Cyphellophora

Cyphellophora G.A. de Vries, Mycopath. Mycol. appl. 16(1):47(1962)

Cyphellophora is cosmopolitan, comprising species distributed from a broad range of environmental sources as human and animal disease, saprobes, epiphytes and plant pathogens (de Hoog et al. 1999, 2000; Jacob and Bhat 2000; Decock et al. 2003; Crous et al. 2007; Zhuang et al. 2010; Feng et al. 2014; Mayfield et al. 2012; Gao et al. 2015; Phookamsak et al. 2019). Most species, including the type species, C. laciniata, were isolated from nails or skin of humans, resulting in clinical symptoms (Feng et al. 2014). Phylogenetically, C. phyllostachysdis clustered with C. europaea, a human or mammal infection of hyperkeratosis (de Hoog et al. 2000). In contrast, C. phyllostachysdis causes sooty blotch and flyspeck (SBFS) of bamboo and is not found in humans (Gao et al. 2015). The sooty mold species C. jingdongensis was introduced with a sexual morph; it reduces plant photosynthesis but does not damage or cause disease of the plant (Chomnunti et al. 2014; Yang et al. 2018).

ClassificationEurotiomycetes, Chaetothyriomycetidae, Chaetothyriales, Cyphellophoraceae

Type speciesCyphellophora laciniata G.A. de Vries, Mycopath. Mycol. appl. 16(1):47(1962)

Distribution – Australia, Brazil, China, Germany, India, Israel, Korea, Taiwan

Disease symptoms – Sooty blotch and flyspeck (main symptoms of this disease are given under Chaetothyrina).

To date, C. artocarpi, C. guyanensis, C. jingdongensis, C. musae, C. olivacea, C. oxyspora, C. phyllostachydis and C. sessilis have been isolated from plant materials (Gams and Holubová-Jechová 1976; de Hoog et al. 1999; Decock et al. 2003; Gao et al. 2015; Yang et al. 2018). Cyphellophora artocarpi, C. musae, C. phyllostachydis and C. sessilis were reported to cause sooty blotch and flyspeck from apple, jackfruit (Artocarpus heterophyllus) and bamboo (Phyllostachys heterocycla, Sinobambusa tootsik), resulting in significant economic damage (Zhuang et al. 2010; Mayfield et al. 2012; Gao et al. 2015).

HostsArtocarpus heterophyllus, Dendrocalamus strictus, Eucalyptus sp., Helomeco velane, Hylomecon verlance, Malus domestica, Musa sp., Phyllostachys sp., Sinobasmbusa tootsik, and Stenocalyx uniflorus.

 

Morphological based identification and diversity

It is difficult to identify this black yeast-like genus based solely on morphological characters since the characters are very similar to those of other black yeast-like fungi, such as Phialophora and Pseudomicrodochium. Species of Cyphellophora resemble those of Phialophora in having melanized thalli with intercalary or terminal phialides bearing collarettes, but Phialophora has aseptate conidia whereas Cyphellophora produces larger, fusiform to sigmoid, aseptate to multi-septate conidia (Réblová et al. 2013). Cyphellophora can also be compared to Pseudomicrodochium, the former having melanized thalli while they are hyaline in Pseudomicrodochium (Decock et al. 2003; de Hoog et al. 2009, 2011). Yang et al. (2018) introduced C. jingdongensis the first sexual morph, which is characterized by subglobose to globose, non-ostiolate ascomata, ellipsoidal to cylindrical asci and fusoid, 1–3 septate ascospores. However, the asexual morph of C. jingdongensis was difficult to observe in culture to compare with other species in Cyphellophora (Yang et al. 2018). There are 26 epithets of Cyphellophora in Index Fungorum (2019). Yang et al. (2018) clarified 23 species in this genus. To properly delineate these species, phylogenetic studies using multi-loci sequences (ITS, LSU, RPB1 and TUB2) and the secondary structures of ITS analyses are needed (Réblová et al. 2013; Feng et al. 2014; Gao et al. 2015; Yang et al. 2018).

 

Molecular based identification and diversity

Based on SSU and LSU sequence data, Cyphellophora clustered in a well-supported clade within the Chaetothyriales (Feng et al. 2014). Generic and species delimitation with morphological characters, ecological traits, host distribution and phylogenetic analyses using the internal transcribed spacer region (ITS), the partial β-tubulin gene (TUB2), the nuclear large subunit rDNA gene (LSU) and the DNA dependent RNA polymerase II largest subunit (RPB1) were recently performed (Feng et al. 2014; Gao et al. 2015). The present study reconstructs the phylogeny of Cyphellophora based on analyses of combined ITS, TUB2, LSU and RPB1 sequence data (Table 4, Fig. 9). The phylogenetic tree in this study is updated with recently introduced Cyphellophora species and corresponds to previous studies (Feng et al. 2014; Gao et al. 2015). Cyphellophoroa indica and C. taiwanensis lack sequences in GenBank (4/7/2019). Cyphellophoroa hylomeconis was synonymized as Camptophora hylomeconis and C. eugeniae was synonymized as Aphanophora eugeniae (Réblová et al. 2013). Cyphellophoroa eucalypti were synonymized as C. guyanensis (Feng et al. 2014). Therefore, these species were not included in the present phylogenetic analyses (Fig. 9).

 

Recommended genetic markers (genus level) – LSU and SSU

Recommended genetic markers (species level) – ITS, LSU, TUB2, RPB1 and secondary (2D) structure of ITS analyses

LSU is useful for preliminary identification at the generic level (Feng et al. 2014). Réblová et al. (2013) resolved Cyphellophora and Phialophora as close relatives within the Chaetothyriales, although both genera were paraphyletic based on analysis of ITS, TUB2 and nuc28S rDNA sequence data. It is recommended to use a combination of ITS, LSU, TUB2, RPB1 and secondary (2D) structure of ITS analyses (Réblová et al. 2013; Feng et al. 2014; Gao et al. 2015) in order to identify to the species level.

Accepted number of species: 24 species

References: Vries 1962, 1986; Matsushima 1987; Walz and Hoog 1987; Decock et al. 2003; Crous et al. 2013, 2016; Réblová et al. 2013; Feng et al. 2014; Gao et al. 2015; Madrid et al. 2016; Yang et al. 2018 (morphology, phylogeny)

Table Details of the Cyphellophora isolates used in the phylogenetic analyses. Ex-type (ex-epitype) strains are in bold and marked with an asterisk* and voucher stains are in bold

Species Isolate/Voucher no ITS LSU RPB1 TUB2
Cyphellophora ambigua CBS 235.93* JQ766431 JQ766480 JQ766386 JQ766340
C. artocarpi CGMCC3.17496* KP010367 KP122930 KP122920 KP122925
C. catalaunica CPC 22929* HG003670 HG003673
C. chlamydospora CBS 127581 (= FMR 10878) * HG003674 HG003675
C. europaea CBS 101466* JQ766443 KC455259 JQ766395 JQ766365
C. europaea CBS 218.78 JQ766441 JQ766488 JQ766393 JQ766366
C. europaea CBS 129.96 JQ766440 JQ766487 JQ766392 JQ766364
C. filicis KUMCC 18-0144 MK404056 MK404052
C. fusarioides CBS 130291* JQ766439 KC455252 JQ766391 JQ766363
C. gamsii CPC 25867* KX228255 KX228307 KX228381
C. guyanensis MUCL 43737* KC455240 KC455253 KC455223
C. guyanensis CBS 124764 GQ303274 GQ303305
C. guyanensis CBS 126014 JQ766434 JQ766483 JQ766389 JQ766339
C. jingdongensis IFRDCC 2659* MF285234 MF285236
C. laciniata CBS 190.61* JQ766423 JQ766472 JQ766378 JQ766329
C. laciniata CBS 174.79 JQ766422 JQ766471 JQ766377 JQ766328
C. laciniata CBS 239.91 JQ766424 JQ766473 JQ766379 JQ766330
C. livistonae CPC19433 KC005774 KC005796
C. musae CGMCC3.17497* KP010370 KP122932 KP122922 KP122927
C. musae GLGZXJ9B KP010368 KP122931 KP122923 KP122926
C. musae GLMMZZ4 KP010369 KP122934 KP122921 KP122928
C. olivacea  CBS 123.74* KC455248 KC455261 KC455231
C. olivacea CBS 122.74 KC455247 KC455260 KC455230
C. oxyspora CBS 698.73* JQ766450 KC455262 JQ766402 KC455232
C. oxyspora CBS 416.89 JQ766449 JQ766497 JQ766401 JQ766374
C. pauciseptata CBS 284.85* JQ766466 JQ766515 JQ766415 JQ766360
C. phyllostachidis CGMCC3.17495* KP010371 KP122933 KP122924 KP122929
C. pluriseptata CBS 286.85* JQ766429 KC455255 JQ766384 JQ766335
C. pluriseptata CBS 109633 JQ766430 JQ766479 JQ766385 JQ766336
C. reptans CBS 113.85* JQ766445 JQ766493 JQ766397 JQ766370
C. reptans CBS 152.90 JQ766446 JQ766494 JQ766398 JQ766371
C. reptans CBS 458.92 JQ766447 JQ766495 JQ766399 JQ766372
C. reptans CBS120903 JQ766448 JQ766496 JQ766400 JQ766373
C. sessilis CBS 243.85* EU514700 EU514700 KC455234
C. sessilis CBS 238.93 AY857541 KF928523 KF928587
C. suttonii CBS 449.91* JQ766459 KC455256 KC455226
C. suttonii FMR 10589 KU705828 KU705845
C. vermispora CBS 228.86* KC455244 KC455257 JQ766381 JQ766332
C. vermispora  CBS 122852 JQ766427 JQ766476 JQ766382 JQ766333
C. vermispora CBS 227.86 JQ766425 JQ766474 JQ766380 JQ766331
Cladophialophora immunda CBS 834.96 EU137318 KC809990 EU137203

Fig. Phylogram generated from RAxML analysis based on combined sequences of ITS, LSU, RPB1 and TUB2 sequences of all accepted species of Cyphellophora. Forty-one strains are included in the analyses, which comprise 2514 characters including gaps. The tree was rooted with Cladophialophora immunda (CBS 834.96). The tree topology of the ML analysis was similar to the MP and BYPP analyses. The best scoring RAxML tree with a final likelihood value of -5928.387430 is presented. The matrix had 337 distinct alignment patterns, with 12.44% of undetermined characters or gaps. Estimated base frequencies were as follows; A = 0.234866, C = 0.250597, G = 0.284325, T = 0.230211; substitution rates AC = 1.492532, AG = 2.025910, AT = 2.769660, CG = 1.674732, CT = 8.545312, GT = 1.000000; gamma distribution shape parameter α = 0.136482. RAxML and maximum parsimony bootstrap support value ≥50% are shown respectively near the nodes. Bayesian posterior probabilities ≥0.95 (BYPP) indicated as thickened black branches. Ex-type strains are in bold.

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