19 Oct. 2007, H.D. Shin, CBS H-21007, CBS 132671 =CPC 14546; on Fagopyrum esculentum (Polygonaceae), 9 Oct. 2007, H.D. Shin, neotype designated here CBS H-21008, culture ex-neotype CBS 132623 =CPC 14541 (holotype specimen, South Korea, Suwon, on Fag. esculentum, Sep. 1934, K. Nakata & S. Takimoto, could not be located and is undoubtedly not preserved); on Fallopia dumentorum (Polygonaceae), 16 Oct. 2002, H.D. Shin, CBS H-21009, CBS 132640 =CPC 10109.

Notes: Phylogenetically the separation of C. fagopyri is supported by the TEF and HIS phylogenies, though it is intermixed with strains of C. cf. sigesbeckiae in the ACT phylogeny and of C. kikuchii in the CAL phylogeny. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. cf. ipomoeae. Presently several isolates originating from diverse host families reside in this clade. However, lesions on Viola appear to be insect associated, and caused by a Colletotrichum species, with Cercospora colonisation being secondary. Furthermore, lesions on Fallopia dumentorum appear to be associated with chemical damage, not Cercospora, again suggestion that Cercospora colonisation was secondary. The fungus occurring on Cercis chinensis is distinct, having very long conidiophores (200-600 μm), and very long conidia. To resolve the host range of C. fagopyri, isolates from Fagopyrum need to be recollected in Korea, and pathogenicity established on the hosts listed above. Thus the name C. fagopyri can only be applied to other isolates than those from Fagopyrum tentatively, awaiting additional fresh collections.

Cercospora cf. flagellaris

Caespituli amphigenous. Mycelium internal. Stromata lacking to well-developed, up to 50 μm diam, brown, intraepidermal and substomatal. Conidiophores straight or successively geniculate at the apex, rarely abruptly geniculate, solitary, or in loose to dense fascicles (2-23), pale brown to brown, paler towards the apex, simple, rarely branched, uniform in width up to the middle, strongly attenuated at the upper portion, sometimes constricted at septa, often constricted following sympodial proliferation, 14-140(-270) × 2.5-6.5 μm, 0-8-septate, truncate or short obconically truncated at the apex. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, multi-local (2-5); loci distinctly thickened, apical or formed on the shoulders caused by geniculation, lateral, rarely protuberant, small, 1-4 μm. Conidia solitary, hyaline, cylindrical to acicular, sometimes obclavate, straight or slightly curved, truncate or short obconical truncate at the thickened and darkened base, acute at the apex, 18-240 (-300) × 2-4.5 μm, 1-12-septate, thin-walled, smooth.

Description of caespituli on V8; MUCC 127: Conidiophores solitary, arising from hyphae, pale brown, uniform in width, sometimes wider at the base, smooth, straight to slightly sinuous, conically truncate at the tip, 10-95 × 3-5 μm, multi-septate. Conidiogenous cells integrated, terminal; loci distinctly thickened, apical, 1.25-2 μm in width. Conidia hyaline, acicular to filiform, slightly thickened and truncate at the base, acute at the apex, 35-220 × 2-3 μm, 2-15-septate.

Specimens examined: Fiji, on Amaranthus sp. (Amaranthaceae), C.F. Hill, Lynfield 677, CPC 5441. Israel, on Trachelium sp. (Campanulaceae), 16 Nov. 2002, E. Tzul-Abad, CBS 132637 =CPC 10079 (as C. campanulae). Japan, Ehime, on Cosmos sulphureus (Asteraceae), 16 Oct. 2004, J. Nishikawa, MUMH 11393, MUCC 127; Tokyo, on Hydrangea serrata (Hydrangeaceae), 10 Nov. 2007, I. Araki & M. Harada, MUMH 10933, MUCC 831; Wakayama, on H. serrata, 30 Oct. 2007, C. Nakashima & I. Araki, MUMH 10860, MUCC 735. South Korea, Hoengseong, on Celosia argentea var. cristata (≡ C. cristata), 11 Oct. 2004, H.D. Shin, CBS 132667 =CPC 11643 (as Cercospora sp.); Jeju, on Dysphania ambrosioides (≡ Chenopodium ambrosioides) (Chenopodiaceae), 12 Nov. 2003, H.D. Shin, CBS 132653 =CPC 10884 (as C. chenopodii-ambrosioidis); on Phytolacca americana (Phytolaccaceae), 1 Nov. 2007, H.D. Shin, CBS 132674 =CPC 14723; CPC 14724; Jinju, on P. americana, 15 Oct. 2003, H.D. Shin, CPC 10684-10686; Namyangju, on Amaranthus patulus, 30 Sep. 2003, H.D. Shin, CBS 132648 =CPC 10722; Pocheon, on P. americana, 23 Oct. 2002, H.D. Shin, CPC 10124; Suwon, on Cichorium intybus (Asteraceae), 14 Oct. 2003, H.D. Shin, CBS 132646 =CPC 10681 (as C. cichorii); Yanggu, on Sigesbeckia pubescens (Asteraceae), 28 Sep. 2007, H.D. Shin, CBS 132670 =CPC 14487. South Africa, Limpopo Province, Messina, Citrus sp. (Rutaceae), M.C. Pretorius, CBS 115482 =CPC 4410; CPC 4411; on Populus deltoides (Salicaceae), P.W. Crous, CPC 1051-1052. Unknown, on Bromus sp. (Poaceae), M.D. Whitehead, CBS 143.51 = CPC 5055. USA, Texas, on Eichhornia crassipes (Pontederiaceae), R. Charudattan & D. Tessmann, 14 Sep. 1996, CBS 113127 (as C. piaropi).

Notes: The isolates from this species form a monophyletic clade identical to one another and the two isolates of C. cf. brunkii on the TEF phylogeny. In the CAL phylogeny the C. cf. flagellaris isolates form a monophyletic clade, albeit with some intraspecific variation. Based on ACT data, the clade splits into four lineages: 1. CPC 4410 and 4411, 2. CPC 1052, 1051 and 10681, 3, CPC 5441 and, 4. the remainder of the isolates. In the HIS phylogeny the species also splits into four lineages: 1. CPC 4410, 4411, 10884 and MUCC 735, 2. CPC 10681 and 11643, 3. CPC 5441 and, 4. the rest of the isolates. These splits in phylogeny (see Fig. 2 parts 2-3) are not supported by morphology: conidiophores are successively geniculate at the upper portion, strongly attenuated at the apex; conidiogenous cells are terminal and intercalary with multi-local loci, and conidia are truncate or short obconically truncate at the thickened base. We strongly suspect that this is a species complex. The latter can only be resolved once more authentic isolates for the names listed above are included (from original hosts and countries), additional DNA loci screened, and pathogenicity tests conducted. Included in this species complex is the isolate used by Tessmann et al. (2001) as C. piaropi. This isolate is indistinguishable from other isolates of C. cf. flagellaris based on the TEF, ACT, CAL and HIS phylogenies. Cercospora flagellaris is the older name (1882) compared to C. piaropi (1917) and should therefore get taxonomic preference.

Cercospora cf. helianthicola

Caespituli amphigenous. Mycelium internal. Stromata brown, lacking or small, intraepidermal or substomatal, up to 25 μm diam. Conidiophores simple, occasionally branched, straight to geniculate, pale brown, arising from small stromata or internal hyphae, solitary or in dense fascicles (up to 15), irregular in width, narrowed at successive geniculation, truncate at the apex, moderately thick-walled, 20-180 × 3-4 μm, septate. Conidiogenous cells integrated, terminal, proliferating sympodially, multi-local; loci distinctly thickened, apical and formed on the shoulders caused by geniculation, rarely lateral, refractive, 1.5-2 μm. Conidia solitary, acicular to cylindrical, hyaline, straight or curved, truncate and distinctly thickened at the base, obtuse at the apex, 10-85 × 3-4 μm, indistinctly multi-septate, thin-walled, smooth.

Specimen examined: Japan, Wakayama, on Helianthus tuberosus (Asteraceae), 30 Oct. 2007, C. Nakashima & I. Araki, MUMH 10844, MUCC 716.

Notes: This species is distinguished from other taxa in that it has slightly protuberant apical loci that are at times formed on shoulders caused by geniculation. The width of its conidiogenous cells is somewhat narrower behind the fertile region, and has a truncate apex. Furthermore, its conidiophores are rarely branched. A possible name that could be applied is C. helianthicola, though the latter species was originally described from South America, and fresh collections would be required to confirm its phylogenetic position. The isolate used in the current study is distinct in the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. cf. citrulina.

Cercospora cf. ipomoeae

Caespituli amphigenous. Mycelium internal. Stromata composed of few brown cells, or well-developed, up to 60 μm diam, intraepidermal or substomatal. Conidiophores in loose fascicles (2-8), pale brown, paler towards apex, straight or geniculate at the apex, irregular in width, tip conically truncate, narrowed at the apex, 22.5-92.5 × 3.5-5.5 μm, 0-4-septate. Conidiogenous cells integrated, terminal, proliferating sympodially, multi-local; loci thickened, darkened, apical, rarely lateral, rarely slightly protuberant, 2-2.5 μm diam. Conidia solitary, hyaline, filiform to acicular, slightly curved, obconically truncate or truncate, and thickened and darkened at the base, acute or obtuse at the apex, 50-135(-245) × 2.5-3(-7.5) μm, 3-19-septate, thin-walled, smooth.

Specimens examined: Japan, Kagawa, on Ipomoea aquatica (Convolvulaceae), Aug. 2005, G. Kizaki, MUMH 11203, MUCC 442; South Korea, Chuncheon, on Ipomoea nil (= I. hederacea) (Convolvulaceae), 7 Oct. 2003, H.D. Shin, CBS H-21010, CBS 132652 =CPC 10833; Pocheon, on Persicaria thunbergii (Polygonaceae), 2 Oct. 2002, H.D. Shin, CBS H-21011, CBS 132639 =CPC 10102.

Notes: This species is supported in the TEF phylogeny but cannot be distinguished from Cercospora sp. M and C. rodmanii in the ACT phylogeny. Isolate MUCC 442 clusters separately from the other two isolates based on the CAL and HIS phylogenies. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. fagopyri. Sequences obtained from Cercospora isolates on Ipomoea spp. cluster in three different clades. Although the name C. ipomoeae is available for this clade, without sequence data from North America (and an appropriate epitype) this name cannot be applied with certainty, above all since isolates from Ipomoea cluster in different clades.

Cercospora kikuchii (T. Matsumoto & Tomoy.) M.W. Gardner, Proc. Indian Acad. Sci. 36: 12. (1926) 1927.

Basionym: Cercosporina kikuchii T. Matsumoto & Tomoy., Ann. Phytopathol. Soc. Japan 1: 10. 1925.

Specimens examined: Argentinia, on Glycine max (Fabaceae), CBS 132633 =CPC 16578. Japan, Kagoshima, on Glycine soja (Fabaceae), 1952, H. Kurata, MUCC 590 = MAFF 305040; on G. soja, Jan. 1927, T. Matsumoto, CBS 128.27 = CPC 5068 (ex-type of C. kikuchii); on seed of G. soja, Jan. 1928, H.W. Wollenweber, CBS 135.28 = CPC 5067.

Notes: The symptoms on seeds and pods of plants inoculated with an isolate of C. richardiicola (MUCC 132; Nakashima, unpubl. data) originating from Osteospermum (Asteraceae) in Japan were quite similar to those caused by C. kikuchii. Cultures of C. kikuchii associated with purple seed stain symptoms cluster apart. This indicates that purple seed stain and leaf blight of G. max is caused by at least two different species of Cercospora, and that the identification of these species should not be based on disease symptoms alone. In the TEF and HIS phylogeny, the four isolates could not be distinguished from isolates of Cercospora sp. O, P and Q, as well as C. cf. richardiicola and C. cf. sigesbeckiae. Although these isolates clustered separate in the ACT phylogeny, intermixed in the clade was isolate CPC 14680 (C. cf. richardiicola) and isolate CPC 18636 (Cercospora sp. O). Similarly, the isolates clustered separate in the CAL phylogeny but intermixed with the isolates of C. fagopyri. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. cf. sigesbeckiae.

Cercospora lactucae-sativae Sawada, Rep. Gov. Agric. Res. Inst. Taiwan 35: 111. 1928.

    • ≡ Cercospora lactucae Welles, Phytopathology 13: 289. 1923, nom. illeg. (homonym), non Henn.

  • = Cercospora longispora Cugini ex Trav., Malpighia 17: 217, 1902, nom. illeg. (homonym).

    • ≡ Cercospora longissima Trav., Malpighia 17: correzione (correction slip) to p. 217, 1903, nom. illeg. (homonym).

    • ≡ Cercospora longissima Cugini ex Sacc., Syll. Fung. 18: 607. 1906, nom. illeg. (homonym).

  • = Cercospora lactucae J.A. Stev., J. Dept. Agric. Puerto Rico 1: 105. 1917, nom. illeg. (homonym).

  • = Cercospora ixeridis-chinensis Sawada, Rep. Gov. Agric. Res. Inst. Taiwan 86: 171. 1943, nom. inval.

  • = Cercospora lactucae-indicae Sawada, Rep. Gov. Agric. Res. Inst. Taiwan 86: 172. 1943, nom. inval.

Caespituli amphigenous. Mycelium internal. Stromata lacking or composed from few brown cells, up to 35 μm diam. Conidiophores arising from internal hyphae or a few intraepidermal brown cells, brown to pale brown, solitary to loosely fasciculate (2-7), straight or mildly geniculate, moderately thick-walled, irregular in width, wider and conically truncate at the apex, constricted at proliferating point, 25-150 × 3.5-6 μm, 0-5-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, uni-local or multi-local (1-2); loci distinctly thickened, 2.5-3.5 μm diam, slightly protuberant, apical. Conidia solitary, hyaline, filiform to acicular, or obclavate, obconically truncate and distinctly thickened at the base, subacute or obtuse, often swelling at the apex, 20-125 × 2-6 μm, 4-12-septate, thin-walled, smooth, rarely catenate.

Description of caespituli on V8 & MEA; MUCC 570 and 571 (= MAFF 238209 and 237719): Conidiophores solitary to loosely fasciculate, pale brown to brown, irregular in width, wider at the apex, constricted at proliferating point, smooth, moderately thick-walled, sinuous-geniculate to geniculate, simple, conically truncate at the apex, 22.5-195 × 3-5.5 μm, multi-septate. Conidiogenous cells integrated, terminal or intercalary, proliferating sympodially; loci moderately thickened, apical, 2.5-3.7 μm in width. Conidia hyaline, cylindrical to cylindrical obclavate, filiform, acicular, hilum distinctly thickened and long obconically truncate at the base, obtuse to acute at the apex, 44.5-215.5 × 3-7 μm, 5-20-septate.

Specimens examined: Japan, Chiba, on Lactuca sativa (Asteraceae), 12 Sep. 1997, S. Uematsu, MUCC 571 = MAFF 237719 = MUCNS 214; 18 Sep. 1998, C. Nakashima, MUMH 11401, MUCC 570 = MAFF 238209 = MUCN S463. South Korea, Chuncheon, on Ixeris chinensis subsp. strigosa (≡ Ixeris strigosa) (Asteraceae), 11 Oct. 2002, H.D. Shin, CBS H-21012, CPC 10082; 7 Oct. 2003, H.D. Shin, CBS H-21013, CBS 132604 =CPC 10728. Taiwan, Taipei, on L. sativa, 9 Mar. 1924 & 5 Apr. 1924, K. Sawada (TNS-F-220470).

Notes: This species is characterised in that conidiophores are wide and conically truncate at the apex, and constricted at the proliferating point. Furthermore, the conidia are not strictly acicular, but range from cylindrical-obclavate to acicular and they are rather broad, 3-7 μm. This species is phylogenetically well-supported based on ACT, CAL and HIS. The species cannot be distinguished from the single isolate of Cercospora sp. S in the TEF phylogeny, and these two species are also sister groups, but distinct, in the ACT phylogeny. The species is distinguished based on the CAL phylogeny, and split into two groups (MUCC 571 and 571 versus CPC 10082 and 10728) in the HIS phylogeny. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. cf. helianthicola.

Cercospora cf. malloti

Caespituli amphigenous. Mycelium internal. Stromata lacking to well-developed, intraepidermal and substomatal, up to 65 μm diam. Conidiophores arising from internal hyphae or few brown cells, solitary or in loose fascicles (2-11), pale brown to brown, paler towards the apex, thick-walled, simple, rarely branched, straight or mildly geniculate, abruptly geniculate at the middle, or successively geniculate at the upper portion, irregular in width, narrowed at the apex, somewhat constricted at the part of proliferation, obconically truncate at the apex, 30-115(-250) × 2.5-5.5 μm, multi-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially or percurrently, multi-local; loci apical or formed on the shoulders caused by geniculation, distinctly thickened, refractive, darkened, flattened, rarely protuberant at the shoulder of successive geniculation, 1-2 μm diam. Conidia solitary, hyaline, filiform to acicular, thickened and truncate at slightly protuberant base, obtuse or swelling at the apex, 40-90(-250) × 1.5-5 μm, 6-11(-20)-septate.

Description of caespituli on V8; MUCC 575 (= MAFF 237872): Conidiophores solitary, brown, paler at the apex, uniform in width, smooth, moderately thick-walled, simple, straight to mildly geniculate, short conically truncate at the tip, 100-465 × 1.25-3 μm, multi-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially; loci thickened, flattened, apical or formed on the shoulders caused by geniculation, 2-3 μm in width. Conidia hyaline, long cylindrical to filiform, slightly thickened and truncate at the base, obtuse at the apex, 30-430 × 2-4 μm, 3-19-septate, thin-walled, smooth.

Specimens examined: Japan, Okinawa, on Mallotus japonicus (Euphorbiaceae), 19 Nov. 2007, C. Nakashima & T. Akashi, MUMH 10837, MUCC 787; on Cucumis melo (Cucurbitaceae), 20 Jan. 1999, K. Uehara, MUCC 575 = MAFF 237872 = MUCNS 582 (as C. citrullina).

Notes: This species is supported by DNA sequence data of TEF, CAL and HIS. In the ACT phylogeny, the isolates from this species are intermixed with some isolates of C. cf. richardiicola (MUCC 128, 132 and 578) and Cercospora sp. P (isolate MUCC 771). In the combined tree (Fig. 2 part 4), it is a sister taxon to Cercospora sp. P. The isolates originated from different host plants, but have identical conidiophores, which are thick-walled and with distinct loci at the apex. However, other characters, which include the pattern of geniculation and size of caespituli, are very different. More detailed studies are required to describe the morphological characters of this species. Cercospora malloti was originally described from Mallotus (Euphorbiaceae) collected in the USA, and fresh material needs to be recollected. The present application of this name for Japanese collections is thus only tentative.

Cercospora mercurialis Pass., in Thüm., Mycoth. Univ., No. 783. 1877.

  • = Cercospora fruticola Sacc., Fungi Ital., Tab. 674. 1892.

  • = Cercospora mercurialis var. annuae Fautrey, in Roumeguere et al., Rev. Mycol. 15: 16. 1893.

  • = Cercospora mercurialis var. latvici Lepik, Tartu Ülik. Juures Oleva Loodusuur. Seltsi Arunded 39: 152. 1933.

  • = Cercospora mercurialis var. multisepta Săvul. & Sandu, Hedwigia 75: 225. 1936.

Specimens examined: Italy, Parma, on Mercurialis annua (Euphorbiaceae), 1874, Passerini, Thüm., Mycoth. Univ. 783, isotypes HBG, HAL. Romania, Distr. Prahova, Cheia, on Mercurialis perennis (Euphorbiaceae), 31 Jul. 1969, O. Constantinescu, epitype designated here CBS H-9850, culture ex-epitype CBS 550.71; on M. annua, 28 Jun. 1967, O. Constantinescu, CBS 549.71; Constanta, Hagieni, on Mercurialis ovata (Euphorbiaceae), 14 Jul. 1970, O. Constantinescu & G. Negrean, CBS H-9848, BUCM 2012, CBS 551.71.

Notes: Cercospora mercurialis is supported by TEF, ACT, CAL and HIS and can therefore be treated as an individual species. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. pileicola.

Cercospora cf. modiolae

Specimen examined: New Zealand, leaf spot on Modiola caroliniana (Malvaceae), 2002, C.F. Hill, Lynfield 535, CPC 5115.

Notes: This species is phylogenetically supported by TEF and ACT, but in the CAL and HIS phylogeny it cannot be distinguished from Cercospora sp. E. In the combined tree (Fig. 2 part 1), it is a sister taxon to Cercospora sp. E. Cercospora modiolae was described from North America and without sequences based on North American collections, this name can only tentatively be applied to the material from New Zealand.

Cercospora cf. nicotianae

Cultures examined: Indonesia, Medan, leaf spot on Nicotiana tabacum (Solanaceae), Jan. 1932, H. Diddens & A. Jaarsveld, CBS 131.32 = CPC 5076. Mexico, southern region of Tamaulipas, on Glycine max, 17 Oct. 2008, Ma. de Jesús Yáñez-Morales, CBS 132632 =CPC 15918. Nigeria, from a leaf spot on N. tabacum, Jul. 1969, S.O. Alasoadura, CBS 570.69 = CPC 5075.

Notes: See C. capsici. The name C. cf. nicotianae, described from the USA, can only tentatively be applied here. North American cultures and sequence data are needed for comparison and confirmation. Phylogenetically, C. cf. nicotianae is supported by CAL and partly HIS (CPC 5075 and 5076 were separated from CPC 15918). In the TEF phylogeny, the three isolates clustered in a distinct clade with a single isolate from C. cf. flagellaris (CPC 5441) but formed three distinct lineages in the ACT phylogeny. In the combined tree (Fig. 2 part 5), it is a sister taxon to C. cf. brunkii. Notes in the CBS database report that isolate CBS 131.32 was pathogenic when inoculated onto Nicotiana leaves. The isolation of C. cf. nicotianae from G. max requires some additional explanation. Leaf spots typical of Corynespora cassicola were observed, and once incubated in damp chambers, a Cercospora sp. was found sporulating on the healthy tissue, which was identified here as C. cf. nicotianae.

Cercospora olivascens Sacc., Michelia 1: 268. 1879.

Specimens examined: Italy, Selva, on Aristolochia clematidis (Aristolochiaceae), Aug. 1877, isotype distributed as Mycoth Veneta 1251, HAL. Romania, Cazanele Dunarii, on A. clematidis, 19 Oct. 1966, O. Constantinescu, epitype designated here CBS H-21014, culture ex-type CBS 253.67= IMI 124975 = CPC 5085.

Notes: This species is supported by TEF, ACT, CAL and HIS. In the combined tree (Fig. 2 part 1), it is a sister taxon to Cercospora sp. F.

Cercospora cf. physalidis

Specimen examined: Peru, on Solanum tuberosum (Solanaceae), L.J. Turkensteen, CBS 765.79.

Notes: This species is supported by CAL and HIS. It cannot be distinguished from Cercospora sp. I and C. alchemillicola / C. cf. alchemillicola based on the TEF and ACT phylogenies. In the combined tree (Fig. 2 part 1), it is a sister taxon to Cercospora sp. G. According to Braun & Melnik (1997), C. physalidis and numerous Cercospora spp. of C. apii s. lat. on various hosts of the Solanaceae are morphologically indistinguishable from the latter species. Fresh material on Solanum from North America is required to resolve this issue.

Cercospora pileicola C. Nakash., Crous, U. Braun & H.D. Shin, sp. nov. MycoBank MB800656. Fig. 9.

Fig. 9.

Fig. 9.

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Cercospora pileicola (CBS 132607 =CPC 10749). A. Leaf spots. B-E. Weakly developed, fasciculate conidiophores. F-I. Conidia. Scale bars = 10 μm.

Etymology: Named after the host genus from which it was collected, Pilea.

Leaf spots circular, 1-2 mm diam, center greyish to pallid, surrounded by purplish brown border lines. Caespituli hypogenous. Mycelium internal. Stromata lacking to small, to 30 μm diam, brown, substomatal. Conidiophores straight to curved, pale brown to dark brown, paler towards the apex, solitary or in loose fascicles (2-5), sometimes mildly geniculate, simple, thick-walled, uniform in width, rarely narrowed after the geniculation, conically truncate at the apex, 30-110 × 3-8.5 μm, often swelling at the base, to 9 μm, 1-3-septate. Conidiogenous cells integrated, terminal, proliferating sympodially; loci distinct, slightly protuberant, apical and formed on shoulder caused by geniculation, lateral, multi-local (1-2), 2.5-4 μm diam. Conidia hyaline, cylindrical, acicular to obclavate, straight or curved, truncate or long obconically truncate, and slightly thickened at the base, acute to obtuse at the apex, 28-175 × 4-7 μm, 0-12-septate.

Culture characteristics: Colonies erumpent, spreading, with moderate, fluffy aerial mycelium and lobate, even margins, reaching 25 mm diam after 1 wk at 25 °C in the dark. On MEA surface dirty white, reverse cream; red pigment absent. On PDA surface dirty white, reverse scarlet, with diffuse red pigment in agar. On OA surface scarlet in middle (due to collapsed aerial mycelium), white in outer region (due to aerial mycelium), with diffuse red pigment surrounding colony.

Specimens examined: South Korea, Dongducheon, on Pilea pumila (= P. mongolica) (Urticaceae), 28 Sep. 2003, H.D. Shin, holotype CBS H-21015, culture ex-type CBS 132607 =CPC 10749; Hoengseong, on Pilea hamaoi (≡ P. pumila var. hamaoi) (Urticaceae), 10 Oct. 2003, H.D. Shin, CBS H-21016, CBS 132647 =CPC 10693; Hongcheon, on Pilea pumila (= P. mongolica), 29 Jul. 2004, H.D. Shin, CPC 11369.

Notes: Cercospora pileicola is characterised by having conidiophores that are thick-walled, almost uniform in width, conically truncate at the apex, and often swelling at the base; sporulation is restricted at the terminal part of conidiophores, and conidia are cylindrical, acicular to obclavate with long obconically truncate basal ends and rather broad, 4-7 μm. Moreover, this species is phylogenetically supported by the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. mercurialis. Cercospora ganjetica (Purkayastha & Mallik 1978), described from India on Urtica urens (Urticaceae), seems to be morphologically similar to C. pileicola, above all due to relatively broad conidia, but the conidia are strictly cylindrical to obclavate with obconically truncate base, i.e. acicular conidia with truncate base are not formed. Length and width of conidiophores agree with those of C. pileicola, but they are pluriseptate (3-6). The affinity of C. ganjetica is quite unclear. Cercospora pileae (Chupp 1954) was described from China on “Pilea sp.” with conidia being olivaceous. This species is not included in the Chinese monograph of Cercospora species (Guo & Liu 2005), but Liu & Guo (1998) reduced this name to synonym with Pseudocercospora profusa, suggesting that the type host was misidentified, which was confirmed by Y.L. Guo (Beijing, in litt.). The type of C. pileae is not Pilea sp. but Acalypha australis (Euphorbiaceae). Chinese collections of Cercospora on various hosts of the Urticaceae, including Pilea spp., have been assigned to Cercospora krugeriana (= nom. inval.), which is a quite distinct C. apii-like species with narrower (2.5-5 μm), pluriseptate, acicular conidia, up to 214 μm long (Hsieh & Goh 1990, Guo & Liu 2005). In addition, the conidiophores are distinctly plurigeniculate. It is possible that the latter collections belong to the C. cf. sigesbeckiae clade as circumscribed in this study.

Cercospora polygonacea Ellis & Everh., J. Mycol. 1: 24. 1885.

  • = Cercospora avicularis var. sagittati G.F. Atk., J. Elisha Mitchell Sci. Soc. 8: 48. 1892.

  • = Cercospora polygoni-caespitosi Sawada, Formosan Agric. Rev. 38: 700. 1942, nom. inval.

  • = Cercospora polygoni-blumei Sawada, nom. nud.

Caespituli amphigenous. Mycelium internal. Stromata lacking to small, up to 30 μm diam, pale olivaceous-brown, intraepiderimal, substomatal. Conidiophores successively geniculate at the upper portion, pale brown, paler towards the apex, solitary or in loose fascicles (2-5), simple, thick-walled, irregular in width, narrowed after the geniculation, conically truncated at the apex, 21-100 × 5-7 μm, 0-3-septate. Conidiogenous cells integrated, terminal, intercalary, proliferating sympodially, multi-local (1-6); loci distinct, protuberant, apical and formed on shoulder caused by geniculation, lateral, 2.5-3 μm diam. Conidia solitary, hyaline, acicular to obclavate, straight or slightly curved, truncate or obconically truncate, and thickened at the base, obtuse or acute at the apex, 60-110 × 3.5-5.5 μm, 4-9-septate, thin-walled, smooth.

Specimen examined: South Korea, Cheongju, on Persicaria longiseta (≡ P. blumei) (Polygonaceae), 4 Jun. 2004, H.D. Shin, CBS H-21017, CBS 132614 =CPC 11318.

Notes: Morphologically the Korean specimen is similar to C. polygonaeae, which Chupp (1954) also reported from Asia (Japan). Material from the USA on Polygonum (Polygonaceae) is required to resolve whether this taxon is the same or phylogenetically distinct. The species is phylogenetically distinct from the other species included in this study based on the TEF and ACT phylogenies, but indistinguishable from C. achyranthis on the HIS phylogeny and from C. achyranthis, C. sojina and C. campi-silii based on the CAL phylogeny. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. achyranthis.

Cercospora punctiformis Sacc. & Roum., Rev. Mycol. 3: 29. 1881.

  • = Fusicladium cynanchi Reichert, Bot. Jahrb. Syst. 56: 720. 1921.

  • = Cercospora punctiformis f. catalaunica Gonz. Frag., Mem. Real Acad. Ci. Exact. Madrid, Ser. 2, 6: 250-252. 1927.

  • = Cercospora cynanchi Lobik, Mat. Fl. Faun. Obsl. Tersk. Okr., Pjatigorsk: 53. 1928.

Leaf spots scattered to confluent, at first appearing as purplish spots, later greyish brown with purplish border lines, mostly vein-limited, but rather circular to irregular in case of humid and hot weather (esp. in rainy summer), mostly less than 7 mm diam. Caespituli amphigenous, but abundantly hypophyllous. Mycelium internal. Stromata well-developed, up to 35 μm diam, substomatal and intraepidermal, brown to dark brown. Conidiophores in fascicles (5-30), loose to moderately divergent, olivaceous-brown, fairly uniform in colour, but paler towards the apex in longer ones, simple, conically truncate at the apex, geniculate (0-4), 20-60(-150) × 4-7.5 μm, 0-3-septate. Conidiogenous cells integrated, proliferating sympodially, terminal and intercalary; loci distinctly thickened, protuberant, apical or formed on the shoulders caused by geniculation, 3-4 μm diam. Conidia solitary, hyaline, variable in shape and length, obclavato-cylindrical or elliptical, obconically truncate and thickened at the base, obtuse to subacute at the apex, 25-100(-175) × 4-6.5 μm, 0-8(-12)-septate, thin-walled, smooth.

Specimen examined: South Korea, Bonghwa, on Cynanchum wilfordii (Asclepiadaceae), 18 Oct. 2007, H.D. Shin, CBS H-21018, CBS 132626 =CPC 14606.

Notes: The Korean sample on Cy. wilfordi is morphologically close to Cercospora punctiformis, but the latter species was described from North Africa. Hence, sequence data based on North African material are needed to confirm the conspecificity of Korean collections. The ACT and HIS phylogenies separate C. punctiformis from the other species included in this study; in the TEF and CAL phylogenies the isolate occurs on a longer branch in a clade consisting of C. sojina and C. achyranthis. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. euphorbiae-sieboldianae.

Cercospora cf. resedae

Specimens examined: New Zealand, Auckland, C.F. Hill, on Reseda odorata (Resedaceae), specimen in HAL, CBS 118793 (as C. resedae). Romania, Bucuresti, on Helianthemum sp. (Cistaceae), 15 Sep. 1966, O. Constantinescu, CBS 257.67 = CPC 5057 (as C. cistinearum).

Notes: Both the names C. resedae and C. cistinearum are available for this clade. We give preference to C. resedae, which is the older name. However, the application of this name is very uncertain and only tentative. Fresh European collections from Reseda (Resedaceae) are needed to designate an epitype and fix the application of the name. The TEF and ACT phylogenies could not distinguish these two isolates from C. apii and C. beticola, and the CAL phylogeny could not distinguish it from C. apii. The HIS phylogeny places the two isolates in the deviating C. beticola Clade 1. A combination of these phylogenetic positions explains the basal position of the species to the C. apii and C. beticola clades in the combined phylogeny (Fig. 2 part 5).

Cercospora cf. richardiicola

Caespituli amphigenous. Mycelium internal. Stromata intraepidermal or substomatal, lacking to well-developed, up to 55 μm diam, pale brown to brown. Conidiophores solitary or in loose fascicles (2-15), simple, rarely branched, pale brown to reddish brown, paler towards the apex, moderately thick-walled, irregular in width, sometimes swelling at the shoulders caused by geniculation, truncate or short obconically truncate at the apex, straight to mildly geniculate, often narrowed with successive geniculation at the apex, sometimes swelling at the base to twice the width, 30-260(-360) × 2-7 μm, multi-septate (2-11). Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially, or rarely percurrently; loci apical or formed on shoulders caused by geniculation, lateral, circumspersed, distinctly thickened and darkened, often slightly protuberant, 1.5-3.5 μm diam. Conidia solitary, rarely catenate, filiform, cylindrical to acicular, hyaline, thickened and truncate or rarely short obconically truncate at the base, rounded or acute at the apex, straight or slightly curved, 25-300 × 2.5-5 μm, 2-20-septate, thin-walled, smooth.

Description of caespituli on V8; (MUCC 128, 132, 138, 582): Caespituli dimorphic in culture; one type is small and commonly observed, while the other is large and rarely observed (C. apii s. lat. type; described in parenthesis). Conidiophores solitary to loosely fasciculate, arising from hyphae, subhyaline to pale brown, irregular in width, smooth, meager and thin-walled, sinuous-geniculate to geniculate (straight to geniculate), sometimes branched (unbranched), truncate or conically truncate at the tip (truncate at the tip), 6.5-60(-520) × 2.5-5 μm, multi-septate. Conidiogenous cells integrated, terminal or intercalary, proliferating sympodially, 1-5 multi-local (uni-local); loci moderately thickened, apical and lateral, circumspersed at the apex of conidiogenous cells, protuberant (not protuberant), 1.25-2(-4.5) μm in width. Conidia hyaline, filiform to acicular, slightly thickened and obconical truncate (truncate) at the base, acute at the apex, 27.5-277.5 × 2-3.5(-6.5) μm, 3-21-septate.

Specimens examined: Japan, Chiba, on Zantedeschia sp. (Araceae), S. Uematsu & C. Nakashima, MUMH 11403, MUCC 578 = MAFF 238210; Ehime, on Tagetes erecta (Asteraceae), 27 Oct. 2004, J. Nishikawa, MUMH 11392, MUCC 128; Shizuoka, on Fuchsia ×hybrida (Onagraceae), 22 Jun. 2006, J. Nishikawa, MUMH 11396, MUCC 138; on Osteospermum sp. (Asteraceae), 11 Sep. 2004, J. Nishikawa, MUMH 11395, MUCC 132; Tokyo, on Gerbera hybrida (Asteraceae), J. Takeuchi, MUCC 582 = MAFF 238880.

Notes: The name Cercospora cf. richardiicola can be applied to this clade only tentatively. The latter species was described from the USA. Hence, sequences obtained from North American collections are necessary to confirm the identity with true C. richardiicola. All clades within this complex (C. cf. richardiicola, C. kikuchii, C. cf. sigesbeckiae) are poorly resolved on TEF, ACT, CAL, and HIS regions. The TEF and HIS phylogenies could not distinguish it from Cercospora spp. M-Q, C. kikuchii and C. cf. sigesbeckiae. The ACT phylogeny split it into three clades, namely isolates MUCC 128, 132 and 578 intermixed with C. malloti and Cercospora sp. P, isolates MUCC 138 and 582 sister to Cercospora sp. N and isolate CPC 14680 intermixed with C. kikuchii and Cercospora sp. O. The CAL phylogeny could not distinguish the isolates from C. rodmanii, C. cf. sigesbeckiae and Cercospora sp. N. Currently this complex is split into three sister clades (Fig. 2 part 4), which could be due to a common ancestor, and an ongoing process of speciation.

Cercospora richardiicola is characterised in that conidiophores are sometimes swelling at the shoulders caused by geniculation, truncate or short obconically truncate at the apex, often narrowed (not attenuated) successive geniculation at the apex, and sometimes swelling at the base up to twice its median width; and loci on conidiogenous cells are circumspersed and distinctly thickened. These characteristics were sometimes difficult to find on the host plant due to the difference of maturity of the fungus. However, the morphological characteristics of this species on V8 medium were well preserved regardless of differences of host and maturity.

Isolates of C. richardiicola have a tendency to infect a wide host range. Isolates are frequently found together with other Cercospora spp. on the same leaf spots, which make identification problematic.

Cercospora ricinella Sacc. & Berl., Atti Reale Ist. Ven. Sci. Lett. Art, Ser. 3: 721. 1885.

    • ≡ Cercosporina ricinella (Sacc. & Berl.) Speg., Anales Mus. Nac. Hist. Nat. Buenos Aires 20: 429. 1910.

  • = Cercospora albido-maculans G. Winter, Hedwigia 24: 202, 1885 (also in J. Mycol. 1: 124. 1885).

  • = Cercospora ricini Speg. Anales Mus. Nac. Hist. Nat. Buenos Aires Ser. 2. 3: 343. 1899.

Leaf spots circular to angular, 1-10 mm diam, first appearing as brown spots, later centre becoming greyish white with reddish brown border lines. Caespituli amphigenous, mainly hypophyllous. Mycelium internal. Stromata lacking to well-developed, pale brown to brown, substomatal or intraepidermal, 14-50 μm. Conidiophores pale brown, paler towards apex, sinuous-geniculate to geniculate above the middle, in loose fascicles (2-14), slightly divergent, irregular in width, slightly attenuated at the apex, conical at the tip, sometimes constricted at proliferating point, 35-140 × 4.5-5.5 μm, 2-4-septate. Conidiogenous cells integrated, terminal and intercalary, proliferating sympodially; multi-local at the apex, loci distinct, slightly protuberant, mainly apical, lateral, 2-3 μm diam. Conidia solitary, rarely catenate, hyaline, cylindrical to cylindro-obclavate, acicular, obconically truncate or truncate and distinctly thickened at the base, acute to subacute at the apex, 20-130 × 2.5-5.5 μm, 1-8-septate, thin-walled, smooth.

Specimens examined: South Korea, Chuncheon, on Ricinus communis (Euphorbiaceae), 11 Oct. 2002, H.D. Shin, CPC 10104; 7 Oct. 2003, H.D. Shin, CBS 132605 =CPC 10734; CPC 10735-10736.

Notes: This species is characterised in that the conidiophores are slightly attenuated at the apex, sinuous-geniculate to geniculate above the middle, and the conidia are rarely catenate. It is supported by ACT, CAL and HIS. In the TEF phylogeny it could not be distinguished from C. delaireae, C. cf. chenopodii and Cercospora sp. K. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. delaireae. Epitype material should be collected in Australia, where this species was described from.

Cercospora rodmanii Conway, Canad. J. Bot. 54: 1082. 1976.

Specimens examined: Brazil, Oroco, on Eichhornia crassipes (Pontederiaceae), R. Charudattan, CBS 113126 =RC3409; Rio Verde, on E. crassipes, R. Charudattan, CBS 113123 =RC3660. Mexico, Carretero, on E. crassipes, R. Charudattan, CBS 113124 =RC2867. USA, Florida, on E. crassipes, R. Charudattan, CBS 113128 =RC394; CBS 113130 =RC393; K. Conway, CBS 113129 =RC397. Venezuela, Maracay, on E. crassipes, R. Charudattan, CBS 113131 =RC395. Zambia, on E. crassipes, M. Morris, CBS 113125 =RC4101.

Notes: Cercospora rodmanii is supported in the TEF phylogeny. In the ACT phylogeny, the clade includes on longer branches also C. cf. ipomoeae and Cercospora sp. M. and in the CAL phylogeny it was intermixed with isolates of C. cf. richardiicola, C. cf. sigesbeckiae and Cercospora sp. N. In the HIS phylogeny, it could not be distinguished from Cercospora spp. N-Q. In the combined tree (Fig. 2 part 4), it is a sister taxon to Cercospora sp. N. Tessmann et al. (2001) considered C. rodmanii to be a synonym of C. piaropi whereas Crous & Braun (2003) retained C. rodmanii as a separate species. From the results of the present study, we prefer to retain these as two separate species as reported previously (Groenewald et al. 2010a, Montenegro-Calderón et al. 2011). The isolate originally included as C. piaropi in this study (CBS 113127) is treated in the present study under C. cf. flagellaris; this isolate is also the same isolate used by Tessmann et al. (2001). Montenegro-Calderón et al. (2011) confirmed the identity of their isolates with the same genes included here, as well as beta-tubulin, and demonstrated that their isolates of C. rodmanii were able to also infect other important crops such as beet and sugar beet whereas C. piaropi (treated under C. cf. flagellaris in this study) isolate CBS 113127 and C. rodmanii isolate CBS 113129 were specific to water hyacinth.

Cercospora rumicis Pavgi & U.P. Singh, Mycopathol. Mycol. Appl. 23: 191. 1964.

  • = Cercospora rumicis Ellis & Langl. ex Chupp, A monograph of the fungus genus Cercospora: 453. 1954, nom. inval.

Specimen examined: New Zealand, Manurewa, on Rumex sanguineus (Polygonaceae), C.F. Hill, Lynfield 671, CPC 5439.

Notes: Cercospora rumicis was treated as part of the larger C. apii s. lat. complex by Crous & Braun (2003). Although it clusters basal to the C. zebrina clade, we suspect that it may represent a distinct taxon. Fresh collections are required from India to fix the application of this name. In the TEF phylogeny, it is not distinguished from C. zebrina and C. armoraciae, and likewise not from C. armoraciae on the ACT phylogeny. In the CAL phylogeny, it is not distinguished from C. zebrina and C. althaeina. It is distinct from all species included in this study based on the HIS phylogeny. In the combined tree (Fig. 2 part 3), it is basal to the lineage containing Cercospora sp. L, C. althaeina, C. zebrina and C. violae.

Cercospora senecionis-walkeri Phengsintham, Chukeatirote, McKenzie, K.D. Hyde & U. Braun, Pl. Pathol. & Quarantine 2(1): 70. 2012.

Specimen examined: Laos, on Senecio walkeri (Asteraceae), 20 Feb. 2010, P. Phengsintham, LC 0396, NUOL P567, CBS 132636 =CPC 19196.

Notes: Several Cercospora species have been described from Senecio (Asteraceae), but all of them are quite distinct from the species on S. walkeri. Cercospora senecionis was reduced to synonym with C. jacquiniana by Chupp (1954). Based on a re-examination of type material, Braun (in Braun & Mel’nik 1997) showed that C. senecionis represents a quite distinct true species of Cercospora with acicular conidia, similar to those of C. apii s. lat., but 80-200 × 3-6 μm in size. Cercospora jaquiniana is similar to C. senecionis-walkeri (Pheng et al. 2012) with regard to its conidial shape, but has much shorter conidiophores and shorter conidia, usually only 1-3-sepate, which are hyaline, subhyaline to faintly pigmented. Thus, this species was reallocated to Passalora by Braun (in Braun & Mel’nik 1997). The Indian taxon C. senecionis-grahamii is close to C. senecionis, but differs in having acicular to obclavate conidia, only 3-4 μm wide. The North American C. senecionicola is also quite distinct from C. senecionis-walkeri by its very narrow acicular-subcylindrical conidia, only 2-3.5 μm wide (Chupp 1954). The South American Passalora senecionicola (Braun et al. 2006) on Senecio bonariensis (Asteraceae) in Argentina is morphologically very close to C. senecionis-walkeri but characterised by having quite distinct lesions, larger stromata, up to 60 μm diam and short conidia that are cylindrical. Passalora senecionicola was assigned to Passalora due to subhyaline to pale olivaceous conidia, but it is possible that this species rather belongs in Cercospora which may be suggested by the phylogenetic position of C. senecionis-walkeri, which clusters within the Cercospora clade, although the conidia range from being almost hyaline to somewhat pigmented. Cercospora senecionis-walkeri is distinct from all other species included in this study based on the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 1), it is basal to the other Cercospora spp.

Cercospora cf. sigesbeckiae

Morphologically similar to taxa in the C. apii s. lat. complex.

Specimens examined: Japan, Chiba, on Begonia sp. (Begoniaceae), 24 Jun. 1997, S. Uematsu, MUMH 11405, MUCC 587 = MAFF 237690 = MUCNS 197; Fukuoka, on Sigesbeckia glabescens (Asteraceae), 31 Oct. 1948, S. Katsuki, holotype in TNS; Saitama, on Glycine max, 1949, H. Kurata, MUCC 589 = MAFF 305039 (as C. kikuchii); Tokyo, on Dioscorea tokoro (Dioscoreaceae), 10 Nov. 2007, I. Araki, MUMH 10951, MUCC 849. South Korea, Chuncheon, on S. glabrescens, 7 Oct. 2003, H.D. Shin, CBS H-21019, CBS 132601 =CPC 10664 (as C. sigesbeckiae); on Persicaria orientalis (= P. cochinchinensis) (Polygonaceae), 11 Oct. 2002, H.D. Shin, CBS 132641 =CPC 10117 (as C. polygonacea); Hongcheon, on Pilea pumila (= P. mongolica), 3 Oct. 2002, H.D. Shin, CBS 132642 =CPC 10128 (as C. ganjetica); Namyangju, on Paulownia coreana (Scrophulariaceae), 22 Oct. 2003, H.D. Shin, CBS H-21020 = HAL 1863, CBS 132606 =CPC 10740; Yanggu, on Sigesbeckia pubescens, 28 Sep. 2007, H.D. Shin, CBS 132621 =CPC 14489 (as C. sigesbeckiae); on Malva verticillata (Malvaceae), H.D. Shin, CBS H-21021, CBS 132675 =CPC 14726 (as C. malvacearum).

Notes: See Cercospora cf. richardiicola. The application of the name C. cf. sigesbeckiae (based on type material from Japan), to this clade can only be tentative. Japanese cultures and sequences are needed to confirm its identity. In the TEF and CAL phylogenies, isolates are intermixed with those of Cercospora spp. M-Q, C. kikuchii and C. cf. richardiicola; in the ACT phylogeny it cannot be distinguished from C. fagopyri. In the HIS phylogeny the isolates form a clade on a longer branch in a clade containing C. kikuchii and some isolates of C. cf. richardiicola. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. kikuchii and C. cf. richardiicola.

Cercospora sojina Hara, Nogyokoku (Tokyo) 9: 28. 1915.

    • ≡ Cercosporina sojina (Hara) Hara, Jitsuyo-sakumotsu-byorigaku: 112. 1925.

    • ≡ Cercosporidium sojinum (Hara) X.J. Liu & Y.L. Guo, Acta Mycol. Sinica 1: 100. 1982.

    • ≡ Passalora sojina (Hara) Poonam Srivast., J. Living World 1: 118. 1994, comb. inval.

    • ≡ Passalora sojina (Hara) H.D. Shin & U. Braun, Mycotaxon 58: 63. 1996.

    • ≡ Passalora sojina (Hara) U. Braun, Trudy Bot. Inst. im. V.L. Komarova 20: 93. 1997, comb. superfl.

  • = Cercospora daizu Miura, Manchurian R.R. Agric. Exp. Stat. Bull. 11: 25. 1920.

Caespituli amphigenous. Mycelium internal. Stromata small, up to 35 μm diam, intraepidermal and substomatal, brown. Conidiophores solitary or in loose fascicles (2-5), brown, paler towards the apex, simple, rarely branched, irregular in width, constricted at the parts of proliferation, conically truncate at the apex, straight to geniculate, 55-200 × 4.5-5 μm, 2-4-septate. Conidiogenous cells integrated, proliferating sympodially, terminal and intercalary, uni- or multi-local (1-2); loci distinctly thickened, protuberant, apical or formed on the shoulders caused by geniculation, 2-4 μm diam. Conidia solitary, hyaline, cylindrical to obclavate, fusiform, obovoid, obconically truncate and thickened at the base, obtuse at the apex, 25-70 × 5.5-9 μm, 1-5-septate, thin-walled, smooth.

Specimens examined: Argentina, on Glycine max (Fabaceae), 2009, F. Scandiani, CPC 17964 = CBS 132684 =CPC 17971 = “CCC 173-09, 09-495”; “CCC 155-09, 09-285-5”; CPC 17965 = “CCC 156-09, 09-285-4”; CPC 17966 = “CCC 157-09, 09-285-3”; CPC 17967 = “CCC 158-09, 09-285-1”; CPC 17968 = “CCC 159-09, 09-285-7”; CPC 17969 = “CCC 167-09, 09-881”; CPC 17970 = “CCC 172-09, 09-320”; CPC 17972 = CCC 174-09; CPC 17973 = “CCC 176-09, 09-882”; CPC 17974 = “CCC 177-09, 09-2488-1”; CPC 17975 = “CCC 178-09, 09-1438-2”; CPC 17976 = “CCC 179-09, 09-2591”; CPC 17977 = “CCC 180-09, 09-2520”. South Korea, Hoengseong, on G. soja, 4 Sep. 2005, H.D. Shin, CBS 132018 =CPC 12322; Hongcheon, on G. soja, 20 Jul. 2004, H.D. Shin, neotype designated here CBS H-21022, culture ex-type CBS 132615 =CPC 11353; CPC 11354; CPC 11420-11423.

Notes: Type material of this species (Japan, Tokyo, on G. max, 1909, K. Hara) was not located and is probably lost. Cercospora sojina was transferred to the genus Passalora based on its distinctly thickened loci, and cylindrical and relatively wide conidia (Shin & Braun 1996). However, the hyaline conidia of this species are indicative of the fact that it is best retained in Cercospora (Crous & Braun 2003), which is fully supported by its position in phylogenetic trees among other Cercospora species. The species is supported as distinct based on the ACT and HIS phylogenies; in the TEF and CAL phylogenies the isolates of C. achyranthis and C. campi-silii are intermixed with the C. sojina isolates. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. campi-silii.

Cercospora sp. A

Culture sequenced: Mexico, on Chenopodium sp. (Amaranthaceae), M. de Jesus Yanez, CBS 132631 =CPC 15872.

Notes: This isolate is phylogenetically distinct (Fig. 2 part 1) from the other species included in this study. Unfortunately, the specimen and specimen details were not available for study.

Cercospora sp. B

Caespituli amphigenous. Mycelium internal. Stromata lacking to developed, up to 60 μm, intraepidemal, substomatal, brown. Conidiophores straight or geniculate, solitary to 2-21 in dense fascicle, 0-5-septate, 20-75 × 4.5-6 μm, almost uniform in width, constricted at shoulder, conically truncate or truncate at the tip. Conidiogenous cells integrated, terminal, intercalary, proliferating sympodially, multilocal; loci thickened, apical, rarely lateral, 2-2.5 μm diam, slightly protuberant. Conidia solitary, hyaline, cylindro-obclavate to acicular, obconically truncate at thickened base, tip obtuse, 45-135 × 4-5 μm, 4-9-septate, thin-walled, smooth.

Specimen examined: South Korea, Kangnung, on Ipomoea purpurea (Convolvulaceae), 10 Sep. 2003, H.D. Shin, CBS 132602 =CPC 10687 (as C. ipomoeae); CPC 10688-10689 (as C. ipomoeae).

Notes: This isolate was obtained from Ipomoea in Korea, but differs in its phylogeny to other isolates of C. cf. ipomoeae. It has a unique position in the ACT, CAL and HIS phylogenies and is intermixed with C. delaireae and Cercospora sp. K based on the TEF phylogeny. In the combined tree (Fig. 2 part 1), it is a basal taxon to C. agavicola. Several species of Cercospora have thus far been described from Ipomoea, and more collections would be required to resolve the status of this collection.

Cercospora sp. C

Culture sequenced: Mexico, M. de Jesus Yanez, CBS 132629 =CPC 15841.

Notes: This isolate is phylogenetically distinct (Fig. 2 part 1) from the other species included in this study. Unfortunately, the specimen and specimen details were not available for study.

Cercospora sp. D

Culture sequenced: Mexico, M. de Jesus Yanez, CBS 132630 =CPC 15856.

Notes: This isolate is phylogenetically distinct (Fig. 2 part 1) from the other species included in this study. Unfortunately, the specimen and specimen details were not available for study.

Cercospora sp. E

Cultures sequenced: Mexico, M. de Jesus Yanez, CBS 132628 =CPC 15632, CPC 15801.

Notes: These isolates are phylogenetically distinct (Fig. 2 part 1) from the other species included in this study. Unfortunately, the specimen(s) and specimen details were not available for study.

Cercospora sp. F

Specimen examined: South Africa, on Zea mays (Poaceae), P. Caldwell, CBS 132618 =CPC 12062.

Notes: This isolate, which is supported by the CAL phylogeny, must be treated as an independent species. In the TEF and HIS phylogenies it is present on a longer branch in a clade consisting of isolates of Cercospora spp. G-I, C. alchemillicola / C. cf. alchemillicola, C. cf. physalidis and C. celosiae. In the ACT phylogeny it cannot be distinguished from Cercospora sp. Q. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. cf. physalidis.

Cercospora sp. G

Caespituli amphigenous. Mycelium internal. Stromata small to well-developed, up to 60 μm diam, brown, intraepidermal and substomatal. Conidiophores straight or sinuously geniculate, loosely fasciculate (3-10), pale brown to brown, paler towards the apex, moderately thick-walled, simple, irregular in width, attenuated at the apex, irregularly constricted following the proliferation, 30-50 × 3.5-4.5 μm, 0-2-septate. Conidiogenous cells integrated, terminal, rarely intercalary, proliferating sympodially, multi-local; loci thickened, darkened, apical or formed on the shoulders caused by geniculation, lateral, sometimes circumspersed, 1.25-2 μm in diam. Conidia solitary, hyaline, cylindrical to obclavate, often acicular, straight or slightly curved, truncate or subtruncate at the thickened base, obtuse or subacute at the apex, 15-165 × 2-4 μm, 1-12-septate, thin-walled, smooth.

Specimen examined: New Zealand, Manurewa, on Salvia viscosa (Lamiaceae), C.F. Hill, Lynfield 626, CPC 5438 (as C. salviicola); Kopuku, on Bidens frondosa (Asteraceae), C.F. Hill, Lynfield 559, CBS 115518 =CPC 5360.

Notes: This species is thus far only known from New Zealand. It is distinct from the other included species based on its position in the HIS phylogeny; in the TEF and ACT phylogenies it cannot be distinguished from Cercospora spp. F, H and I as well as C. alchemillicola / C. cf. alchemillicola, C. cf. physalidis and C. celosiae. In the CAL phylogeny it forms a distinct clade that cannot be distinguished from Cercospora sp. H. In the combined tree (Fig. 2 part 1), it is a sister taxon to Cercospora sp. H.

Cercospora sp. H

Specimens examined: Argentina, on Chamelaucium uncinatum (Myrtaceae), S. Wolcan, CPC 11620 = 1CRI. New Zealand, on Dichondra repens (Convolvulaceae), C.F. Hill, Lynfield 536, CBS 115205 =CPC 5116.

Notes: This species is distinct from the other included species based on its position in the HIS phylogeny; in the TEF and ACT phylogenies it cannot be distinguished from Cercospora spp. F, G and I as well as C. alchemillicola / C. cf. alchemillicola, C. cf. physalidis and C. celosiae. In the CAL phylogeny it forms a distinct clade that cannot be distinguished from Cercospora sp. G. Whether Cercospora spp. G and H could be conspecific awaits collection of more isolates. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. celosiae and Cercospora sp. I.

Cercospora sp. I

  • ?Cercospora deutziae Ellis & Everh., J. Mycol. 4: 5. 1888.

  • ?Cercospora guatemalensis A.S. Mull. & Chupp, Ceiba 1: 173. 1950.

Specimens examined: South Korea, Suwon, on Ajuga multiflora (Lamiaceae), 22 Oct. 2002, H.D. Shin, CBS 132643 =CPC 10138 (as C. guatemalensis). New Zealand, Manurewa, on Coreopsis verticillata (Asteraceae), 2 Jun. 2003, C.F. Hill, Lynfield 866A, CBS 132597 =CPC 10615; Lynfield 866B, CPC 10616; on Deutzia crenata (Hydrangeaceae), 5 May 2002, C.F. Hill, Lynfield 610, CBS 114818 =CPC 5362 (named as C. deutziae); on Deutzia purpurascens (Hydrangeaceae), 5 May 2002, C.F. Hill, Lynfield 607, CBS 114815 =CPC 5364 (named as C. deutziae); on Deutzia ×rosea (= D. gracilis × purpurascens) (Hydrangeaceae), Apr. 2002, C.F. Hill, Lynfield 599, CBS 114816 =CPC 5363 (named as C. deutziae); on Fuchsia procumbens (Onagraceae), 5 May 2002, C.F. Hill, Lynfield 613, CBS 114817 =CPC 5365 (named as C. fuchsia); on Nicotiana sp. (Solanaceae), 8 Jun. 2002, C.F. Hill, Lynfield 667, CPC 5440; Mt Albert, on Gunnera tinctoria (Gunneraceae), 29 Feb. 2004, C.F. Hill, Lynfield 997, CBS 115121; Whangarei, on Archontophoenix cunninghamiana (Arecaceae), 10 Feb. 2004, C.F. Hill, CBS 115117.

Notes: This clade is quite distinct based on the combined tree (Fig. 2 part 1), and mainly consists of isolates from various host plants in New Zealand. In the TEF and ACT phylogenies it cannot be distinguished from Cercospora spp. F, G and H as well as C. alchemillicola / C. cf. alchemillicola, C. cf. physalidis and C. celosiae. In the CAL phylogeny it forms a distinct clade that cannot be distinguished from the single isolate of C. celosiae. In the HIS phylogeny it cannot be distinguished from Cercospora sp. F, C. alchemillicola / C. cf. alchemillicola and C. celosiae. In the combined tree (Fig. 2 part 1), it is a sister taxon to C. celosiae and Cercospora sp. H. Most of the Cercospora sp. I isolates from New Zealand would be given a species epithet based on each host plant, if these were classified with a conventional species concept. From the results of the phylogenetic tree, these isolates are recognised as belonging to a single species with a wide host range. Braun & Hill (2004) examined the collections on Co. verticillata, D. crenata, D. purpurascens, D. × rosea, F. procumbens, Nicotiana sp., and Braun et al. (2006) studied the samples on A. cunninghamiana and G. tinctoria. They referred all of them to C. api s. lat. as circumscribed in Crous & Braun (2003) as they are characterised by having hyaline acicular conidia formed singly, i.e. the present unnamed species is a C. apii-like plurivorous species.

Cercospora sp. J

Culture sequenced: Japan, Aichi, on Antirrhinum majus (Plantaginaceae), 8 May 2007, M. Matsusaki, MUMH10490, MUCC 541.

Notes: This isolate is phylogenetically distinct (Fig. 2 part 2) from the other species included in this study. Unfortunately, the specimen was not available for study.

Cercospora sp. K

Caespituli amphigenous. Mycelium internal. Stromata lacking or composed of a few brown cells. Conidiophores emerging through the cuticle or arising from stomatal openings, pale brown, paler towards the apex, almost uniform in width, sometimes narrowed at the apex following the sympodial proliferation, often constricted at septa and proliferating points, solitary or 2-3 in a loose fascicle, straight or slightly curved to sinuously geniculate, moderately thick-walled, 0-5-septate, 30-110 × 3.5-5 μm, truncate or conically truncate at the apex. Conidiogenous cells terminal, rarely intercalary, proliferating sympodially; loci slightly thickened, slightly protuberant (subtruncate) or flat, refractive, apical and lateral, 1.5-2.5 μm in diam. Conidia solitary, hyaline, filiform to acicular or obclavate, straight to slightly curved, truncate or obconically truncate at the slightly thickened at the basal end, acute at the apex, indistinctly or distinctly 1-14-septate, 35-230 × 1.5-5 μm, thin-walled, smooth.

Specimens examined: South Korea, Namyangju, on Ipomoea coccinea (≡ Quamoclit coccinea) (Convolvulaceae), 9 Oct. 2002, H.D. Shin, CPC 12391; 30 Sep. 2003, H.D. Shin, CBS 132603 =CPC 10719; 15 Oct. 2005, H.D. Shin, CPC 10094.

Notes: This species is phylogenetically supported based on DNA sequence data of ACT, CAL and HIS. In the TEF phylogeny, these isolates cannot be distinguished from C. ricinella, C. cf. chenopodii and C. delaireae. In the combined tree (Fig. 2 part 2), it is a sister taxon to C. cf. flagellaris. Different species of Cercospora have been described from Ipomoea spp. Cercospora ipomoeae-pedis-caprae was previously treated as a synonym of C. ipomoeae (Bagyanarayana et al. 1995, Shin & Kim 2001), since the length of the conidiophores and conidia in the latter species is variable. Braun et al. (2001) pointed out the differences among the Cercospora species on Ipomoea spp. based on the description of these species by García et al. (1996), and proposed that C. ipomoeae-pedis-caprae must be retained as a separate species. However, Cercospora isolates on Ipomoea cluster in three different places in the tree, and thus this complex remains unresolved and without epitypification the application of the names C. ipomoeae and C. ipomoeae-pedis-caprae remains unclear.

Cercospora sp. L

Specimen examined: New Zealand, on Crepis capillaris (Asteraceae), C.F. Hill, Lynfield 534, CBS 115477 =CPC 5114.

Notes: In vivo material on Crepis capillaris from New Zealand collected by C.F. Hill, Auckland, 9 Jul. 2000, deposited at HAL has been examined and is characterised as follows: Conidiophores solitary or in small, loose fascicles, straight to usually geniculate-sinuous, unbranched, 20-100 × 3-6 μm, usually 1-4-septate, pale olivaceous throughout or olivaceous-brown below and paler towards the tip; conidiogenous cells integrated, usually terminal, sympodial, multi-local; conidiogenous loci 2-3 μm diam, thickened and darkened; conidia solitary, acicular, short conidia occasionally subcylindrical, straight curved to somewhat sigmoid, 60-170 × 3-4 μm, pluriseptate, apex subacute or subobtuse, base truncate, occasionally slighty attenuated at the very base (at hilum), hila 2-3 μm wide. The application of the name Cercospora crepidis Onděj & Zavrěl, described from Europe (Czech Republic) on Crepis capillaris, for the fungus from New Zealand is not possible. The latter species is characterised by having obclavate conidia with distinctly obconically truncate base and short, aseptate conidiophores, only 14-22 μm long (Ondřej & Zavrěl 1971). In the TEF and CAL phylogeny this isolate clusters with C. zebrina and C. armoraciae and on a longer branch in the C. zebrina clade in the ACT phylogeny. It is only in the HIS phylogeny that this isolate is clearly distinct, clustering as sister taxon to C. delaireae. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. althaeina and C. zebrina.

Cercospora sp. M

Specimen examined: Thailand, Chachoengsao Province, Sanamchaikhet, on leaves of Acacia mangium (Fabaceae), 28 May 2003, K. Pongpanich, CBS H-9876, CBS 132596 =CPC 10553.

Notes: Crous et al. (2004b) isolated several species of Cercospora from A. mangium in Thailand, some of which were linked to single ascospore isolates of a mycosphaerella-like telemorph (see Crous et al. 2004b, fig. 5). Isolate CPC 10553 (=CBS 132596) occurred on the same leaf spots with C. acaciae-mangii (CBS 116365 =CPC 10526), which is here treated under Cercospora sp. P. The TEF phylogeny could not distinguish it from Cercospora spp. N-Q, C. kikuchii and C. cf. sigesbeckiae, whereas the HIS phylogeny could not distinguish it from some isolates of Cercospora spp. P and Q. The ACT phylogeny places it on a longer branch with C. rodmanii and C. cf. ipomoeae. The CAL phylogeny could not distinguish it from Cercospora spp. P and Q, C. alchemillicola / C. cf. alchemillicola and C. cf. sigesbeckiae. In the combined tree (Fig. 2 part 4), it is basal to the lineage containing C. rodmanii and other species.

Cercospora sp. N

Specimen examined: Bangladesh (western part), on Musa sp. (Musaceae), I. Buddenhagen, CBS 132619 =CPC 12684 (named as C. hayi).

Notes: Cercospora sp. N has shorter conidiophores than ascribed to C. hayi, which was described from Musa in Cuba. It is evident that a complex of Cercospora spp. occur on banana. The TEF phylogeny could not distinguish it from Cercospora spp. O-Q, C. kikuchii and C. cf. sigesbeckiae, whereas the HIS phylogeny could not distinguish it from some isolates of Cercospora spp. P and Q and C. rodmanii. The CAL phylogeny could not distinguish it from C. rodmanii, C. cf. richardiicola and C. cf. sigesbeckiae. The ACT phylogeny distinguishes it from the other species included in this study. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. cf. richardiicola and C. kikuchii.

Cercospora sp. O

Specimen examined: Thailand, Chiang Mai, Mae Klang Loung, N18°32.465’ E98°32.874’, on Musa sp. (Musaceae), 6 Oct. 2010, P.W. Crous, CBS 132635 =CPC 18636 (named as C. hayi).

Notes: Based on its shorter conidophores, Cercospora sp. O is distinct from C. hayi, and morphologically is more similar to Cercospora sp. N. The TEF phylogeny could not distinguish it from Cercospora spp. M, N and Q, C. kikuchii and C. cf. sigesbeckiae, whereas the HIS phylogeny could not distinguish it from some isolates of Cercospora spp. N, P and Q and C. rodmanii. The CAL phylogeny could not distinguish it from Cercospora spp. P and Q, C. alchemillicola / C. cf. alchemillicola and C. cf. sigesbeckiae and the ACT phylogeny from C. kikuchii. In the combined tree (Fig. 2 part 4), it is a sister taxon to C. cf. malloti.

Cercospora sp. P

Specimens examined: Ghana, on leaves of Dioscorea rotundata (Dioscoreaceae), 2000, S. Nyako & A.O. Danquah, CBS 132660 =CPC 11629 = GHA-4-0; CPC 11630 = GHA-4-3; CPC 11631 = GHA-5-0; CPC 11632 = GHA-7-4; CPC 11633 = GHA-8-4 (as C. dioscoreae-pyrifoliae). Japan, Okinawa, on Coffea arabica (Rubiaceae), C. Nakashima, MUMH 10823, MUCC 771 (as C. coffeicola). Mexico, Tamaulipas, on Ricinus communis, 31 Nov. 2008, Ma. de Jesús Yáñez-Morales, CBS 132680 =CPC 15827. New Zealand, Auckland (imported from Fiji islands), on leaves of Hibiscus sabdariffa (Malvaceae), C.F. Hill, Lynfield 578, CPC 5262. Papua New Guinea, on leaves of Dioscorea nummularia (Dioscoreaceae), 2000, J. Peters & A.N. Jama, CBS 132662 =CPC 11635 = PNG-009; on leaves of D. rotundata, 2000, J. Peters & A.N. Jama, CBS 132664 =CPC 11637 = PNG-022; on leaves of Dioscorea bulbifera (Dioscoreaceae), 2000, J. Peters & A.N. Jama, CBS 132665 =CPC 11638 = PNG-023. South Africa, Nelspruit, on Cajanus cajan (Fabaceae), L. van Jaarsveld, CBS 113996 =CPC 5326; CBS 115413 =CPC 5328; CPC 5327; Komatipoort, on Citrus ×sinensis (≡ C. aurantium var. sinensis) (Rutaceae), M.C. Pretorius, CBS 112728 =CPC 3949; CBS 112730 =CPC 3948; CBS 112894 =CPC 3950. Swaziland, on Citrus ×sinensis (≡ C. aurantium var. sinensis), M.C. Pretorius, CPC 4001; CPC 4002; on Citrus sp. leaf spot, M.C. Pretorius, CBS 112649 =CPC 3946; CBS 112722 =CPC 3947; CBS 115609 =CPC 3945. Thailand, on Acacia mangium, M.J. Wingfield, CBS 116365 =CPC 10526; CBS 132645 =CPC 10527 (Mycosphaerella teleomorph ascospore isolate, ex-type of Cercospora acaciae-mangii, small colonies); on A. mangium, K. Pongpanich, CPC 10552.

Notes: Isolates of this clade were mainly obtained from Acacia, Cajanus, Citrus (Rutaceae), Coffea (Rubiaceae), Dioscorea, Hibiscus (Malvaceae) and Ricinus (Euphorbiaceae). Many previously described species names have in the past been applied to different isolates clustering in this clade. Based on the gene loci screened in the present study, we were unable to resolve the taxonomy of these isolates, and for now prefer to treat them as an unresolved species complex. In none of the single-gene phylogenies generated in this study did the isolates from this species form a pure monophyletic lineage, as isolates were frequently intermixed with that of Cercospora sp. Q, C. cf. sigesbeckiae and C. cf. richardiicola. Given this overlap in sequence identity and host species, it is possible that Cercospora spp. P (Fig. 2 parts 4-5) and Q (Fig. 2 part 5) could be considered as a single species complex (see species notes for Cercospora sp. Q below). More extensive screening of additional loci is needed to define the species boundaries in this complex. Also present in this complex are numerous isolates from Dioscorea, for which the name C. dioscoreae-pyrifoliae could have been a candidate. From the present study it is clear that several species of Cercospora can be isolated from this host and a more detailed study is needed to fix that name to a specific lineage.

The ex-type culture of Cercospora acaciae-mangii (Crous et al. 2004) is located in the last subclade (Fig. 2 part 5). Cercospora acaciae-mangii was isolated from Acacia leaves that also contained a mycosphaerella-like teleomorph that formed a Cercospora state in culture. However, the same leaf spots were also colonised by a second, morphologically similar species (distinguished by its ability to form larger, faster-growing colonies in agar).

Cercospora sp. Q

Specimens examined: Mexico, on Phaseolus vulgaris (Fabaceae), 20 Oct. 2008, M. de Jesus Yanez, CBS 132679 =CPC 15807; Tamaulipas, on Taraxacum sp. (Asteraceae), 30 Oct. 2008, Ma. de Jesús Yáñez-Morales, CBS 132682 =CPC 15850; on Euphorbia sp. (Euphorbiaceae), 31 Oct. 2008, Ma. de Jesús Yáñez-Morales, CPC 15875; 30 Oct. 2008, Ma. de Jesús Yáñez-Morales, CBS 132681 =CPC 15844. Papua New Guinea, on leaves of Dioscorea rotundata, 2000, J. Peters & A.N. Jama, CBS 132661 =CPC 11634 = PNG-002, on leaves of Dioscorea esculenta (Dioscoreaceae), 2000, J. Peters & A.N. Jama, CBS 132663 =CPC 11636 = PNG-016; CPC 11639 = PNG-037. South Africa, Nelspruit, on Cajanus cajan, L. van Jaarsveld, CBS 113997 =CPC 5325; CBS 115410 =CPC 5331; CBS 115411 =CPC 5332; CBS 115412 =CPC 5333; CBS 115536 =CPC 5329; CBS 115537 =CPC 5330. Thailand, on Acacia mangium, K. Pongpanich, CPC 10550 (big colony on same plate as small colonies of Cercospora acaciae-mangii); CPC 10551 (big colony); CBS 132656 =CPC 11536; CPC 11539.

Notes: Several isolates from diverse hosts and families cluster in this clade, to which different names can be applied. To resolve their taxonomy, fresh collections authentic for the names (based on host and country) need to be recollected and included in future studies. Based on the genes studied here, we were unable to resolve the phylogeny of these taxa. See also the species notes for Cercospora sp. P. Screening the isolates from this species with five more genomic loci in this study did not clarify their potential species boundaries. By testing other candidate loci as they become available from comparative genomics and other sources we will continue to try and identify optimal genes for species recognision in this complex.

Cercospora sp. R

Specimen examined: New Zealand, Auckland, Grey Lynn, on Myoporum laetum (Myoporaceae), Dec. 2003, C.F. Hill, Lynfield 186-B, CBS 114644.

Notes: Pseudocercosporella myopori is a true species of Pseudocercosporella (Braun & Hill 2002), which was originally described without deposting an ex-type culture. A later collection deposited at CBS (isolate CBS 114644), however, proved to be representative of an undescribed species of Cercospora, phylogenetically closely related to Cercospora sp. S and C. corchori (Fig. 2 part 5). This isolate has a unique phylogenetic position in the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 5), it is a sister taxon to Cercospora sp. S.

Cercospora sp. S

Specimen examined: South Korea, Yangpyeong, on Crepidiastrum denticulatum (≡ Youngia denticulata) (Asteraceae), 30 Sep. 2003, H.D. Shin, CBS 132599 =CPC 10656; CPC 10654-10655 (as Cercospora lactucae-sativae).

Notes: Isolate CPC 10656 is located on a slightly longer branch in the majority of genomic loci evaluated (ACT, CAL and HIS); only in the TEF phylogeny is it intermixed with isolates of C. lactucae-sativae. It is a close sister taxon to Cercospora sp. R and C. corchori (Fig. 2 part 5), but more isolates need to be collected to resolve its identity.

Cercospora vignigena C. Nakash., Crous, U. Braun & H.D. Shin, sp. nov. MycoBank MB800657. Fig. 10.

Fig. 10.

Fig. 10.

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Cercospora vignigena (CBS 132611 =CPC 10812). A. Leaf spots. B. Close-up of lesion. C-E. Fasciculate conidiophores. F-I. Conidia. Scale bars = 10 μm.

Etymology: Named after the host genus from which it was collected, Vigna.

Leaf spots subcircular, amphigenous, pale to medium brown, 8-20 mm diam, with inconspicuous margin. Caespituli amphigenous. Mycelium internal. Stromata small to well-developed, pale brown to brown, intraepidermal and substomatal, 35-60 μm in diam. Conidiophores in loose to dense fascicles (2-12), straight to slightly sinuous-geniculate, pale brown, paler towards the apex, moderately thick-walled or thick-walled, cylindrical, almost uniform in width, often wider towards the apex, distinctly conical at the apex, 40-130 × 5-7(-10) μm, 0-3-septate. Conidiogenous cells integrated, terminal, intercalary, proliferating sympodially, 20-40 × 4-5 μm, multi-local (1-2); loci distinctly thickened, darkened, slightly protuberant, apical and lateral, 2.5-4 μm diam. Conidia solitary, rarely catenate, hyaline, straight to slightly curved, cylindrical to obclavate, obconically truncate and distinctly thickened at the base, subobtuse to obtuse at the apex, (35-)45-70(-150) × (2.5-)4-6(-10) μm, (3-)4-7(-14)-septate, thin-walled, smooth.

Culture characteristics: Colonies spreading, erumpent, with even, lobate margins and sparse to moderate aerial mycelium, reaching 25 mm diam after 2 wk. On OA olivaceous-grey in centre, pale olivaceous-grey in outer region. On MEA pale olivaceous-grey with patches of dirty white, reverse iron-grey. On PDA pale olivaceous-grey, margin submerged, grey-olivaceous; reverse olivaceous-grey.

Specimens examined: Japan, Gumma, on Vigna unguiculata (= V. sinensis) (Fabaceae), Sep. 1993, K. Kishi, MUCC 579 = MAFF 237635. South Africa, Potchefstroom, on V. unguiculata (= V. sinensis), 3 Jan. 1995, S. van Wyk, CPC 1133-1134. South Korea, Jeongeup, on V. unguiculata (= V. sinensis), 29 Oct. 2003, H.D. Shin, holotype CBS H-21023, culture ex-type CBS 132611 =CPC 10812.

Notes: This independent clade is supported by ACT, CAL and HIS and is composed of the isolates of Cercospora species that were identified as C. canescens on Vigna (Fabaceae) plants. In the TEF phylogeny, the clade is split into two lineages, isolates CPC 1134 and MUCC 579 as sister clade to C. apiicola and CPC 10812 basal to C. apii and C. beticola. In the combined tree (Fig. 2 part 2), it is basal to the lineage containing C. apiicola and other species. The examined isolates of C. canescens (the true C. canescens has acicular conidia), for which the original host is the genus Phaseolus, were located in other clades. These results show that the fungus on Vigna must be treated as a species distinct from C. canescens. Cercospora vignicaulis (described on V. unguiculata (= V. sinensis) collected from the USA) has in the past been listed as a synonym of C. canescens. However, C. vignicaulis has acicular conidia, which differs from the isolates studied here, and thus the present collection is described as a distinct species that appears to be specific to Vigna.

Cercospora violae Sacc., Nuovo Giron. Bot. Ital. 8: 187. 1876.

  • = Cercospora violae-tricoloris Briosi & Cavara, Atti Ist. Bot. Univ. Pavia 2: 285. 1892.

  • = Cercospora violae var. minor Rota-Rossi, Atti Ist. Bot, Univ. Pavia, Ser. 2, 13: 199. 1914.

  • = Cercospora violae-kiusianae Sawada, Rep. Gov. Agric. Res. Inst. Taiwan 85: 126. 1943.

  • = Cercospora difformis Tehon, Mycologia 40: 322. 1948.

  • = Cercospora trinctatis Pass. (unpublished name cited by Chupp 1954)

Caespituli amphigenous. Mycelium internal. Stromata lacking to well-developed, up to 80 μm diam, brown, intraepidermal, substomatal. Conidiophores in dense fascicles (2-16), irregular in width, slightly attenuated at the upper portion, straight or mildly sinuous-geniculate, straight, wall moderately thickened, simple, pale brown to brown, short conically truncate at the apex, wider at the base, 20-175 × 2.5-7.5 μm, 1-10-septate, usually uni-local. Conidiogenous cells integrated, terminal, rarely intercalary, proliferating sympodially; loci distinct, thickened, apical, rarely lateral, 2-3 μm diam, not protuberant. Conidia solitary, hyaline, cylindrical to obclavate or acicular, distinctly thickened and obconically truncated at the base, obtuse at the apex, 35-195 × 2.5-5 μm, 0-18-septate, thin-walled, smooth.

Specimens examined: Italy, Selva, on Viola odorata (Violaceae), Aug. 1874, Treviso, isotypes distributed as Sacc. Mycotheca Veneta 279, isotype at HAL examined. Japan, Kochi, on Viola sp., 16 Nov. 2004, J. Nishikawa, MUMH 10333, MUCC 129; Nagano, on V. tricolor, 16 Feb. 2005, J. Nishikawa, MUMH 10332, MUCC 133; Shizuoka, on V. tricolor, 15 Jan. 2003, J. Nishikawa, MUMH 10334, MUCC 136. Romania, Cazanele Dunarii, on V. tricolor, O. Constantinescu, epitype designated here CBS H-21024, culture ex-epitype CBS 251.67 = CPC 5079. New Zealand, on V. odorata, C.F. Hill, CPC 5368.

Notes: See also C. zebrina. One culture that was isolated from Viola (strain CPC 10725) is representative of C. fagopyri. The original specimen of this isolate was distinguishable from C. violae in having circumspersed and slightly protuberant loci on its conidiophores. The isolates included here for C. violae are phylogenetically distinct from the other species included in this study on the basis of the TEF, ACT, CAL and HIS phylogenies. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. zebrina.

Cercospora zeae-maydis Tehon & E.Y. Daniels, Mycologia 17: 248. 1925.

Specimens examined: China, Liaoning Province, on Zea mays (Poaceae), CBS 132668 =CPC 12225 = CHME 52. Mexico, Tlacotepec, on Z. mays, 16 Sep. 2008, Ma. de Jesús Yáñez-Morales, CBS 132678 =CPC 15602. USA, Illinois, Alexander Co., McClure, on Z. mays, 29 Aug. 1924, P.A. Young, holotype ILLS 4276, isotype BPI 442569; Delaware, 1997, B. Fleener, DE-97 = A359 = CBS 117756; Indiana, Princeton, 1999, B. Fleener, PR-IN-99 = A364 = CBS 117761; Indiana, Princeton, 2003, B. Fleener, YA-03 = A358 = CBS 117755; Iowa, Johnston, 2004, B. Fleener, JH-IA-04 = A361 = CBS 117758; Iowa, Reinbeck, 1999, B. Fleener, RENBECK-IA-99 = A367 = CBS 117763; Missouri, Dexter, 2000, B. Fleener, DEXTER-MO-00 = A365 = CBS 117762; Pennsylvania, New Holland, 1999, B. Fleener, NH-PA-99 = A363 = CBS 117760; Tennessee, Union City, 1999, B. Fleener, UC-TN-99 = A362 = CBS 117759; Wisconsin, Janesville, 2002, B. Fleener, epitype, CBS H-17774, culture ex-epitype JV-WI-02 = A360 = CBS 117757.

Notes: This species is phylogenetically supported by ITS, TEF, ACT, CAL and HIS. In the combined tree (Fig. 2 part 1), it is a basal lineage. Gray leaf spot of maize was originally attributed to “group I” and “group II” siblings of C. zeae-maydis (Wang et al. 1998). More detailed information on this species was provided in Crous et al. (2006a).

Cercospora zebrina Pass., Hedwigia 16: 124. 1877.

    • ≡ Cercosporina zebrina (Pass.) Matsuura, J. Pl. Protect. (Tokyo) 17: 1. 1930.

  • = Cercospora helvola Sacc., Michelia 2: 556. 1882.

  • = Cercospora stolziana Magnus, Die Pilze von Tirol (etc.) 3: 558. 1905.

  • == Cercospora helvola var. zebrina Ferraris, Fl. Ital. Cryptog. 1: 423, 1910, fide Chupp (1954: 341).

Specimens examined: Australia, on Trifolium cernuum (Fabaceae), M.J. Barbetti, CBS 118791 =IMI 264190 = WA 2054 = WAC 7993; on T. subterraneum, M.J. Barbetti, CBS 118789 =WAC 5106; CBS 118790 =IMI 262766 = WA 2030 = WAC 7973. Canada, Ottawa, 13 Lucas lane, on T. repens, 1 Sep. 2000, K.A. Seifert, CBS H-21025, CBS 112723 =CPC 3957; CBS 112736 =CPC 3958; on T. pratense, K.A. Seifert, CBS H-21026, CBS 112893 =CPC 3955. Italy, on Hedysarum coronarium (Fabaceae), CBS 137.56 = CPC 5118 (as C. ariminensis). New Zealand, on Hebe sp. (Scrophulariaceae), C.F. Hill, CBS 114359 =CPC 10901; Auckland, on Lotus pedunculatus (Fabaceae), C.F. Hill, Lynfield 644, CPC 5437 (as C. loti); Blockhouse Bay, on T. repens, C.F. Hill, Lynfield 603, CBS 113070 =CPC 5367; on Jacaranda mimosifolia (Bignoniaceae), C.F. Hill, Lynfield 693, CPC 5473 (as C. canescens). Romania, Hagieni, on Astragalus spruneri (Fabaceae), O. Constantinescu, CBS 537.71 = IMI 161108 = CPC 5089 (as C. astragali). South Korea, Namyangju, on T. repens, 22 Oct. 2003, H.D. Shin, CBS H-21027, CBS 132650 =CPC 10756. Unknown, on Medicago arabica (= M. maculata) (Fabaceae), E.F. Hopkins, CBS 108.22 = CPC 5091 (as C. medicaginis). USA, Wisconsin, on T. subterraneum, CBS 129.39 = CPC 5078.

Notes: Morphological characteristics of the larger C. zebrina clade include conidiophores that are short, almost straight, slightly attenuated and distinctly conically truncate at the apex with distinctly thickened loci, and conidia, which are cylindrical to cylindro-obclavate. The type of C. zebrina was collected on Trifolium in Italy. More European collections are required to resolve this species and to delinate it from other, closely allied species.

Cercospora althaeina, which has wide host range on malvaceous plants, has a similar morphology to C. zebrina. Cercospora violae, which clusters basal to the C. zebrina clade, has longer and wider conidiophores, and cylindrical to acicular conidia, which separates this species from C. zebrina.

In the TEF phylogeny, isolates are intermixed with those of C. armoraciae, C. rumicis and Cercospora sp. L and in the ACT and CAL phylogenies with those of Cercospora sp. L and C. althaeina. Only in the HIS phylogeny do these isolates form a pure monophyletic clade. In the combined tree (Fig. 2 part 3), it is a sister taxon to C. violae.

Cercospora zeina Crous & U. Braun, Stud. Mycol. 55: 194. 2006.

Specimens examined: South Africa, KwaZulu-Natal, Pietermaritzburg, on Zea mays (Poaceae), 2005, P. Caldwell, holotype CBS H-17775, culture ex-type CBS 118820 =CPC 11995; CBS 132617 =CPC 11998.

Notes: This species is phylogenetically supported by ITS, TEF, ACT, CAL and HIS. In the combined tree (Fig. 2 part 1), it is a basal lineage. More detailed information on this species was provided in Crous et al. (2006a).

Cercospora cf. zinniae

Caespituli amphigenous. Mycelium internal. Stromata lacking to small, up to 35 μm diam, intraepidermal or substomatal, pale brown to brown. Conidiophores in loose fascicles (3-8), pale brown to brown, straight, mildly geniculate above the middle, multi-septate, attenuated, successively geniculate, tip truncate or conically truncate, 65-300 × 3.5-5 μm, 1-12-septate. Conidiogenous cells integrated, proliferating sympodially, terminal and intercalary, multi-local; loci distinctly thickened, darkened, apical and lateral, sometimes circumspersed, often slightly protuberant, 2-2.5 μm diam. Conidia solitary, hyaline, filiform to acicular, cylindro-obclavate, straight to curved, long obconically truncate or truncate, and thickened at the base, acute at the apex, multi-septate, 30-120 × 1-4 μm, 3-13-septate.

Description of caespituli on V8; (MUCC 131): Conidiophores solitary, arising from hyphae, subhyaline to pale brown, irregular in width, smooth, meager and thin-walled, sinuous-geniculate to geniculate, unbranched, truncate or conically truncate at the tip, 13-63 × 3-5 μm, multi-septate. Conidiogenous cells integrated, terminal, proliferating sympodially, single to multi-local (1-2); loci moderately thickened, apical, sometimes slightly protuberant, 1.25-2 μm in width. Conidia hyaline, filiform to acicular, slightly thickened and long obconically truncate at the base, acute to obtuse at the apex, 25-160 × 2.5-4 μm, 3-11-septate.

Specimens examined: Brazil, Valverde, Alto Rio Doce, on unknown substrate, A.C. Alfenas, CBS 132676 =CPC 15075. Japan, Chiba, on Zinnia elegans (Asteraceae), 12 Sep. 1997, S. Uematsu, MUCC 572 = MAFF 237718 = MUCNS 215; Shizuoka, on Z. elegans, 17 Sep. 2004, J. Nishikawa, MUMH 11397, MUCC 131. South Korea, Yangpyeong, on Z. elegans, 18 Oct. 2007, H.D. Shin, CBS 132624 =CPC 14549.

Notes: This species is characterised in that the conidiophores are mildly geniculate above the middle, multi-septate, attenuated with successive geniculation; loci circumspersed and distinctly thickened; conidia are narrower than those of other taxa in C. apii s. lat. Moreover, this species is phylogenetically supported by DNA sequence data of TEF, CAL and HIS. In the ACT phylogeny, two distinct lineages are formed, namely CPC 14549 versus CPC 15075, MUCC 132 and MUCC 572. In the combined tree (Fig. 2 part 4), it is basal to the lineage containing, for example, C. cf. ipomoeae, C. fagopyri and C. rodmanii. North American cultures and sequence data are necessary to confirm the identity of Asian collections as C. zinniae and to designate an epitype.

DISCUSSION

This study was initiated to resolve Cercospora taxonomy on the basis of morphological and DNA sequence data. Based on our earlier studies incorporating multi-gene phylogenies on smaller datasets (Crous et al. 2004b, 2006a, Groenewald et al. 2005, 2006a, 2010a), we realised this was an ambitious task. Even though a whole range of hosts and countries were included in our study, attempts to apply existing names to the different clades in the phylogenetic trees obtained proved difficult. In addition, the lack of ex-type cultures or at least reference sequences from type material, made it especially problematic to assign existing names to the derived phylogenetic clades. To our knowledge, this study presently represents the largest combination of diverse sampling of cercosporoid fungi coupled with multi-locus sequence data in a single manuscript.

One important finding is that Crous & Braun (2003) were over-optimistic when they referred 281 Cercospora names to C. apii s. lat. based on morphology alone. Of the species treated as distinct in the present paper, the following five were originally referred to C. apii s. lat. by Crous & Braun (2003), namely C. beticola, C. canescens, C. fagopyri, C. kikuchii and C. rumicis. The following eight species, C. armoraciae, C. corchori, C. lactucae-sativae, C. mercurialis, C. polygonacea, C. ricinella, C. violae and C. zebrina, treated as distinct in the present study, were treated by Crous & Braun (2003) as close to or possibly identical with C. apii s. lat. It is evident that morphology alone provides an insufficient basis on which to establish synonymies, to describe novel species or in many cases to identify species of Cercospora.

In the last 10 years, 45 novel Cercospora names were lodged with MycoBank (Crous et al. 2004a). Of these, only five species are based on morphology and multi-locus sequence data, two species have morphology supplemented with ITS sequences and 38 species are based on morphology alone. Of these 45 species, only 10 species were described in culture, 26 were reported without culture characteristics and of the remaining nine it is unlikely that cultures were established. This is an alarming statistic and is something that should be addressed by the whole community working on cercosporoid fungi. If the situation is compared to that of Colletotrichum, it is clear that there is room for improvement. Phylogenetic studies on Colletotrichum species based on cultures and ITS data date back to at least 20 years, with the last 10 years showing a significant increase in species descriptions based on multi-locus sequence data (Cannon et al. 2012).

Groenewald et al. (2010a) reported on the performance of the five loci used for the phylogenetic inference in this study. They found the ITS region had limited resolution (2.7 % clade recovery) and was best be used to confirm the generic affiliation of a species, with less value when used for species comparison, specifically within the C. apii complex. Although CAL is necessary to distinguish C. apii and C. beticola, it only distinguished about half of the observed species clades (46.6 % clade recovery), whereas ACT was slightly more successful (58.9 % clade recovery). The HIS region compared well with ACT (63 % clade recovery), but it did split C. beticola into two clades. Both of these C. beticola clades contain isolates from the same sugar beet fields in Germany and New Zealand (Groenewald et al. 2006b) and whether this implies population variation or the presence of an additional cryptic species on sugar beet requires further molecular analyses of more C. beticola populations. The TEF region was comparable to CAL in terms of clade recovery (45 % clade recovery). Although we believe that there is still a need to identify the best barcode locus for Cercospora, the current multi-locus approach does enable species identification. Comparison of a few Cercospora genomes selected from across the phylogenetic tree might reveal a single locus with better resolution than the currently used loci.

Similar to the situation in Pseudocercospora (Crous et al. 2013), we also encountered a situation where we could not use names based on North American or European types for African or Asian cultures and vice versa. Based on morphological features and their distinct sequences we have chosen to treat those clades in the present study as “cf.” pending comparison of those species with (epi-)type material from the original country and host as discussed under the species notes above. For numerous clades (“Cercospora sp. A-S”), it was not possible to unequivocally assign a species name; frequently these clades contained isolates from multiple hosts and/or countries and the same hosts occurred in multiple clades, or the host information was not available. For example, isolates from Cajanus cajan in South Africa can be attributed to Cercospora sp. P and Cercospora sp. Q. Crous & Braun (2003) list four Cercospora species associated with this host, namely C. apii s. str., C. canescens, C. instabilis and C. thirumalacharii. The first two species were included in this study, the third is listed on Cajanus from numerous countries (but not including South Africa) and the last is known from India (Crous & Braun 2003). It was not possible to include authentic cultures of the latter two species, so any of these two names are potentially available for a clade. An additional complicating factor is that there are numerous sub-clades inside Cercospora sp. P and Cercospora sp. Q, which could represent either intra-specific variation or the presence of cryptic species, which are not distinguished by the loci used in this study. We sequenced five additional loci for Cercospora sp. Q isolates and did not find a single locus that provided better insight into this clade. Isolates from Cajanus also occur in the same clade with other hosts, raising the question of wide host range versus simply a chance infection (Crous & Groenewald 2005). A similar situation was observed for isolates isolated from yams (Dioscorea). Crous & Braun (2003) list numerous Pseudocercospora and Passalora species, and three Cercospora species (C. aragonensis, C. dioscoreae-pyrifoliae and C. golaghatti) from this host genus; of the three Cercospora names, C. dioscoreae-pyrifoliae is commonly used in literature. In this study, it was not possible to apply this name to any of the clades. Isolates from Dioscorea are found in the C. canescens complex, Cercospora cf. sigesbeckiae, Cercospora sp. P and Cercospora sp. Q, but none of these isolates were from the original host or locality of the type description for C. dioscoreae-pyrifoliae (based on Dioscorea pyrifolia in Singapore). One of the isolates included in the present study (MUCC 849, as Cercospora cf. sigesbeckiae) was treated by Nakashima et al. (2011) as C. dioscoreae-pyrifoliae. The authors noted that, although the morphological characteristics were similar to the original description, the width of the conidiophores and conidia was different. Similarly, most of the isolates from Dioscorea were sent to us under the name C. dioscoreae-pyrifoliae although we could not confirm the identification with confidence. These examples highlight the need to locate original specimens, or at least recollect material that can be used for epitypification, to fix the names used in the various phylogenetic clades. It also illustrates the importance of establishing cultures, which can be used for future molecular studies, when describing taxonomic novelties.

We believe that this study serves as a backbone for future studies on Cercospora taxonomy. Unfortunately, many (epi-)type cultures and adequate sequence data are lacking for a significant number of Cercospora species. Future studies will require the recollection of material from the original hosts and continents so that epitypes can be found and names stabilised. Furthermore, all species, especially those currently in common use, need proper molecular identification. Based on searches in Google and Google Scholar, the most commonly used Cercospora species names are C. zeae-maydis, C. beticola, C. apii, C. canescens, C. kikuchii, C. sojina, C. arachidicola, C. coffeicola, C. personata and C. nicotianae. Although the taxonomy of C. apii, C. beticola (Groenewald et al. 2005, 2006a) and C. zeae-maydis (Crous et al. 2006a) was resolved in the past, the present study resolved C. kikuchii and C. sojina but it was unable to resolve C. canescens. Similar studies are needed for C. arachidicola, C. coffeicola, C. nicotianae and C. personata.

Acknowledgments

We would like to thank all colleagues for supplying us with material and cultures, without which this study would not have been possible. We thank the technical staff, Arien van Iperen (cultures), Marjan Vermaas (photographic plates), and Mieke Starink-Willemse (DNA isolation, amplification and sequencing) for their invaluable assistance.

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