Skip to main content
NCBI home page
IMA Fungus logoLink to IMA Fungus
. 2013 Oct 28;4(2):187–199. doi: 10.5598/imafungus.2013.04.02.04

Septoria-like pathogens causing leaf and fruit spot of pistachio

Pedro W Crous 1,2,3,✉, William Quaedvlieg 1,2, Kamil Sarpkaya 4, Canan Can 5, Ali Erkılıç 6
PMCID: PMC3905937  PMID: 24563831

Abstract

Several species of Septoria are associated with leaf and fruit spot of pistachio (Pistacia vera), though their identity has always been confused, making identification problematic. The present study elucidates the taxonomy of the Septoria spp. associated with pistachio, and distinguishes four species associated with this host genus. Partial nucleotide sequence data for five gene loci, ITS, LSU, EF-1α, RPB2 and Btub were generated for a subset of isolates. Cylindroseptoria pistaciae, which is associated with leaf spots of Pistacia lentiscus in Spain, is characterised by pycnidial conidiomata that give rise to cylindrical, aseptate conidia. Two species of Septoria s. str. are also recognised on pistachio, S. pistaciarum, and S. pistaciae. The latter is part of the S. protearum species complex, and appears to be a wide host range pathogen occurring on hosts in several different plant families. Septoria pistacina, a major pathogen of pistachio in Turkey, is shown to belong to Pseudocercospora, and not Septoria as earlier suspected. Other than for its pycnidial conidiomata, it is a typical species of Pseudocercospora based on its smooth, pigmented conidiogenous cells and septate conidia. This phenomenon has also been observed in Pallidocercospora, and seriously questions the value of conidiomatal structure at generic level, which has traditionally been used to separate hyphomycetous from coelomycetous ascomycetes. Other than DNA barcodes to facilitate the molecular identification of these taxa occurring on pistachio, a key is also provided to distinguish species based on morphology.

Keywords: Capnodiales, coelomycete, hyphomycete, ITS, LSU, Mycosphaerellaceae, Pistachia, Pseudocercospora, RPB2, Septoria, systematics

INTRODUCTION

The genus Pistacia (Anacardiaceae), which is believed to have originated in Central Asia, consists of at least 11 species (Parfitt & Badenes 1997). Among these, Pistacia vera (pistachio), which is native to Western Asia and parts of the Middle East, is the only cultivated and economically important species (Tous & Ferguson 1996). Several important plant pathogens have been recorded from pistachio, causing fruit and root rot, blossom and shoot blight, canker and rust, and other problems (Michailides et al. 1995, http://nt.ars-grin.gov/fungaldatabases/). Of these, Septoria leaf spot is one of the more important diseases associated with fruit and leaf spot.

Desmaziéres (1842) published the first description of a Septoria species causing a leaf spot of Pistacia vera in northern France, for which he introduced the name S. pistaciae. In the same year, Léveillé (1842) described and illustrated Dothidea pistaciae causing a leaf spot of a Pistacia sp. in Crimea. Cooke (1884), upon examination of the type material on which Léveillé based D. pistaciae, transferred it to Septoria. Apparently Cooke was unaware of the existence of Desmaziéres’ name. Allescher (1901) proposed the binominal S. pistacina to replace S. pistaciae (Lév.) Cooke 1884 and to differentiate it from S. pistaciae Desm. 1842. Caracciolo (1934) reported a third species from pistachio as causing a serious leaf spot in Sicily, which he subsequently described as S. pistaciarum. Finally, Chitzanidis (1956) reported sexual morphs for two of the three species, namely Mycosphaerella pistacina (for Septoria pistacina) and Mycosphaerella pistaciarum (for Septoria pistaciarum) (Teviotdale et al. 2001).

Septoria pistaciarum is known from the USA, and the eastern Mediterranean and southeast Anatolian regions (Young & Michailides 1989). Septoria pistaciae is known from the USA (Califonia), Asia (Armenia, Republic of Georgia, India, Israel, Kazakhstan, Kirgizstan, Syria, Tadjikistan, Turkey, Turkmenistan and Uzbekistan), Europe (Albania, France, Greece, Italy, Portugal and Ukraine), and Africa (Egypt) (Pantidou 1973, Dudka et al. 2004, Andrianova & Minter 2004, Haggag et al. 2006). Septoria pistacina is known from Greece (Chitzanidis 1956), Syria, Turkey and Iran (Aghajani et al. 2009), and appears to have a more limited distribution.

The application of these Septoria names to the respective diseases that they are associated with has been plagued by confusion ever since they were first introduced. The aim of the present study is to elucidate the taxonomy of the Septoria species associated with fruit and leaf spot diseases of pistachio, and to place them in a phylogenetic context within Mycosphaerellaceae.

MATERIALS AND METHODS

Isolates

Isolations were made from leaf spots by placing leaves in damp chambers for 1–2 d to enhance sporulation. Single conidial colonies were established from sporulating conidiomata on Petri dishes containing 2 % malt extract agar (MEA) as described earlier (Crous et al. 1991). Additional strains were obtained from the culture collection of the CBS-KNAW Fungal Biodiversity Centre (CBS), Utrecht, The Netherlands. Colonies were subcultured onto potato-dextrose agar (PDA), oatmeal agar (OA), and MEA (Crous et al. 2009c), and incubated at 25 °C under continuous near-ultraviolet light to promote sporulation. Reference strains were deposited at the CBS (Table 1).

Table 1.

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

Species Isolate no.1 Host Location Collected by GenBank accession no.2
RPB2 LSU ITS Btub EF-1α
Caryophylloseptoria lychnidis CBS 109098 Silene pratensis Austria G. Verkley KF252292 KF251790 – – –
Caryophylloseptoria silenes CBS 109100 Silene nutans Austria G. Verkley KF252298 KF251796 – – –
CBS 109103 Silene pratensis Austria G. Verkley KF252299 KF251797 – – –
Caryophylloseptoria spergulae CBS 109010 Spergula morisonii Netherlands A. Aptroot KF252487 KF251995 – – –
CBS 397.52 Dianthus caryophyllus Netherlands Schouten KF252301 KF251799 – – –
Cercospora apii CBS 118712 – Fiji P. Tyler KF252302 KF251800 – – –
Cercospora ariminensis CBS 137.56 Hedysarum coronarium Italy M. Ribaldi KF252303 KF251801 – – –
Cercospora beticola CBS 124.31 Beta vulgaris Romania – KF252155 KF251650 – – –
Cercospora zebrina CBS 118790 Trifolium subterraneum Australia M.J. Barbetti KF252156 KF251651 – – –
Cylindroseptoria pistaciae CBS 471.69 Pistacia lentiscus Spain H.A. van der Aa KF252161 KF251656 – – –
Pallidocercospora acaciigena CBS 112515 Acacia mangium Venezuela M.J. Wingfield KF442687 KF442656 – – –
CBS 112516 Acacia mangium Venezuela M.J. Wingfield KF442688 GU253697 – – –
Pallidocercospora colombiensis CBS 110968 Eucalyptus urophylla Colombia M.J. Wingfield KF442689 AY752148 – – –
CBS 110969 Eucalyptus urophylla Colombia M.J. Wingfield KF442690 KF442657 – – –
Pallidocercospora crystallina CBS 110699 Leucospermum USA P.W. Crous KF442691 KF442658 – – –
CBS 111045 Eucalyptus grandis South Africa M.J. Wingfield KF442692 KF442659 – – –
CBS 681.95 Eucalyptus bicostata South Africa M.J. Wingfield KF442693 EU167579 – – –
Pallidocercospora heimii CPC 11441 – Brazil A.C. Alfenas KF442694 KF442660 – – –
CPC 11716 – Brazil A.C. Alfenas KF442695 KF442661 – – –
CPC 11926 Acacia auriculiformis Thailand W. Himaman KF442696 KF442662 – – –
CPC 13099 Eucalyptus dunnii Australia A.J. Carnegie KF442697 GQ852606 – – –
CBS 110682 Eucalyptus sp. Madagascar P.W. Crous KF442698 GQ852604 – – –
Pallidocercospora heimioides CBS 111190 Eucalyptus sp. Indonesia M.J. Wingfield KF442699 GU214439 – – –
CBS 111364 – Indonesia M.J. Wingfield KF442700 KF442663 – – –
Pallidocercospora irregulariramosa CBS 111211 Eucalyptus saligna South Africa M.J. Wingfield KF442701 KF442664 – – –
Pallidocercospora konae CPC 10992 Eucalyptus sp. Colombia M.J. Wingfield KF442702 KF442665 – – –
Pallidocercospora sp. CPC 21817 Ventilago denticulata Thailand P.W. Crous KF442703 KF442666 KF442645 – –
Pallidocercospora thailandica CBS 120723 Eucalyptus camaldulensis Thailand W. Himaman KF442704 KF442667 – – –
Phaeophleospora stonei CBS 120830 Eucalyptus sp. Australia P.W. Crous KF442705 KF442668 – – –
Pseudocercospora angolensis CBS 112748 Citrus sp. Zimbabwe P.W. Crous JX902001 JX901878 – – –
CBS 112933 Citrus sp. Zimbabwe M.C. Pretorius JX902002 JX901879 – – –
CBS 115645 Citrus sp. Zimbabwe P.W. Crous JX902003 JX901880 – – –
CBS 149.53 Citrus sinensis Angola T. de Carvalho & O. Mendes JX902004 JX901881 – – –
CBS 244.94 Citrus sp. Zimbabwe P.W. Crous JX902000 JX901877 – – –
Pseudocercospora assamensis CBS 122467 Musa sp. India I.W. Buddenhagen JX902005 JX901882 – – –
Pseudocercospora atromarginalis CPC 11372 Solanun nigrum South Korea H.D. Shin JX902006 JX901883 – – –
Pseudocercospora basiramifera CBS 111072 Eucalyptus pellita Thailand M.J. Wingfield KF442706 GU253709 – – –
CBS 114757 Eucalyptus pellita Thailand M.J. Wingfield KF442707 GU253802 – – –
Pseudocercospora basitruncata CBS 114664 Eucalyptus grandis Colombia M.J. Wingfield KF442708 GU253710 – – –
Pseudocercospora cercidis-chinensis CPC 14481 Cercis chinensis South Korea H.D. Shin JX902007 JX901884 – – –
Pseudocercospora chiangmaiensis CBS 123244 Eucalyptus camaldurensis Thailand R. Cheewangkoon JX902008 JX901885 – – –
Pseudocercospora clematidis CPC 11657 Clematis sp. USA M. Palm JX902009 JX901886 – – –
Pseudocercospora crousii CBS 119487 Eucalyptus sp. New Zealand C.F. Hill KF442709 GQ852631 – – –
Pseudocercospora eucalyptorum CBS 110776 Eucalyptus nitens South Africa P.W. Crous KF442710 KF442669 – – –
CBS 110903 Eucalyptus nitens South Africa P.W. Crous KF442711 KF442670 – – –
CBS 111268 Eucalyptus grandis Kenya M.J. Wingfield KF442712 KF442671 – – –
Pseudocercospora flavomarginata CBS 118824 Eucalyptus camaldulensis China M.J. Wingfield JX902010 JX901887 – – –
CBS 124990 Eucalyptus camaldulensis Thailand W. Himaman JX902028 JX901905 – – –
Pseudocercospora fori CBS 113285 Eucalyptus grandis South Africa G.C. Hunter KF442713 GU253824 – – –
CBS 113286 Eucalyptus sp. South Africa J. Roux KF442714 KF442672 – – –
Pseudocercospora gracilis CPC 11144 Eucalyptus sp. Indonesia M.J. Wingfield JX902011 JX901888 – – –
CPC 11181 Eucalyptus sp. Indonesia M.J. Wingfield JX902012 JX901889 – – –
CBS 111189 Eucalyptus urophylla – M.J. Wingfield JX902013 JX901890 – – –
Pseudocercospora humuli-japonici CPC 11315 Humulus japonicus South Korea H.D. Shin JX902014 JX901891 – – –
Pseudocercospora madagascariensis CBS 124155 Eucalyptus camaldulensis Madagascar M.J. Wingfield JX902016 JX901893 – – –
Pseudocercospora marginalis CBS 131582 Fraxinus rhynchophylla South Korea H.D. Shin KF442715 GU253812 – – –
Pseudocercospora natalensis CBS 111069 Eucalyptus nitens South Africa T. Coutinho KF442716 KF302405 – – –
Pseudocercospora norchiensis CBS 120738 Eucalyptus sp. Italy W. Gams JX902017 JX901894 – – –
Pseudocercospora paraguayensis CBS 111286 Eucalyptus nitens Brazil P.W. Crous JX902018 JX901895 – – –
Pseudocercospora pini-densiflorae CBS 125138 Pinus sp. Japan Sung-Oui Suh JX902021 JX901898 – – –
CBS 125140 Pinus kesiya Japan Sung-Oui Suh JX902020 JX901897 – – –
Pseudocercospora pistacina CPC 21874 Pistacia vera Turkey K. Sarpkaya KF442719 KF442675 KF442648 KF442734 KF442638
CPC 23117; 27NT080 Pistacia vera Turkey K. Sarpkaya KF442717 KF442673 KF442646 KF442732 KF442636
CPC 23118; 09mrk010 Pistacia vera Turkey K. Sarpkaya KF442718 KF442674 KF442647 KF442733 KF442637
CBS 135840; 45sln005 Pistacia vera Turkey K. Sarpkaya KF442720 KF442676 KF442649 KF442735 KF442639
CBS 135841; 63br043 Pistacia vera Turkey K. Sarpkaya KF442721 KF442677 KF442650 KF442736 KF442640
Pseudocercospora plechranti CPC 11462 Plectranthus South Korea H.D. Shin JX902015 JX901892 – – –
Pseudocercospora pyracanthigena CPC 10808 Pyracantha angustifolia South Korea H.D. Shin KF252323 KF251823 – – –
Pseudocercospora rhoina CPC 11464 Rhus chinensis South Korea H.D. Shin JX902026 JX901903 – – –
Pseudocercospora robusta CBS 111175 Eucalyptus robur Malaysia M.J. Wingfield JX902027 JX901904 – – –
Pseudocercospora sphaerulinae CBS 112621 Eucalyptus sp. – P.W. Crous JX902029 JX901906 – – –
Pseudocercospora subulata CBS 118489 Eucalyptus botryoides New Zealand M. Dick JX902030 JX901907 – – –
Pseudocercospora tereticornis CPC 13315 Eucalyptus nitens Australia P.W. Crous JX902032 JX901909 – – –
CBS 124996 Eucalyptus nitens Australia A.J. Carnegie JX902033 JX901910 – – –
Pseudocercospora vitis CPC 11595 Vitis vinifera South Korea H.D. Shin JX902035 JX901912 – – –
Ramulispora sorghi CBS 110578 Sorghum bicolor South Africa D. Nowell KF442722 KF442678 – – –
CBS 110579 Sorghum bicolor South Africa D. Nowell KF442723 KF442679 – – –
Septoria astragali CBS 109117 Astragalus glycyphyllos Austria G. Verkley KF252350 KF251853 – – –
CBS 123878 Astragalus glycyphyllos Czech Republic G. Verkley KF252351 KF251854 – – –
Septoria cytisi USO 378994 Laburnum anagyroides Czech Republic J. A. Baumler – JF700954 – – –
Septoria hibiscicola CBS 128611 Hibiscus syriacus South Korea H.D. Shin KF252430 KF251937 – – –
Septoria hippocastani CBS 411.61 Aesculus hippocastanum Germany W. Gerlach KF252432 KF251939 – – –
Septoria justiciae CBS 128610 Justica procumbens South Korea H.D. Shin KF252433 KF251940 – – –
Septoria lamiicola CBS 109113 lamium album Austria G. Verkley KF252443 KF251950 – – –
Septoria pistaciae CBS 420.51 Pistacia vera Italy G. Goidánich KF442724 KF252025 – – –
Septoria pistaciarum CPC 23116; 5DMR032 Pistacia vera Turkey K. Sarpkaya KF442725 KF442680 KF442651 KF442737 KF442635
CPC 23114; 003c Pistacia vera Turkey K. Sarpkaya KF442726 KF442681 KF442652 KF442738 KF442641
CPC 23115; 002B Pistacia terebinthus Turkey K. Sarpkaya KF442727 KF442682 KF442653 KF442739 KF442642
CBS 135838; 45sln034 Pistacia vera Turkey K. Sarpkaya KF442728 KF442683 KF442654 KF442740 KF442643
CBS 135839; 001A Pistacia vera Turkey K. Sarpkaya KF442729 KF442684 KF442655 KF442741 KF442644
Septoria protearum CBS 101013 Masdevallia sp. Netherlands W. Veenbaas-Rijks KF252504 KF252013 – – –
CBS 101354 Gevuina avellana New Zealand S. Ganev KF252505 KF252014 – – –
CBS 113392 Lobelia erinus – S. Wolcon KF252507 KF252016 – – –
CBS 410.61 Gerbera jamesonii Italy W. Gerlach KF252514 KF252024 – – –
CBS 566.88 Hedera helix France H.A. van der Aa KF252515 KF442693 – – –
Septoria rumicum CBS 503.76 Rumex acetosa France H. A. van der Aa KF252523 KF252034 – – –
Septoria stellariae CBS 102376 Stellaria media Netherlands G. Verkley KF252567 KF252079 – – –
CBS 102378 Castanea sativa Netherlands G. Verkley KF252568 KF252080 – – –
Sonderhenia eucalypticola CPC 11252 Eucalyptus globulus Spain M.J. Wingfield KF442730 KF442685 – – –
Sphaerulina betulae CBS 116724 Betula pubescens Scotland S. Green KF252595 KF252107 – – –
CBS 128600 Betula platyphylla South Korea H.D. Shin KF252598 KF252110 – – –
Sphaerulina musiva CBS 130559 Populus sp. Canada J. LeBoldus KF252611 KF252124 – – –
CBS 130562 Populus sp. Canada J. LeBoldus KF252612 KF252125 – – –
Sphaerulina quercicola CBS 109009 Quercus rubra Netherlands G. Verkley KF252619 KF252132 – – –
CBS 115016 Quercus robur Netherlands G. Verkley KF252620 KF252133 – – –
Zymoseptoria verkleyi CBS 133618 Poa annua Netherlands S.I.R. Videira KF442731 KF442686 – – –
Open in a new tab

1CBS: CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands; CPC: Culture collection of Pedro Crous, housed at CBS; USO: United States Department of Agriculture, National Fungus Collections (BPI)

2Btub: β-tubulin; EF-1α: Translation elongation factor 1-alpha; ITS: internal transcribed spacers and intervening 5.8S nrDNA; LSU: 28S large subunit of the nrRNA gene; RPB2: RNA polymerase II second largest subunit.

DNA isolation, amplification and analyses

Genomic DNA was extracted from fungal colonies growing on MEA using the UltraCleanTM Microbial DNA Isolation Kit (MoBio Laboratories, Solana Beach, CA, USA) according to the manufacturer’s protocol. The primers LSU1Fd (Crous et al. 2009a) and LR5 (Vilgalys & Hester 1990) were used to amplify the partial 28S rRNA gene (LSU), ITS5 and ITS4 (White et al. 1990) were used to amplify the ITS region T1 (O’Donnell & Cigelnik 1997) and b-Sandy-R (Stukenbrock et al. 2012) were used to amplify the partial β-tubulin locus (Btub), EF1-728F (Carbone & Kohn 1999) and EF-2 (O’Donnell et al. 1998) were used to amplify the partial translation elongation factor-1α locus (EF) and fRPB2-5F (Liu et al. 1999) and fRPB2-414R (Quaedvlieg et al. 2011) were used to amplify the partial RNA polymerase II second largest subunit locus (RPB2). A basic alignment of the obtained sequence data was first done using MAFFT v. 7 [(http://mafft.cbrc.jp/alignment/server/index.html) (Katoh et al. 2002)] and if necessary, manually improved in BioEdit v. 7.0.5.2 (Hall 1999). To check the congruency of the RPB2 and LSU datasets, a 70 % neighbour-joining (NJ) reciprocal bootstrap was performed (Mason-Gamer & Kellogg 1996, Lombard et al. 2010). A Bayesian analysis (critical value for the topological convergence diagnostic set to 0.01) was performed on the concatenated LSU/RPB2 loci using MrBayes v. 3.2.1 (Huelsenbeck & Ronquist 2001) as described by Crous et al. (2006) using nucleotide substitution models that were selected using MrModeltest v. 2.3 (Nylander 2004). Sequences derived from this study were lodged at GenBank, and the alignment was deposited in TreeBASE (www.treebase.org/treebase/index.html).

Morphology

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 Zen software. Colony characters and pigment production were noted after 2 wk of growth on MEA, PDA and OA incubated at 25 °C. Colony colours (surface and reverse) were rated according to the colour charts of Rayner (1970). Morphological descriptions were based on cultures sporulating on PDA, and taxonomic novelties and metadata were deposited in MycoBank (www.MycoBank.org; Crous et al. 2004).

RESULTS

The RPB2 and LSU sequence datasets did not show any conflicts in their tree topology for the 70 % reciprocal bootstrap trees, allowing us to combine them in the multigene analyses. The LSU sequence contained 745 base pairs, of which 99 where unique, the RPB2 sequence contained 317 base pairs, of which 157 where unique. For both datasets, the GTR-I-gamma substitution model (as calculated by MrModeltest) was used during the MrBayes run. During the generation of the tree (Fig. 1), a total of 7 216 trees were generated, and 5 412 (75 %) of them where sampled for the final tree

Fig. 1.

Fig. 1

Open in a new tab

A Bayesian 50 % majority rule RPB2/LSU consensus tree containing representative isolates belonging to Pseudocercospora and related genera (Mycosphaerellaceae). Bayesian posterior probabilities support values for the respective nodes are displayed in the tree. A stop rule (set to 0.01) for the critical value for the topological convergence diagnostic was used for the Bayesian analysis. The tree was rooted to Zymoseptoria verkleyi (CBS 133618). The scalebar indicates 0.1 expected changes per site.

TAXONOMY

Cylindroseptoria pistaciae Quaedvlieg et al., Stud. Mycol. 75: 359 (2013).

(Fig. 2)

Fig. 2.

Fig. 2

Open in a new tab

Cylindroseptoria pistaciae (CBS 471.69). A–B. Conidiomata sporulating in culture. C–D. Intercalary chains of chlamydospore-like cells. E–F. Conidiogenous cells. G–H. Conidia. Bars = 10 μm, H applies to C and D.

Description: Conidiomata pycnidial, erumpent, globose, black, separate, with a black crusty outer layer of cells, to 200 μm diam, with a central ostiole; wall of 3–6 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells. Conidiogenous cells phialidic (mostly monophialidic, but a few observed to also be polyphialidic), lining the inner cavity, hyaline, smooth, ampulliform, 5–8 × 3–4 μm, proliferating percurrently (inconspicuous) or with periclinal thickening at apex (also occurring as solitary loci on superficial hyphae surrounding pycnidia). Conidia hyaline, smooth, cylindrical, mostly straight, rarely slightly curved, apex subobtuse, base truncate, guttulate, aseptate, (9–)11–13(–18) × 2.5–3(–3.5) μm (from Quaedvlieg et al. 2013)

Culture characteristics: Colonies on PDA flat, circular, lacking aerial mycelium, surface fuscous-black, reverse olivaceous-black, after 14 d at 24 °C, 3.5 cm diam; on MEA surface fuscous-black, reverse olivaceous-black, after 14 d, 4.5 cm diam; on OA similar to PDA.

Type: Spain: Mallorca: El Arenal, on leaves of Pistacia lentiscus, 25 May 1969, H. A. van der Aa (CBS H-21301 – holotype; culture ex-type CBS 471.69).

Notes: Quaedvlieg et al. (2013) established the genus Cylindroseptoria for taxa having cupulate to pycnidial conidiomata, and phialidic conidiogenous cells with periclinal thickening, that give rise to cylindrical, aseptate conidia. Although Cylindroseptoria pistaciae was introduced as a novel species (from symptomatic leaves of Pistacia lentiscus), no information is available about its potential role as plant pathogen.

Pseudocercospora pistacina (Allesch.) Crous, Quaedvlieg & Sarpkaya, comb. nov.

Basionym: Septoria pistacina Allesch., Rabenh. Krypt.-Fl. 1(6): 830 (1900) [“1899”].

Synonyms: Dothidea pistaciae Lév., in Démidoff, Voy. Russ. Mér. 2: 108 (1842).

Non Pseudocercospora pistaciae (Chupp) Crous & U. Braun, Mycotaxon 78: 338 (2001).

Septoria pistaciae (Lév.) Cooke, Grevillea 13 (66): 45 (1884); nom. illegit., non S. pistaciae Desm. 1842.

Mycosphaerella pistacina Chitzan., Ann. Inst. Phytopath. Benaki 10: 42 (1956).

MycoBank MB805893

(Fig. 3)

Fig. 3.

Fig. 3

Open in a new tab

Pseudocercospora pistacina (CBS 135840). A. Fruit tree orchard. B–C. Leaf spots. D. Disease symptoms on fruit. E. Conidia cirrhi oozing from immersed pycnidial conidiomata. F–G. Vertical section through pycnidia. H. Conidiogenous cells giving rise to conidia. I. Conidia. Bars: F = 300 μm, G = 150 μm, H–I = 10 μm.

Description: Leaf spots numerous, brown, amphigenous, angular, confined by leaf veins, to 30 mm long, 3–6 mm diam, containing numerous small, aggregated, immersed conidiomata. Fruit spots grey to pale brown, 1–4 mm diam, coalescing to form larger spots, surrounded by a distinct, reddish margin. Conidiomata subepidermal, globose to depressed, to 300 μm diam with a wide central ostiole, to 100 μm diam; wall 10–20 μm thick, of 3–6 layers of brown textura angularis. Conidiophores subcylindrical, pale brown, smooth, 0–3-septate, branched or not, 10–30 × 3–5 μm. Conidiogenous cells terminal and sublateral, pale brown, smooth, subcylindrical to doliiform, 6–15 × 2.5–4 μm; proliferating several times percurrently at the apex. Conidia pale brown, smooth, guttulate, subcylindrical, curved, medianly 1-septate, constricted at the septum, apex obtuse, tapering at the base to a truncate hilum, 1.5–2 μm diam, (32–) 35–42(–50) × (3–)3.5–4(–5) μm.

Chitzanidis (1956) reports ascomata as 90–110 × 80–110 μm, asci as 44.5–54.5 × 13–14.5 μm, and ascospores as 26–40 × 3–5 μm.

Culture characteristics: Colonies after 2 wk at 24 °C reaching 10 mm diam, erumpent with sparse aerial mycelium and even, lobate margins; on OA, MEA and PDA dirty white, remaining sterile; in reverse iron-grey.

Specimens examined: Turkey: Manisa: Selendi, on Pistachio vera, 2010, K. Sarpkaya (CPC 45sln005 = CBS 135840). Gaziantep: Nizip, on P. vera, 2010, K. Sarpkaya (CPC 27NZ080 = CPC 23117). Sanliurfa: Birecik, on P. vera, 2010, K. Sarpkaya (CPC 63br043 = CBS 135841). Aydin: Merkez, on P. vera, 2010, K. Sarpkaya (CPC 09mrk010 = CPC 23118); collection site unknown, on P. vera, 2010, K. Sarpkaya (CPC 21874).

Notes: Because of the pycnidial conidiomata and pigmented conidia, Pseudocercospora pistacina can be confused with Phaeophloeospora or Kirramyces (syn. Teratosphaeria; Crous et al. 2009a, b), though it is phylogenetically unrelated to these genera. Pseudocercospora pistacina clusters basally within Pseudocercospora, but based on the genes studied here, could not be recognised as a separate genus. The genus Pseudocercospora was recently circumscribed as having species with conidiophores that are solitary, fasciculate, synnematal, or arranged in sporodochia, giving rise to conidia that are pigmented, have unthickened or slightly thickened and darkened scars (Crous et al. 2013a). By including Septoria pistacina in Pseudocercospora, we are expanding the generic circumscription of the latter to also include taxa with well-defined pycnidial conidiomata (on host and in culture). Conidiomatal structure has to date been paramount in identifying taxa with enclosed conidiomata (Sutton 1980, Nag Raj 1993), and thus P. pistacina is rather atypical within Pseudocercospora s. str.

Septoria pistaciae Desm., Annls Sci. Nat., Bot., sér. 2 17: 112 (1842).

Synonyms: Phloeospora pistaciae (Desm.) Petr., Annls mycol. 20: 18 (1922).

Cylindrosporium pistaciae (Desm.) Vassil., Fungi Imp. Paras. 2: 510 (1950).

(Fig. 4)

Fig. 4.

Fig. 4

Open in a new tab

Septoria pistaciae (PC 0142143). A. Herbarium specimen. B–F. Conidiogenous cells giving rise to conidia. G. Conidia. Bars = 10 μm, D applies to E–G.

Description: Leaf spots initially small, orbicular or oblong, scattered, brown to dark brown, 1–2 mm diam, becoming irregular, 5–10 mm, covering large portions of leaf, becoming greyish brown with distinct, narrow brown margin. Conidiomata pycnidial, amphigenous, separate or densely aggregated in the centre of leaf spots, immersed, becoming erumpent, brown to dark brown, globose to pyriform, (40–) 70–90(–120) μm diam, with central ostiole, 15–20 μm diam; wall of 3–4 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells, or up to 4-septate, subcylindrical with lateral and terminal conidiogenous cells, 5–25 × 3–4 μm. Conidiogenous cells hyaline, smooth, ampulliform to subcylindrical, 5–10 × 3–4 μm, lining inner layer of conidiomatal cavity, proliferating sympodially, rarely percurrently. Conidia hyaline, smooth, 0–3-septate, (9–)13–22(–25) × (1.5–)2(–3) μm, obclavate to narrowly subcylindrical, apex subobtuse, base obconically truncate with flattened scar. Spermatial state occurring in conidiomata along with conidia. Spermatogenous cells hyaline, smooth, ampulliform, 4–6 × 3–5 μm. Spermatia hyaline, smooth, ellipsoid to subcylindrical, with obtuse ends, 2.5–3.5 × 1.5 μm.

Culture characteristics: Colonies after 2 wk at 25 °C reaching 40 mm diam on OA; surface sienna, smooth, with even margins, lacking aerial mycelium; culture sterile on OA, PDA, MEA and on barley leaves placed on synthetic nutrient-poor agar (Crous et al. 2009c).

Specimens examined: France: on leaves of Pistacia vera, 1842, Desmazière [Pl. Crypt. Nord Fr., fasc. 24, no. 1181] (PC0142144 – holotype; authentic specimen from general herbarium (PC) no. 1181, PC0142143). – Italy: on leaves of P. vera, June 1951, G. Goidánich (CBS 420.51; culture sterile).

Notes: Septoria pistaciae is part of the species complex for which Verkley et al. (2013) adopted the oldest name, S. protearum, which has an ex-type culture. Isolates in this complex could not be robustly distinguished based on a seven-gene phylogeny, and represent collections with a range of hosts covering six different plant families. Whether this is one plurivorous taxon that can undergo host jumping (Crous & Groenewald 2005), or several closely related taxa that cannot be distinguished based on the set of genes employed by Verkley et al. (2013), awaits further study and inoculation trials.

Andrianova & Minter (2004) described conidia of S. pistaciae as 1–3-septate, (20–)22–25(–34) × 1.5(–2) μm, obclavate to narrowly subcylindrical (based on type material, LE 42353). Our measurements from type material are considerably smaller, namely 0–3-septate, (9–)13–22(–25) × (1.5–)2(–3) μm (PC 0142144). Type material of S. protearum has conidia that are (0–)1–3(–4)-septate, (6–)12–22(–30) × 1.5–2 μm, obclavate to narrowly subcylindrical (Swart et al. 1998, Crous et al. 2013b). If these two taxa are eventually shown to be synonymous, the name S. pistaciae (1842) predates that of S. protearum (1998), but even that may not be the oldest epithet for this taxon. The single isolate available to us for study (CBS 420.51) proved to be sterile, so its morphology could not be confirmed.

Septoria pistaciarum Caracc., Boll. Stud. Inform. R. Giard Colon Palermo 13: 10 [extr.] (1934).

Synonym: Mycosphaerella pistaciarum Chitzan., Ann. Inst. Phytopath. Benaki 10: 42 (1956).

(Fig. 5)

Fig. 5.

Fig. 5

Open in a new tab

Septoria pistaciarum (CBS 135838). A. Colony sporulating on SNA with sterile barley leaves. B. Colony on OA. C–E. Conidiogenous cells giving rise to conidia. F–G. Conidia. Bars: A–B = 200 μm, C, F–G = 10 μm, C applies to D and E.

Description: Leaf spots angular, brown, amphigenous, 1–2 mm diam, coalescing to become larger leaf spots, confined by leaf veins. Conidiomata pycnidial, erumpent, brown, globose, to 200 μm diam, with central ostiole, exuding a crystalline cirrhus of conidia; wall of 3–6 layers of brown textura angularis. Conidiophores reduced to conidiogenous cells, or one supporting cell which can be branched at the base. Conidiogenous cells lining the inner cavity, hyaline, smooth, subcylindrical to ampulliform or doliiform, 5–15 × 2.5–4 μm, proliferating percurrently near apex, or sympodially. Conidia solitary, hyaline, smooth, guttulate, straight to curved, narrowly obclavate to subcylindrical, (1–)3-septate, apex subobtuse, base obconically truncate, 2 μm diam with minute marginal frill, (45–)55–65(–75) × (2.5–)3(–3.5) μm.

Chitzanidis (1956) reports ascomata as 95–130 × 85–120 μm, asci 47.5–60.5 × 8–12 μm, and ascospores 18–30 × 3–5 μm.

Culture characteristics: Colonies after 2 wk at 24 °C reaching 30 mm diam. Colonies erumpent, folded with feathery, lobate margins. On PDA surface olivaceous grey with patches of pale olivaceous grey and dirty white, reverse olivaceous grey. On OA surface greyish sepia with patches of dirty white, and an umber pigment diffusing into agar. On MEA surface pale olivaceous grey with patches of dirty white; olivaceous grey in reverse.

Specimens examined: Turkey: Hatay: Merkez, on Pistacia terebinthus, 2012, K. Sarpkaya (CPC 002B = CPC 23115). Sakarya: Geyve, on P. vera, 2012, K. Sarpkaya (CPC 003C = CPC 23114). Kutahya: Emet, on P. vera, 2012, K. Sarpkaya (CPC 001A = CBS 135839). Manisa: Selendi, on P. vera, 2012, K. Sarpkaya (CPC 45sln034 = CBS 135838); Demirci, on P. vera, 2012, K. Sarpkaya (CPC 5DMR032 = CPC 23116).

Notes: Septoria pistaciarum is morphologically distinct from the other species occurring on pistachio, in having much larger conidia (45–75 × 2.5–3.5 μm). In the field it can also be disnguished on diseased host plants in causing more angular leaf spots, confined by leaf veins.

DISCUSSION

The aim of the present study was to clarify which species of Septoria occur on pistachio, and to place them in a phylogenetic context within Mycosphaerellaceae, as recently circumscribed (Quaedvlieg et al. 2013, Verkley et al. 2013). From results obtained, it is clear that up to four septoria-like taxa occur on pistachio, of which two belong to other genera, namely Cylindroseptoria pistaciae and Pseudocercospora pistacina. The remaining two species represent true species of Septoria, namely S. pistaciae and S. pistaciarum. Because of discrepancies in previously published literature, much confusion arose regarding how to distinguish these taxa. In the present study we have been able to compile a key to facilitate identification of these taxa (see below). Sexual morphs have also been described for two of these taxa, namely Septoria pistacina (i.e. Mycosphaerella pistacina) and Septoria pistaciarum (i.e. Mycosphaerella pistaciarum) (Chitzanidis 1956, Teviotdale et al. 2001). However, because the genus Mycosphaerella is restricted to Ramularia (Verkley et al. 2004, Crous et al. 2009a, b, Koike et al. 2011), in moving towards a single nomenclature for fungi (see Hawksworth et al. 2011, Wingfield et al. 2012), the use of Mycosphaerella should be avoided for the mycosphaerella-like sexual morphs linked to Septoria.

The placement of Septoria pistacina in Pseudocercospora is somewhat controvertial, as it has a typical pycnidial conidioma, rather than superficial fascicles or synnemata encountered in Pseudocercospora. Phylogenetically, however, there is no support for recognising S. pistacina as a separate genus based on it being a “pigmented Septoria”. Morphologically, the conidiogenous cells and conidia fit the circumscription of Pseudocercospora, but the conidiomatal anatomy does not. Although species of Capnodiales are known to have synasexual morphs with closed and open conidiomata (Crous et al. 2007, 2009a, b), this is the first example of a taxon with a pycnidial conidioma that clusters among species with fasciculate conidiomata. In addition to S. pistacina, we are also aware of a second as yet undescribed species of “pigmented Septoria” (Crous et al., unpubl.), which again clusters in Pallidocercospora (Crous et al. 2013a). Another example of a genus reported to have acervuli, but observed to have superficial conidiomatal fascicles, is Ciferiella, which has also been reduced to synonymy with Pseudocercospora (Quaedvlieg et al. 2013). These findings support the view that conidiomatal morphology in Pseudocercospora is a continuum from sporulating superficially (fascicles, synnemata, sporodochia), via acervuli, to sporulation in an enclosed structure (pycnidia).

In spite of being morphologically distinct, that two of the reported septoria-like taxa on pistachio represent different genera is rather suprising. Although the pathological relevance of Pseudocercospora pistacina (as S. pistacina), S. pistaciae, and S. pistaciarum on Pistacia vera is well-documented (Michailides 2005), nothing is known about that of Cylindroseptoria pistaciae, other than it was associated with leaf spots of Pistacia lentiscus in Spain. Furthermore, it also appears that the importance of certain diseases of pistachio differs between regions or countries. Approximately 85 % of the world’s pistachio production presently comes from Iran, the USA, and Turkey (http://faostat.fao.org/site/339/default.aspx). However, pistachio is irrigated in Iran and the USA, where more rounded fruit bearing cultivars are grown. In contrast, irrigation is not practiced in Turkey, and more elongated fruit cultivars are commonly grown there. These differences in cultivation practices also lead to differences in phytopatological problems. In the USA, the main pathogens are reported to be Botryosphaeria dothidea, Botrytis cinerea, and Alternaria alternata. In Turkey, however, Pseudocercospora pistacina is the most common disease of pistachio (Dinç 1983, Michailides et al. 1995), leading to reports of 3–100 % yield loss in epidemic years by this pathogen (Dinç et al. 1979).

Key to septoria-like species occurring on pistachio

  • 1

    Conidia aseptate, 9–18 × 2.5–3.5 μm .................... Cylindroseptoria pistaciae

    Conidia septate .................... 2

  • 2(1)

    Conidia pale brown, medianly 1-septate, 32–50 × 3–5 μm .................... Pseudocercospora pistacina

    Conidia hyaline, 1–3-septate ..................... 3

  • 3(2)

    Conidia 9–34 × 1.5–3 μm .................... Septoria pistaciae

    Conidia 45–75 × 2.5–3.5 μm .................... Septoria pistaciarum

Acknowledgments

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.

REFERENCES

  1. Aghajani MA, Aghapour B, Michailides TJ. (2009) First report of Septoria leaf spot of pistachio in Iran. Australasian Plant Disease Notes 4: 29–31 [Google Scholar]
  2. Allescher A. (1901) Fungi Imperfecti: Hyalin-sporige Sphaerioideen. Dr L. Rabenhorst’s Kryptogamen-Flora von Deutschland, Oestereich und der Schweiz 1(6): 961–1016 [Google Scholar]
  3. Andrianova TV, Minter DW. (2004) Septoria pistaciae. IMI Descrpitions of Fungi and Bacteria 1586: 1–2 [Google Scholar]
  4. Bremer H, Karel G, Bıyıkoğlu K, Göksel N, Petrak F. (1952) Beiträge zur Kenntnis der parasitischen Pilze der Türkei. VI. Revue de la Faculté des Sciences de l’Université d’Istanbul, Série B, 17: 260–261 [Google Scholar]
  5. Bremer H. (1954) Bahçe Kültürleri Hastalıkları. Türkiye Fitopatolojisi 295: 109–110 [Google Scholar]
  6. Caracciolo F. (1934) Una grave septoriosi del pistacchio. Bolle Di Studi ed Informazione del R. Giardino di Palermo 13: 66–73 [Google Scholar]
  7. Carbone I, Kohn LM. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556 [Google Scholar]
  8. Chitzanidis A. (1956) Species of Septoria on the leaves of Pistacia vera and their perfect states. Annales de l’Institut Phytopathologique Benaki 10: 29–44 [Google Scholar]
  9. Cooke MC. (1884) Synopsis Pyrenomycetum (continued). Grevillea 13: 41–45 [Google Scholar]
  10. Crous PW, Braun U, Groenewald JZ. (2007) Mycosphaerella is polyphyletic. Studies in Mycology 58: 1–32 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crous PW, Braun U, Hunter GC, Wingfield MJ, Verkley GJM, Shin H-D, Nakashima C, Groenewald JZ. (2013a) Phylogenetic lineages in Pseudocercospora. Studies in Mycology 75: 37–114 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Crous PW, Denman S, Taylor JE, Swart L, Bezuidenhout CM, Hoffman L, Palm ME, Groenewald JZ. (2013b) Cultivation and diseases of Proteaceae: Leucadendron, Leucospermum and Protea. 2nd edn [CBS Biodiversity Series no. 13.] Utrecht: CBS-KNAW Fungal Biodiversity Centre [Google Scholar]
  13. Crous PW, Gams W, Stalpers JA, Robert V, Stegehuis G. (2004) MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology 50: 19–22 [Google Scholar]
  14. Crous PW, Groenewald JZ. (2005) Hosts, species and genotypes: opinions versus data. Australasian Plant Pathology 34: 463–470 [Google Scholar]
  15. Crous PW, Schoch CL, Hyde KD, Wood AR, Gueidan C, et al. (2009a) Phylogenetic lineages in the Capnodiales. Studies in Mycology 64: 17–47 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, et al. (2006) Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55: 235–253 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Hunter GC, et al. (2009b) Unravelling Mycosphaerella: do you believe in genera? Persoonia 23: 99–118 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Crous PW, Verkley GJM, Groenewald JZ, Samson RA. (eds) (2009c) Fungal Biodiversity. [CBS Laboratory Manual Series no.1.]. Utrecht: CBS-KNAW Fungal Biodiversity Centre [Google Scholar]
  19. Crous PW, Wingfield MJ, Park RF. (1991) Mycosphaerella nubilosa a synonym of M. molleriana. Mycological Research 95: 628–632 [Google Scholar]
  20. Desmaziéres JB. (1842) Neuviéme notice sur quelques plantes cryptogames. Annales des Sciences Naturelles, Botanique, série 2 17: 91–118 [Google Scholar]
  21. Dinç N. (1983) Antepfıstığı Hastalıkları ve Mücadele Usulleri. Mesleki Eserler Serisi 2: 19–34 [Google Scholar]
  22. Dinç N, Göksedef O, Turan K. (1979) Gaziantep ili antepfıstıklarında zarar yapan Karazenk hastalığı (Septoria pistacina All.) nın Bio-ekolojisi ve korunma olanakları üzerine araştırmalar. Bitki Koruma Bülteni 19: 16–38 [Google Scholar]
  23. Dudka IO, Heluta VP, Tykhonenko YY, Andrianova TV, Hayova VP, et al. (2004) Fungi of the Crimean Peninsula. Kiev: M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine [Google Scholar]
  24. Haggag WM, Abou Rayya MSM, Kasim NE. (2006) First report of Septoria pistaciae causing leaf spot of pistachio in Egypt. Plant Disease 90: 1553. [DOI] [PubMed] [Google Scholar]
  25. Hall TA. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98 [Google Scholar]
  26. Hawksworth DL, Crous PW, Redhead SA, Reynolds DR, Samson RA, et al. (2011) The Amsterdam Declaration on Fungal Nomenclature. IMA Fungus 2: 105–112 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hoog GS de, Gerrits van den Ende AHG. (1998) Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41: 183–189 [DOI] [PubMed] [Google Scholar]
  28. Huelsenbeck JP, Ronquist F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755 [DOI] [PubMed] [Google Scholar]
  29. Katoh K, Misawa K, Kuma K, Miyata T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059–3066 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Koike SK, Baameur A, Groenewald JZ, Crous PW. (2011). Cercosporoid leaf pathogens from whorled milkweed and spineless safflower in California. IMA Fungus 2: 7–12 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lombard L, Crous PW, Wingfield BD, Wingfield MJ. (2010) Species concepts in Calonectria (Cylindrocladium). Studies in Mycology 66: 1–13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Leveillé JH. (1842) Obsérvations médicales et énumérations des plantes récueillies en Tauride. In: Voyage dans la Russie meridionale et la Crimée (Démidoff A, ed.) 2: 80–135 Paris: Ernes Boudier [Google Scholar]
  33. Liu Y, Whelen S, Hall B. (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biology and Evolution 16: 1799–1808 [DOI] [PubMed] [Google Scholar]
  34. Mason-Gamer RJ, Kellogg EA. (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Systematic Biology 45: 524–545 [Google Scholar]
  35. Michailides TJ. (2005) Pest, disease, and physiological disorders management: above ground fungal diseases. In: Pistachio Production Manual (Beede RH, Freeman MW, Haviland DR, Holtz BA, Kallsen CE, eds): 214–232 Davis, CA: Fruit and Nut Research and Information Center, Department of Plant Sciences, University of California Davis [Google Scholar]
  36. Michailides TJ, Morgan DP, Doster MA. (1995) Diseases of pistachio in California and their significance. Acta Horticulturae 419: 337–343 [Google Scholar]
  37. Nag Raj TR. (1993) Coelomycetous anamorphs with appendage-bearing conidia. Waterloo, ON: Mycologue Publications [Google Scholar]
  38. Nylander JAA. (2004) MrModeltest. Version 2. Uppsala: Distributed by the author. Evolutionary Biology Centre, Uppsala University [Google Scholar]
  39. O’Donnell K, Cigelnik E. (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution 7: 103–116 [DOI] [PubMed] [Google Scholar]
  40. O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC. (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proceedings of the National Academy of Sciences, USA 95: 2044–2049 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pantidou ML. (1973) Fungus-Host Index for Greece. Athens: Benaki Phytopathological Institute [Google Scholar]
  42. Parfitt DE, Badenes ML. (1997) Phylogeny of the genus Pistacia as determined from analysis of the chloroplast genome. Proceedings of the National Academy of Sciences, USA 94: 7987–7992 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, Razavi M, Gohari AM, Mehrabi R, Crous PW. (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26: 57–69 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Quaedvlieg W, Verkley GJM, Shin H-D, Barreto RW, Alfenas AC, et al. (2013) Sizing up Septoria. Studies in Mycology 75: 307–390 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Rayner RW. (1970) A Mycological Colour Chart. Kew: Commonwealth Mycological Institute [Google Scholar]
  46. Stukenbrock EH, Quaedvlieg W, Javan-Nikhah M, Zala M, Crous PW, McDonald BA. (2012) Zymoseptoria ardabilia and Z. pseudotritici, two progenitor species of the septoria tritici leaf blotch fungus Z. tritici (synonym: Mycosphaerella graminicola). Mycologia 104: 1397–1407 [DOI] [PubMed] [Google Scholar]
  47. Sutton BC. (1980) The Coelomycetes: fungi imperfecti with pycnidia, acervuli, and stromata. Kew: Commonwealth Mycological Institute [Google Scholar]
  48. Swart L, Crous PW, Denman S, Palm ME. (1998) Fungi occurring on Proteaceae. I. South African Journal of Botany 64: 137–145 [Google Scholar]
  49. Teviotdale BL, Michailides TJ, MacDonald J. (2001) Diseases of Pistachio (Pistacia vera L.). Common Names of Plant Diseases. St Paul, MN: American Phytopathological Society Press [Google Scholar]
  50. Tous J, Ferguson L. (1996) Mediterranean fruits. In: Progress in New Crops (Janick J. ed.): 416–430 Arlington, VA: American Society for Horticultural Science Press [Google Scholar]
  51. Vassiljevsky NI, Karakulin BP. (1950) Parazitnye Nesovershennye Griby. Vol. 2. Melanconiales. Moscow: Izdatel’stvo, AN SSSR [Google Scholar]
  52. Verkley GJM, Crous PW, Groenewald JZ, Braun U, Aptroot A. (2004) Mycosphaerella punctiformis revisited: morphology, phylogeny, and epitypification of the type species of the genus Mycosphaerella (Dothideales, Ascomycota). Mycological Research 108: 1271–1282 [DOI] [PubMed] [Google Scholar]
  53. Verkley GJM, Quaedvlieg W, Shin HD, Crous PW. (2013) A new approach to species delimitation in Septoria. Studies in Mycology 75: 213–305 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Vilgalys R, Hester M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. White TJ, Bruns T, Lee J, Taylor SB. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ. eds): 315–322 San Diego: Academic Press [Google Scholar]
  56. Wingfield MJ, De Beer ZW, Slippers B, Wingfield BD, Groenewald JZ, et al. (2012) One fungus, one name promotes progressive plant pathology. Molecular Plant Pathology 13: 604–613 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Young DJ, Michailides TJ. (1989) First report of Septoria leaf spot of pistachio in Arizona. Plant Disease 73: 775 [Google Scholar]

Articles from IMA Fungus are provided here courtesy of The International Mycological Association

RESOURCES