Skip to main content
NCBI home page
Fungal Systematics and Evolution logoLink to Fungal Systematics and Evolution
. 2018 Mar 26;1:131–140. doi: 10.3114/fuse.2018.01.06

Neocosmospora perseae sp. nov., causing trunk cankers on avocado in Italy

V Guarnaccia 1, M Sandoval-Denis 1,,2, D Aiello 3, G Polizzi 3, PW Crous 1
PMCID: PMC7259237  PMID: 32490364

Abstract

Trunk and branch cankers are among the most important diseases compromising avocado production worldwide. A novel species, Neocosmospora perseae sp. nov. is described isolated from trunk lesions on Persea americana in the main avocado producing area of Sicily, Italy. The new species is characterised using a polyphasic approach including morphological characters and a multilocus molecular phylogenetic analysis based on partial sequences of the translation elongation factor-1α, the internal transcribed spacer regions plus the large subunit of the rDNA cistron, and the RNA polymerase II second largest subunit. Pathogenicity tests and the fulfilment of Koch’s postulates confirm N. perseae as a novel canker pathogen of Persea americana.

Keywords: canker, morphology, multigene phylogeny, pathogenicity, one new taxon

INTRODUCTION

Fusaria are omnipresent fungi belonging to Nectriaceae, commonly found in soil, water, air, dead or living plant material, food, and many other substrates, where they are acting mainly as saprobes (Lombard et al. 2015). Nevertheless, some species are of great importance as mycotoxin producers which can affect human and animal health. The genus Fusarium sensu lato has recently been segregated into several fusarium-like genera, i.e. Albonectria, Bisifusarium, Cyanonectria, Geejayessia, Neocosmospora and Rectifusarium (Gräfenhan et al. 2011, Lombard et al. 2015). These taxa are among the most impactful human, animal and plant pathogens, affecting an extensive variety of hosts (O’Donnell et al. 2008, 2010, Lombard et al. 2015).

The agri-food production sector has been undergoing major changes over the last few decades in Italy. These changes especially concern the introduction of alternative crops such as avocado. In the 20th century, avocado (Persea americana) was introduced to Italy and cultivated for ornamental purposes. However, due to a decline in demand for lemon, and a global increasing demand for avocado, it took the place of lemon orchards in eastern Sicily, where it represents an important fruit industry and a viable alternative crop to citrus (Guarnaccia et al. 2016). Unfortunately, avocado production is compromised by several pathogens causing branch cankers (Menge & Ploetz 2003, Guarnaccia et al. 2016). Frost or mechanical injuries such as pruning wounds may represent the initial access wounds for these canker-causing pathogens. Moreover, species belonging to Nectriaceae are well-known as responsible for diseases on avocado plants (Vitale et al. 2012, Parkinson et al. 2017), including several members of Fusarium and fusarium-like genera, such as Albonectria and Neocosmospora (Farr & Rossman 2018).

In one of the most renowned cases, damage was inflicted to avocado trees in Israel in 2009, caused by the ambrosia beetle Euwallacea fornicatus, and a vectored symbiotic fungal species belonging to Neocosmospora (formerly the Fusarium solani species complex, FSSC; O’Donnell et al. 2008, Lombard et al. 2015, Aoki et al. 2018). The affected plants showed dieback, wilt, including sugar or gum exudates, and ultimately host tree mortality (Mendel et al. 2012). In 2012, the beetle was recorded on several tree species in southern California and Israel, playing a major role as serious threat to avocado production (Mendel et al. 2012, Freeman et al. 2013, Kasson et al. 2013). “Fusarium” euwallaceae, found associated with the beetle is closely related to Neocosmospora ambrosia, another obligate symbiont occurring in Sri Lanka and India causing damage to tea plantations (Lombard et al. 2015). Both fungal pathogens are nested in an exclusive lineage (the Ambrosia clade) within Clade 3 of Neocosmospora, together with at least another eight unnamed phylogenetic species, all symbionts of the fungus-farming Euwallacea ambrosia beetles and one of the best examples of host-fungus co-evolution (Freeman et al. 2013, O’Donnell et al. 2016, Aoki et al. 2018). The fulfilment of Koch’s postulates (Mendel et al. 2012) demonstrated the ability of ”Fusarium” euwallaceae to cause wilt and dieback on avocado in Israel and California with no beetle-association (Freeman et al. 2013).

After the observation of prominent trunk cankers on avocado trees in an orchard located in the Catania province (eastern Sicily) during 2015, efforts were made to identify the causal agent.

In this study, a new fungal pathogen of avocado belonging to the genus Neocosmospora is proposed. The fungus is described on the basis of morphological and cultural characteristics as well as phylogenetic analyses of combined DNA sequences. Moreover, the pathogenicity on the host from which the fungus was isolated, is evaluated.

MATERIALS AND METHODS

Field sampling and isolation

During 2015, trunk canker symptoms were observed in a 14-yr-old avocado (Hass cultivar) orchard, located in the avocado plant-production region in eastern Sicily. The disease incidence (DI) was recorded based on the number of symptomatic plants compared to the total number present. Branch canker samples were taken from 10 plants. Fragments (5 × 5 mm) of symptomatic tissues were cut from the lesion margins, surface-sterilised in a sodium hypochlorite solution (10 %) for 20 s, followed by 70 % ethanol for 30 s, and rinsed three times in sterilised water. Tissue fragments were dried between sterilised filter papers, placed on 2 % potato dextrose agar (PDA; Difco, Leeuwarden, The Netherlands) amended with 100 μg/mL penicillin and 100 μg/mL streptomycin (PDA-PS) and incubated at 25 °C until characteristic fungal colonies were observed. Pure cultures were obtained by transferring germinating single conidia to fresh PDA plates with the aid of a Nikon SMZ1000 dissecting microscope.

Fungal isolates and morphological characterization

The cultural and micromorphological features of all the isolates included in this study were evaluated following the procedures of Aoki et al. (2003) with some modification as described previously (Sandoval-Denis et al. 2018). Colour notation followed the mycological colour charts of Rayner (1970). Micromorphological characteristics were examined and photographed using a Nikon Eclipse 80i microscope with Differential Interference Contrast (DIC) optics and a Nikon AZ100 stereomicroscope, both equipped with a Nikon DS-Ri2 high definition colour digital camera. Photographs and measurements were taken using the Nikon software NIS-elements D software v. 4.50.

DNA extraction, PCR amplification and sequencing

Fungal isolates were grown on PDA for 4–7 d at room temperature, under a natural day/night photoperiod. Total genomic DNA was extracted from fresh mycelium scraped from the colony surface using the Wizard® Genomic DNA purification Kit (Promega Corporation, Madison, WI, USA). Fragments of four nuclear loci including the translation elongation factor 1-alpha (EF-1α), the internal transcribed spacer region of the rDNA (ITS), the large subunit of the rDNA (LSU) and the RNA polymerase second largest subunit (RPB2) were PCR amplified as described previously (O’Donnell et al. 2009, 2010, Sandoval-Denis et al. 2018) and sequenced using the following primer pairs: EF-1/EF-2 for EF-1α (O’Donnell et al. 2008), ITS4/ITS5 for ITS (White et al. 1990), LR0R/LR5 for LSU (Vilgalys & Hester 1990, Vilgalys & Sun 1994) and 5f2/7cr and 7cf/11ar for RPB2 (Liu et al. 1999, Sung et al. 2007). Sequences generated in this study were uploaded to GenBank and the European Nucleotide Archive (ENA) databases (Table 1).

Phylogenetic analyses and molecular identification

Sequence alignments were performed individually for each locus using MAFFT on the European Bioinformatics Institute (EMBL-EBI) portal (http://www.ebi.ac.uk/Tools/msa/mafft/). BLASTn searches on GenBank and pairwise sequence alignments on the Fusarium MLST database of the Westerdijk Fungal Biodiversity Institute (http://www.westerdijkinstitute.nl/fusarium/) were performed using EF-1α and RPB2 sequences in order to preliminary identify the fungal isolates to generic level. Following this initial identification, a combination of DNA sequences from four loci (EF-1α, ITS, LSU and RPB2) was used for the final molecular identification and phylogenetic analyses (O’Donnell et al. 2008).

The different gene datasets were analysed independently and combined using RAxML (ML) and Bayesian methods (BI) as described previously (Sandoval-Denis et al. 2018). Evolutionary models for the four loci (GTR+I+G for ITS, LSU and RPB2; GTR+G for EF-1α) were calculated using MrModelTest v. 2.3 (Nylander 2004) selecting the best-fit model for each data partition according to the Akaike criterion.

Pathogenicity tests

Pathogenicity tests were performed on potted, healthy avocado seedlings (6-mo-old) with a subset of two representative isolates. Each experiment was conducted twice. For each experiment three replicates per isolate were used with 10 plants per replicate. Twigs were superficially wounded between two nodes forming a slit using a sterile blade. Inoculations were conducted by placing a 1-wk-old, 6-mm-diam colonised agar plug from each fungal isolate on a wound. Wounds were then wrapped with Parafilm® (American National Can, Chicago, IL, USA). Ten twigs were inoculated as described above with 6-mm-diam non-colonised MEA plugs as negative controls. The same number of wounds/plants were inoculated with sterile MEA plugs and served as controls. After inoculation, plants were covered with a plastic bag for 48 h and maintained at 25 ± 1 °C and 95 % relative humidity (RH) under a 12-h fluorescent light/dark regime. All plants were irrigated 2–3 times per week and examined weekly for disease symptom development. Disease incidence (DI) was recorded as described above.

RESULTS

Field sampling and fungal isolation

Symptoms referable to fusaria species were detected in an avocado orchard in the main avocado-producing region of Eastern Sicily, Italy (GPS coordinates: 37.687247, 15.175479). The disease was observed on established plants (14-yr-old) in an open field. Disease incidence was ascertained at 10 %. The symptoms observed on avocado plants consisted of trunk cankers. Bark appeared cracked, darkly discoloured and/or slightly sunken. Occasionally, a sugar exudate was present on the surface. Cankers were internally reddish brown in colour and variable in shape. Transverse cuts revealed a characteristic wedge-shaped canker extending deep into the xylem (Fig. 1). Only fusarium-like isolates growing in pure culture were obtained from the symptomatic avocado trees, from which five monosporic strains were retained.

Fig. 1.

Fig. 1.

Open in a new tab

Natural and artificial symptoms referable to Neocosmospora perseae. A, B. Sugar exudation from avocado trunk cankers. C, D. External and internal canker caused by N. perseae inoculation.

Phylogenetic analyses and species identification

Pairwise sequence alignments on the Fusarium MLST database and GenBank BLASTn searches demonstrated that the five fungal isolates belonged to the genus Neocosmospora.

Subsequently, more inclusive multilocus phylogenetic analyses were performed based on EF-1α, ITS, LSU, and RPB2 sequences. A first analysis spanned the currently known phylogenetic diversity of the genus Neocosmospora, and included sequences from a total of 365 strains, based on the alignments published by O’Donnell et al. (2008). According to this analysis, the five strains from avocado formed an exclusive new linage in the genus Neocosmospora (data not shown, alignments, trees and statistics all available at TreeBASE). A second analysis was run based on a selected subset of DNA data representing most of the species of Neocosmospora currently assigned with Latin binomials, plus several yet unnamed phylogenetic clades phylogenetically related to the new lineage (Fig. 2). This final analysis included sequences from 80 strains, representing 48 taxa and a total of 2 917 character sites, of which 2 203 were conserved (EF-1α 212, ITS 372, LSU 441 and RPB2 1178), and 555 were variable and phylogenetically informative (EF-1α 69, ITS 101, LSU 35 and RPB2 350). The BI analyses identified a total of 774 unique sites (EF-1α 134, ITS 179, LSU 43 and RPB2 418) and sampled a total 315 000 trees, from which 236 250 were used to calculate the 50 % consensus tree and posterior probability (PP) values, after discarding 25 % of trees as burn-in fraction. Results from ML and BI methods showed that the clade encompassing the five strains from cankers on P. americana (CPC 29829 to 26833) correspond to a new linage in Neocosmospora (BS 96 / PP 1), closely related to the unnamed phylogenetic species FSSC 37 and 38, and clearly unrelated with the common Persea pathogens in the Ambrosia clade of Neocosmospora (clade nomenclature according to O’Donnell et al. 2008, 2016). The new lineage is proposed here as the new species Neocosmospora perseae.

Fig. 2.

Fig. 2.

Open in a new tab

Maximum-likelihood (ML) phylogram of the genus Neocosmospora obtained from combined EF-1α, ITS, LSU and RPB2 sequences. Branch lengths are proportional to distance. Numbers on the nodes are ML bootstrap values (BS) above 55 %; and Bayesian posterior probability values (PP) above 0.95. Full supported branches (BS = 100 and PP = 1) and isolates obtained from Persea americana are indicated in bold. Ex-type and ex-epitype strains are indicated with <SUP>T</SUP>, and <SUP>ET</SUP>, respectively.

Pathogenicity tests

Two Neocosmospora isolates tested were pathogenic to the Persea americana seedlings inoculated, and produced symptoms similar to those observed on diseased plants in the avocado orchard. Canker and internal discolouration symptoms were observed corresponding to inoculation points on avocado plants. Initial symptoms were observed after 1 mo. High DI (100 %) was observed after 3 mo with serious symptoms leading to plant death (Fig. 1). Similar results were obtained in both tests performed.

The pathogen was re-isolated from the artificially inoculated plants and identified as previously described, completing Koch’s postulates. No symptoms were observed on control plants.

TAXONOMY

Neocosmospora perseae Sandoval-Denis & Guarnaccia, sp. nov. MycoBank MB824587. Fig. 3.

Fig. 3.

Fig. 3.

Open in a new tab

Neocosmospora perseae (from ex-type CBS 144142). A, B. Colonies on PDA and OA, respectively, after 7 d at 24 °C in the dark. C. Colony on PDA after 20 d at 24 °C under continuous white light. D–F. Sporodochia formed on the surface of carnation leaves. G–I. Sporodochial conidiophores. J–O. Aerial conidiophores and phialides. P, Q. Aerial conidia (microconidia). R–T. Chlamydospores. U. Sporodochial conidia (macroconidia). Scale bars: P, Q, S, T = 5 μm, G = 20 μm, all others = 10 μm.

Etymology: Named after the host genus Persea.

Sporulation abundant from conidiophores formed directly on the substrate and aerial mycelium, and from sporodochia. Conidiophores straight to slightly flexuous, up to 350 μm tall, solitary and simple or branched one to several times irregularly and laterally, verticillately or sympodially, each branch bearing a single terminal monophialide; phialides subulate to subcylindrical, smooth- and thin-walled, (40.5–)45–66.5(–90.5) μm long, (2–)2.5–3(–3.5) μm wide at the base, tapering to (1–)1.5–2(–2.5) μm wide at the apex, often with conspicuous periclinal thickening and a minute, discrete collarette; conidia formed on aerial conidiophores, hyaline, obovoid, ellipsoidal, short clavate to cylindrical, symmetrical or gently bent dorsoventrally, smooth- and thin-walled, 0(–1)-septate, (4.5–)6–10.5(–13.5) × (1.5–)2.5–4(–6) μm, clustering in false heads at the tip of monophialides. Sporodochia at first white to cream-coloured, becoming pale luteous, green to dark blue-green when mature, formed abundantly on the surface of carnation leaves and lately on and under the agar surface. Conidiophores in sporodochia 26–54 μm tall, densely packed in a cushion-like structure, irregularly or verticillately branched, with terminal branches bearing verticills of 1–3 monophialides; sporodochial phialides doliiform, subulate to subcylindrical, (13.5–)14.5–18.5(–20.5) × 2.5–3.5(–4.5) μm, smooth- and thin-walled, with periclinal thickening and an inconspicuous apical collarette. Sporodochial conidia falcate, wedge-shaped, tapering toward the basal part, robust; smaller sized conidia often conspicuously curved; large sized conidia somewhat straight on its ventral line with a moderate dorsal curvature; apical cell blunt, more or less equally sized than the adjacent cell; basal cell distinctly notched, (3–)4–5(–6)-septate, hyaline, thick- and smooth-walled. Three-septate conidia: 30.5–32.5 × 5–5.5 μm; four-septate conidia: (39–)40.5–47(–49) × 5–5.5(–6.5) μm; five-septate conidia: (39.5–)45.5–51.5(–56) × (4.5–)5.5–6(–6.5) μm; six-septate conidia: 49–53.5(–55) × (5–)6–7 μm; overall (30.5–)43.5–52(–55.5) × (4.5–)5.5–6(–7) μm. Chlamydospores abundant and rapidly formed on agar media (approx. 7 d), hyaline to pale brown, spherical to subspherical (4.5–)6–8(–9) μm diam, solitary or in chains, terminal, intercalary or borne on short lateral pegs, smooth- and thick-walled.

Cardinal temperatures for growth: Minimum 9 °C, maximum 36 °C, optimum 27–30 °C.

Culture characteristics: Colonies on PDA showing radial growth rates of 4.4–7.2 mm/d at 27 °C and 4.1–6.8 mm/d at 30 °C in the dark, reaching a diameter of 72–74 mm after 7 d at 24 °C. Colony surface straw to pale luteous, flat, felty to floccose, aerial mycelium and sporulation abundant, white, becoming pale luteous to sulphur yellow; colony margins regular and filiform. Reverse amber to sulphur yellow, becoming bright red to scarlet with the production of abundant diffusible pigment. Colonies on OA showing a diameter of 62–66 mm after 7 d at 24 °C. Colony colour white with sienna to umber patches, flat to slightly umbonate and radiate, felty to floccose, aerial mycelium and sporulation abundant; margins filiform and slightly undulate. Reverse pale luteous with slight production of a scarlet to sienna coloured diffusible pigment.

Typification: Italy, Catania, San Leonardello, from trunk canker lesions on Persea americana, 25 Mar. 2015, G. Polizzi (holotype CBS H-23433, culture ex-type CBS 144142 = CPC 26829).

Additional isolates examined: Italy, Catania, San Leonardello, from trunk canker lesions on Persea americana, 25 Mar. 2015, G. Polizzi (CBS 144143 = CPC 26830; CBS 144144 = CPC 26831; CBS 144145 = CPC 26832; CBS 144146 = CPC 26833).

DISCUSSION

In this study, five Neocosmospora isolates were recovered from Persea americana trees showing trunk canker symptoms in Sicily (Southern Italy) during 2015, and identified based on single and multilocus phylogenetic analyses of four loci (EF-1α, ITS, LSU and RPB2), as well as morphological characters. These analyses revealed that the five isolates belonged to a novel species, described here N. perseae.

The robust four-loci based analysis allowed to distinguish N. perseae from “Fusarium” euwallaceae and N. ambrosia, already known as canker-causing species associated with symbiotic Euwallacea beetles. In spite of the recent detection of similar cankers caused by other fungal species in the same area (Guarnaccia et al. 2016), N. perseae was found as the only fungus associated with the disease. Because cankers developed in the absence of Euwallacea beetles, the fungus is clearly able to cause wood cankers independently. Furthermore, pathogenicity tests confirmed that N. perseae causes a high disease incidence on Persea americana, thereby fulfilling Koch’s postulates.

Neocosmospora perseae was clearly not related phylogenetically or morphologically with the most significant Neocosmospora canker pathogens affecting Persea, known to belong to the Ambrosia clade (Aoki et al. 2018). Moreover, while the new species exhibits the typical hyaline, falcate and multiseptate macroconidia and short clavate to cylindrical microconidia commonly attributed to this genus, the Persea pathogens in the Ambrosia clade of Neocosmospora are characterised by their irregularly clavate, somewhat swollen conidia, a putative evolutionary adaptation to its host (Freeman et al. 2013). Additionally, all currently known members of the Ambrosia clade exhibit a symbiotic lifestyle, associated with species of the shot hole borer beetle genus Euwallacea (Coleoptera, Xyleborini) (Mendel et al. 2012, Freeman et al. 2013, Kasson et al. 2013). In contrast, N. perseae showed no evidence of association with any vector, as demonstrated by the absence of wood galleries or any other sign of insect infestation in the trees. Its transmission is therefore more likely to respond to soil contamination and plant-associated reservoirs. Furthermore, the new species proved to be genetically closely related to two undescribed lineages (FSSC 37 and FSSC 38), yet, being phylogenetically and ecologically distinct. So far, phylogenetic species FSSC 37 is only known from diseased cocoa pods in New Guinea. However, FSSC 38, known from Benin & Uganda, has been isolated from the coffee borer beetle Hypothenemus hampei (Coleoptera, Scotylini) (O’Donnell et al. 2012), a relative to Euwallacea beetles. Similarly, the unrelated phylogenetic species FSSC 45 is known to inhabit the abdomen and external surfaces of Xylosandrus compactus (Coleoptera, Xyleborini) and its galleries (Bateman et al. 2016), which could suggest either that a similar insect-fungus mutualism or opportunism could also exist in other Neocosmospora lineages. However, no clear indication exists of FSSC 38 or FSSC 45 having either a pathogenic or symbiotic lifestyle with their insect hosts.

This study has revealed and characterised a new pathogenic fungal species, N. perseae, associated with trunk cankers on avocado in Italy, and includes information on its pathogenicity. As no epidemiological data are yet available it is not possible to suggest any control strategies to avoid N. perseae infections. Previous studies in the same geographical area have revealed a diversity of soil-borne fungal species (Polizzi et al. 2012, Vitale et al. 2012), including species pathogenic to avocado trees (Dann et al. 2012). Thus, these and other diseases might threaten avocado production, and could become a major limiting factor for future production.

Table 1.

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

Species Clade numbera Strain numberb Country and substrate GenBank/EBI accession numberc
EF-1α ITS LSU RPB2
Fusarium brasiliense NRRL 22743 Brazil, Glycine max EF408407 FJ919502 FJ919502 EU329525
Fusarium cuneirostrum NRRL 31104 Japan, Phaseolus vulgaris EF408413 FJ919509 FJ919509 EU329558
Fusarium ensiforme FSSC 15 NRRL 28009 USA, human eye DQ246869 DQ094351 DQ236393 EF470136
FSSC 15 NRRL 32792 Japan, human DQ247101 DQ094561 DQ236603 EU329621
Fusarium euwallaceae CBS 135855 = NRRL 54723 Israel, Beetle from Avocado Tree JQ038008 JQ038015 JQ038015 JQ038029
CBS 135856 = NRRL 54724 Israel, Beetle from Avocado Tree JQ038009 JQ038016 JQ038016 JQ038030
Fusarium keratoplasticum FSSC 2 CBS 490.63T = NRRL 22661 Japan, human eye DQ246846 DQ094331 DQ236373 EU329524
FSSC 2 NRRL 28561 USA, human DQ246902 DQ094375 DQ236417 EU329552
Fusarium lichenicola FSSC 16 NRRL 34123 India, human eye DQ247192 DQ094645 DQ236687 EU329635
Fusarium paranaense CML 1830T Brazil, Soybean root KF597797 KF680011
CML 1833 Brazil, Soybean root KF597798 KF680012
Fusarium petroliphilum FSSC 1 NRRL 22141 New Zealand, cucurbit AF178329 DQ094307 DQ236349 EU329491
FSSC 1 NRRL 43812 USA, contact lens solution EF453054 EF453205 EF453205 EF470093
Fusarium solani f. sp. pisi FSSC 11 NRRL 22820 USA, Glycine max AF178355 DQ094310 DQ236352 EU329532
FSSC 11 NRRL 45880 USA, Lab cross T10 (pea) and T219 (soil) FJ240352 EU329689 EU329689 EU329640
Fusarium solani f. sp. batatas FSSC 23 NRRL 22400 USA, Ipomoea batatas AF178343 AF178407 DQ236345 EU329509
Fusarium solani f. sp. xanthoxyli FSSC 22 NRRL 22163 Japan, Xanthoxylum sp. AF178336 AF178401 AF178370 FJ240380
Fusarium striatum FSSC 21 NRRL 22101 Panama, cotton cloth AF178333 AF178398 AF178367 EU329490
Neocosmospora ambrosia FSSC 19 NRRL 20438 India, Camellia sinensis AF178332 AF178397 DQ236357 JX171584
FSSC 19 NRRL 22346 India, Camellia sinensis FJ240350 EU329669 EU329669 EU329503
Neocosmospora croci CBS 142423T = CPC 27186 Italy, Citrus sinensis LT746216 LT746264 LT746264 LT746329
Neocosmospora croci CPC 27187 Italy, Citrus sinensis LT746217 LT746265 LT746265 LT746330
Neocosmospora cyanescens FSSC 27 CBS 518.82T = NRRL 37625 Netherlands, human foot FJ240353 EU329684 EU329684 EU329637
Neocosmospora falciformis FSSC 3+4 NRRL 32757 USA, sand DQ247075 DQ094536 DQ236578 EU329614
FSSC 3+4 NRRL 32828 USA, human DQ247135 DQ094594 DQ236636 EU329626
Neocosmospora illudens NRRL 22090 New Zealand, Beilschmiedia tawa AF178326 AF178393 AF178362 JX171601
Neocosmospora macrospora CBS 142424T = CPC 28191 Italy, Citrus sinensis LT746218 LT746266 LT746281 LT746331
CPC 28192 Italy, Citrus sinensis LT746219 LT746267 LT746282 LT746332
CPC 28193 Italy, Citrus sinensis LT746220 LT746268 LT746283 LT746333
Neocosmospora perseae CBS 144142T# = CPC 26829 Italy, Persea americana LT991902 LT991940 LT991947 LT991909
CBS 144143# = CPC 26830 Italy, Persea americana LT991903 LT991941 LT991948 LT991910
CBS 144144 = CPC 26831 Italy, Persea americana LT991904 LT991942 LT991949 LT991911
CBS 144145 = CPC 26832 Italy, Persea americana LT991905 LT991943 LT991950 LT991912
CBS 144146 = CPC 26833 Italy, Persea americana LT991906 LT991944 LT991951 LT991913
Neocosmospora plagianthi NRRL 22632 New Zealand, Hoheria glabrata AF178354 AF178417 AF178386 JX171614
Neocosmospora pseudensiformis FSSC 33 NRRL 22354 French Guiana, bark AF178338 AF178402 DQ236358 EU329504
Neocosmospora solani FSSC 5 CBS 140079ET = NRRL 66304 Slovenia, Solanum tuberosum KT313611 KT313633 KT313633 KT313623
FSSC 5 CPC 27736 Italy, Ficus carica LT991907 LT991945 LT991952 LT991914
FSSC 5 CPC 27737 Italy, Ficus carica LT991908 LT991946 LT991953 LT991915
FSSC 5 NRRL 32741 USA, human eye DQ247061 DQ094522 DQ236564 EU329608
Neocosmospora sp. FSSC 6 CBS 143194 = NRRL 22782 Spain, human corneal ulcer DQ246850 EU329670 EU329670 EU329528
FSSC 6 CBS 143210 = NRRL 32785 USA, human toenail cancer DQ247094 * FJ240371 EU329618
FSSC 7 CBS 130181 = NRRL 43502 USA, human eye DQ790488 DQ790532 DQ790532 DQ790576
FSSC 7 CBS 143209 = NRRL 32770 USA, human eye DQ247083 DQ094544 DQ236586 EU329615
FSSC 9 CBS 143208 = NRRL 32755 USA, turtle head lesion DQ247073 DQ094534 DQ236576 EU329613
FSSC 10 NRRL 22098 USA, cucurbit DQ247073 DQ094534 DQ236576 EU329613
FSSC 10 NRRL 22153 Panama, cucurbit AF178346 DQ094302 DQ236344 EU329492
FSSC 12 CBS 143212 = NRRL 32821 USA, turtle eggs DQ247128 DQ094587 DQ236629 EU329625
FSSC 12 NRRL 22642 Japan, Penaceous japonicus DQ246844 DQ094329 DQ236371 EU329522
FSSC 13 NRRL 22161 Japan, Robinia pseudoacacia AF178330 DQ094311 DQ236353 EU329494
FSSC 13 NRRL 22586 Japan, Robinia pseudoacacia AF178353 AF178416 AF178385 EU329516
FSSC 14 NRRL 32705 USA, human skin DQ247025 DQ094488 DQ236530 EU329594
FSSC 14 NRRL 32736 USA, human eye DQ247056 DQ094517 DQ236559 EU329605
FSSC 17 NRRL 22157 Japan, Morus alba AF178359 DQ094306 DQ236348 EU329493
FSSC 17 NRRL 22230 Japan, Morus alba AF178358 DQ094305 DQ236347 EU329499
FSSC 18 NRRL 31158 USA, human DQ246916 DQ094389 DQ236431 EU329559
FSSC 18 NRRL 32301 USA, human eye DQ246929 EU329677 EU329677 EU329567
FSSC 20 CBS 143214 = NRRL 32858 USA, human wound DQ247163 DQ094617 DQ236659 EU329630
FSSC 20 NRRL 28001 USA, human skin DQ246866 DQ094348 DQ236390 EF470129
FSSC 24 CBS 117481 = NRRL 22389 USA, Liriodendron tulipifera AF178340 AF178404 DQ236356 EU329506
FSSC 25 CBS 130328 = NRRL 31169 USA, human oral wound DQ246923 DQ094396 DQ236438 KR673999
FSSC 26 NRRL 28541 USA, human synovial fluid DQ246882 EU329674 EU329674 EU329542
FSSC 28 CBS 109028 = NRRL 32437 Switzerland, human subcutaneous nodule DQ246979 DQ094446 DQ236488 EU329581
FSSC 29 NRRL 28008 USA, human DQ246868 DQ094350 DQ236392 EF470135
FSSC 30 NRRL 22579 Indonesia, tree bark AF178352 AF178415 AF178384 EU329515
FSSC 31 NRRL 22570 Brazil, Piper nigrum AF178360 AF178422 AF178391 EU329513
FSSC 32 NRRL 22178 Venezuela, dicot tree AF178334 AF178399 AF178368 EU329498
FSSC 34 NRRL 46703 Spain, nematode HM347126 EU329712 EU329712 EU329661
FSSC 35 NRRL 46707 Brazil, human HM347127 EU329716 EU329716 EU329665
FSSC 37 NRRL 25137 New Guinea, diseased cocoa pods JF740757 JF740899 JF740899 JF741084
FSSC 37 NRRL 25138 New Guinea, diseased cocoa pods DQ247537 JF740900 JF740900 JF741085
FSSC 38 NRRL 52781 Benin, Hypothenemus hampei adult JF740849 * * JF741175
FSSC 38 NRRL 52782 Benin, Hypothenemus hampei adult * JF740850 JF740850 JF741176
FSSC 38 NRRL 52783 Benin, Hypothenemus hampei adult JF740851 * * JF741177
FSSC 39 FRC S-2432 USA, building JN235756 JN235326 JN235326 JN235941
FSSC 43 NRRL 54992 USA, Zebra shark multiple tissues KC808213 KC808255 KC808354
FSSC 43 NRRL 54993 USA, Zebra shark multiple tissues KC808214 KC808256 KC808355
FSSC 45 NRRL 62797 USA, Xylosandrus compactus KF906129 KF906130 KF906130 KF906132
Neocosmospora vasinfecta FSSC 8 CBS 130182 = NRRL 43467 USA, human eye EF452940 EF453092 EF453092 EF469979
FSSC 8 NRRL 22436 South Africa, soil AF178348 AF178412 DQ236359 JX171610
Open in a new tab
a

Clade nomenclature follows O’Donnell et al. (2008, 2016).

b

CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; CPC: Culture collection of P.W. Crous, housed at Westerdijk Fungal Biodiversity Institute; CML: Coleção Micológica de Lavras, Universidade Federal de Lavras, Minas Gerais, Brazil; F: College of Forestry, Northwest A&F University, Taicheng Road, Yangling, Shaanxi China; FRC: Fusarium Research Center, University Park, PA, USA; NRRL: Agricultural Research Service, Peoria, IL, USA. Ex- and ex-epitype strains are indicated with T, and ET, respectively.

#

Strains used in the pathogenicity tests.

c

EF-1α: Translation elongation factor 1-alpha; ITS: Internal transcribed spacer regions of the rDNA and 5.8S region; LSU: Partial large subunit of the rDNA; <I>RPB2</I>: RNA polymerase II largest subunit. * Sequences not publicly available, provided as DNA datasets by Kerry O’Donnell.

REFERENCES

  1. Aoki T, Kasson MT, Berger MC, et al. (2018). Fusarium oligoseptatum sp. nov., a mycosymbiont of the ambrosia beetle Euwallacea validus in the Eastern U.S. and typification of F. ambrosium. Fungal Systematics and Evolution 1: 23–39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aoki T, O’Donnell K, Homma Y, et al. (2003). Sudden-death syndrome of soybean is caused by two morphologically and phylogenetically distinct species within the Fusarium solani species complex - F. virguliforme in North America and F. tucumaniae in South America. Mycologia 95: 660–684. [PubMed] [Google Scholar]
  3. Bateman C, Šigut M, Skelton J, et al. (2016). Fungal associates of the Xylosandrus compactus (Coleoptera: Curculionidae, Scolytinae) are spatially segregated on the insect body. Environmental Entomology 45: 883–890. [DOI] [PubMed] [Google Scholar]
  4. Dann EK, Cooke AW, Forsberg LI, et al. (2012). Pathogenicity studies in avocado with three nectriaceous fungi, Calonectria ilicicola, Gliocladiopsis sp. and Ilyonectria liriodendri. Plant Pathology 61: 896–902. [Google Scholar]
  5. Farr DF, Rossman AY. (2018). Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Retrieved February 05, 2018, from https://nt.ars-grin.gov/fungaldatabases.
  6. Freeman S, Sharon M, Maymon M, et al. (2013). Fusarium euwallaceae sp. nov. – a symbiotic fungus of Euwallacea sp., an invasive ambrosia beetle in Israel and California. Mycologia 105: 1595–1606. [DOI] [PubMed] [Google Scholar]
  7. Guarnaccia V, Vitale A, Cirvilleri G, et al. (2016). Characterisation and pathogenicity of fungal species associated with branch cankers and stem-end rot of avocado in Italy. European Journal of Plant Pathology 146: 963–976. [Google Scholar]
  8. Gräfenhan T, Schroers HJ, Nirenberg HI, et al. (2011). An overview of the taxonomy, phylogeny, and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutella. Studies in Mycology 68: 79–113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kasson MT, O’Donnell K, Rooney AP, et al. (2013). An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. Fungal Genetics and Biology 56: 147–157. [DOI] [PubMed] [Google Scholar]
  10. Lombard L, Van der Merwe NA, Groenewald JZ, et al. (2015). Generic concepts in Nectriaceae. Studies in Mycology 80: 189–245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Liu YJ, Whelen S, Hall BD. (1999). Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biology and Evolution 16: 1799–1808. [DOI] [PubMed] [Google Scholar]
  12. Mendel Z, Protasov A, Sharon M, et al. (2012). An Asian ambrosia beetle Euwallacea fornicatus and its novel symbiotic fungus Fusarium sp. pose a serious threat to the Israeli avocado industry. Phytoparasitica 40: 235–238. [Google Scholar]
  13. Menge J, Ploetz RC. (2003). Diseases of avocado. In: Diseases of tropical fruit crops (Ploetz RC, ed.). Wallingford, UK: CABI Publishing: 35–71. [Google Scholar]
  14. Nylander JAA. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. [Google Scholar]
  15. O’Donnell K, Humber RA, Geiser DM, et al. (2012) Phylogenetic diversity of insecticolous fusaria inferred from multilocus DNA sequence data and their molecular identification via FUSARIUM-ID and Fusarium MLST. Mycologia 104: 427–445. [DOI] [PubMed] [Google Scholar]
  16. O’Donnell K, Gueidan C, Sink S, et al. (2009). A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genetics and Biology 46: 936–948. [DOI] [PubMed] [Google Scholar]
  17. O’Donnell K, Libeskind-Hadas R, Hulcr J, et al. (2016). Invasive Asian Fusarium – Euwallacea ambrosia beetle mutualists pose a serious threat to forests, urban landscapes and the avocado industry. Phytoparasitica 44: 435–442. [Google Scholar]
  18. O’Donnell K, Sutton DA, Fothergill A, et al. (2008). Molecular phylogenetic diversity, multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. Journal of Clinical Microbiology 46: 2477–2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. O’Donnell K, Sutton DA, Rinaldi MG, et al. (2010). Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. Journal of Clinical Microbiology 48: 3708–3718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Parkinson LE, Shivas RG, Dann EK. (2017). Pathogenicity of nectriaceous fungi on avocado in Australia. Phytopathology 107: 1479–1485. [DOI] [PubMed] [Google Scholar]
  21. Polizzi G, Vitale A, Aiello D, et al. (2012). First report of Calonectria ilicicola causing a new disease on Laurus (Laurus nobilis) in Europe. Journal of Phytopathology 160: 41–44. [Google Scholar]
  22. Rayner RW. (1970). A mycological colour chart. CMI and British Mycological Society, Kew, Surrey, UK. [Google Scholar]
  23. Sandoval-Denis M, Guarnaccia V, Polizzi G, et al. (2018). Symptomatic citrus trees reveal a new pathogenic lineage in Fusarium and two new Neocosmospora species. Persoonia 40: 1–25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sung GH, Sung JM, Hywel-Jones NL, et al. (2007). A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Molecular phylogenetics and evolution 44: 1204–1223. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Vilgalys R, Sun BL. (1994). Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proceedings of the National Academy of Science USA 91: 4599–4603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vitale A, Aiello D, Guarnaccia V, et al. (2012). First report of root rot caused by Ilyonectria (=Neonectria) macrodidyma on avocado (Persea americana) in Italy. Journal of Phytopathology 160: 156–159. [Google Scholar]
  28. White TJ, Bruns T, Lee S, et al. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications (Innes MA, Gelfand DH, Sninsky JJ, White TJ, eds). USA, NY, Academic Press: 315–322. [Google Scholar]

Articles from Fungal Systematics and Evolution are provided here courtesy of Westerdijk Fungal Biodiversity Institute

RESOURCES