Cladosporium Link, Mag. Gesell. naturf. Freunde, Berlin 7: 37 (1816) [1815]


Cladosporium belongs to Cladosporiaceae in the order Capnodiales (Hyde et al. 2013; Liu et al. 2017). Established in 1816 with C. herbarum as type species, Cladosporium is one of the largest genera of dematiaceous hyphomycetes. Davidiella was erected by Braun et al. (2003) to accommodate the sexual morph of Cladosporium sensu stricto. Davidiella was therefore recognized as a synonym of Cladosporium as Cladosporium has priority over Davidiella at generic rank, and is also the more commonly used name in literature (Bensch et al. 2012). Therefore, Cladosporiaceae took preference over Davidiellaceae (Bensch et al. 2012). Cladosporium species have a worldwide distribution and can be easily spread in the environment, because of their small conidia. Cladosporium includes many important pathogens causing leaf spots and stem rots of many plant hosts. For example, Cladosporium fulvum is the causal agent of tomato leaf mold (van Kan et al. 1991). Cladosporium species have been recorded as endophytes and may have a positive effect, for example, C. sphaerospermum was isolated from the roots of Glycine max which can promote its growth (Hamayun et al. 2009). Some species, such as C. herbarum, are also known as common contaminants in clinical laboratories and cause allergic lung disease (de Hoog et al. 2000). Several species were also isolated from human respiratory samples (Sandoval-Denis et al. 2016). Thirteen species are fungicolous (Heuchert et al. 2005; Sun et al. 2019) and have the potential for biological control in agriculture and forestry (Torres et al. 2017).

There have been studies towards understanding the genetic components of Cladosporium. Cladosporium fulvum is an important model species in the plant pathology study. Iakovidis et al. (2020) reported classical mapping strategies for loci of tomato that response to sequence-monomorphic effector Ecp5. Convergent evolution could be used for choosing different functional genes according to individual plant breeding needs. Ge et al. (2019) showed that Cladosporium species have the potential to be used in industrial processes. They identified a new glucose oxidase gene CtgoxB from C. tianshanense and suggested this could be a candidate for the aquatic feed and detergent industries. Transcriptome and proteome analyses of C. fulvuim showed that 14 out of 59 predicted proteases are expressed during in vitro and in planta, of which nine belong to serine proteases and the rest belong to metallo and aspartic proteases (Jashni et al. 2019). This study also confirmed the presence of six proteases at proteome level during the infection.

Grinn-Gofroń et al. (2019) developed and evaluated the models of forecasting possibilities of airborne spore concentrations in 18 sites in six countries across Europe. The study revealed the possibility of reliable prediction of fungal spore levels using gridded meteorological data. They concluded that these forecasting models can be used in the more timely and efficient management of phytopathogenic and of human allergic diseases. An environmentally isolated strain of C. sphaerospoermum substantially enhanced plant growth, early flowering and increase in crop yield after exposure in vitro (Li et al. 2019). Pan et al. (2020) identified four new hybrid polyketides (Cladosin L-O) from C. shaerospermum which showed strong cytotoxicity, antifungal activity and moderate antibacterial activity.

Classification: Ascomycota, Pezizomycotina, Dothideomycetes, Pleosporomycetidae, Capnodiales, Cladosporiaceae

Type speciesCladosporium herbarum (Pers.) Link

Distribution– Worldwide

Disease symptoms–Leaf spots, leaf blight, discolourations, necrosis, or shot-hole symptoms, on stems and fruits, rots

HostsCladosporium species occur on a wide range of host plants including Asparagaceae, Asteraceae, Fabaceae, Myrtaceae, Orchidaceae, Poaceae, Solanaceae and Vitaceae (Farr and Rossman 2020). Some species can be hyperparasites of insects and fungi (Heuchert et al. 2005; Islam et al. 2019; Sun et al. 2019; Abdel-Baky 2000). These species can cause allergies in humans such as sneezing, hives and also can cause eye, ear and sinus infections (de Hoog et al. 2000).

Pathogen biology, disease cycle and epidemiology

Cladosporium survives in the soil or on plant debris and produce spores during humid weather. Fungal spores germinate under high humidity and cool to warm temperatures. Wind, rain and irrigation splash, workers, tools, and insects readily disseminate spores (Jordan et al. 1990; Lan and Scherm 2003; Liu et al. 2019).


Morphological based identification and diversity

The asexual morph of Cladosporium species is characterized by a unique coronate structure of the conidiogenous loci and conidia, consisting of the central convex dome surrounded by a raised periclinal rim (Bensch et al. 2012; Fig 1), while ascomata of sexual morphs are identical to those of Mycosphaerella (sect. Tassiana) (Braun et al. 2003). Historically, all types of dematiaceous hyphomycetes with amero- to phragmosporous conidia formed in acropetal chains had been assigned to Cladosporium sensu lato, resulting in the complication to resolve a natural classification of Cladosporium. Various mycologists proposed natural genetic circumscriptions of Cladosporium (David 1997; Braun et al. 2003; Aptroot 2006). David (1997) found the unique structure of conidiogenous loci and conidial hila using scanning electron microscopy. Based on the genetic circumscriptions, some cladosporioid groups, such as Fusicladium being non-coronate (Schubert et al. 2003), have been excluded from Cladosporium s. str. Various Cladosporium species have been re-examined based on the new generic concepts (Schubert and Braun 2004, 2005a, b, 2007; Schubert 2005; Schubert et al. 2006; Braun and Schubert 2007; Braun et al. 2008). A polyphasic approach revealed three major species complexes within Cladosporium, viz. C. cladosporioides, C. herbarum and C. sphaerospermum (Schubert et al. 2007; Dugan et al. 2008; Bensch et al. 2010; Bensch et al. 2015). A modern monograph of the genus treated 993 names of Cladosporium sensu lato, of which 169 were recognized in Cladosporium sensu stricto and others remain doubtful (Bensch et al. (2012).

Fig. 1 Cladosporium cladosporioides.a. Conidiomata. b-c,e. Macro- and micronematous conidiophores and conidia chains. d. Secondary ramoconidia. f. Conidia. Scale bars: b–c, e–f=50 µm, d–g=10 µm.

Molecular based identification and diversity

The first molecular examination of Cladosporium-like hyphomycetes based on ITS and SSU was carried out by Braun et al. (2003), who confirmed the strong heterogeneity. A new genus Davidiella was established to accommodate the sexual morphs of Cladosporium sensu stricto species which were previously assigned in Mycosphaerella. Aptroot (2006) made a better circumscription of Davidiella after he found species of Davidiella have ascospores with irregular cellular inclusions, which are absent in Mycosphaerella. Schoch et al. (2006) studied the phylogenetic relationships of 96 taxa of the Dothideomycetes using LSU, SSU, tef1 and rpb2 gene data. Davidiella and its Cladosporium asexual morphs were assigned to the family Cladosporiaceae in the order Capnodiales, together with Mycosphaerellaceae. Crous et al. (2007) delimited Cladosporium from morphologically similar genera using their morphology and DNA phylogeny based on LSU. Several species were transferred to new genera such as Hyalodendriella, Ochrocladosporium, Rachicladosporium, Rhizocladosporium, Toxicocladosporium and Verrucocladosporium. Furthermore, C. castellanii was confirmed as a synonym of Stenella araguata, while the type species of Stenella resided in Teratosphaeriaceae instead of Mycosphaerellaceae. Schubert et al. (2007) performed a comprehensive study of the C. herbarum species complex based on both morphology and phylogenetic analysis with five combined genes. Bensch et al. (2010) carried out species and ecological diversity within the C. cladosporioides species complex. More than 200 isolates belonging to the C. cladosporioides species complex were examined and analyzed on the basis of ITS, actand tef1 gene regions. A comprehensive monograph of Cladosporium sensu lato was provided by Bensch et al. (2012) based on morphology and combined ITS, act and tef1 sequence data. In their study, 993 names assigned to Cladosporium sensu lato are treated and 169 names were recognized in Cladosporium sensu stricto. Bensch et al. (2015) introduced the three major species complexes in Cladosporium, i.e. C. cladosporioides, C. herbarum and C. sphaerospermum, and 19 new species were described. Razafinarivo et al. (2016) introduced a new species C. lebrasiae from milk bread rolls in France, Ma et al. (2017) introduced six new soil-inhabiting Cladosporium species from plateaus in China. Bensch et al. (2018) studied Cladosporium species from indoor environments and introduced 16 new species. Several new Cladosporium species including Cladosporium omanense (Halo et al. 2019), C. passiflorae and C. passifloricola (Rosado et al. 2019) have been introduced more recently. In this study, we reconstruct the phylogeny of Cladosporium based on ITS, tef1 and act sequenced data (Table 1; Fig 2).

Recommended genetic marker (genus level) – ITS and LSU

Recommended genetic markers (species level)act and tef1 (in a few cases tub2)

Accepted number of species–There are 844 epithets listed in Index Fungorum (2020), however, 138 species have DNA sequence data.

References–David 1997, Aptroot 2006, Schubert and Braun 2004, 2005a, b, 2007; Schubert 2005; Schubert et al. 2006; Braun and Schubert 2007; Braun et al. 2008 (morphology); Braun et al. 2003,Schoch et al. 2006, Bensch et al. 2010, 2012, 2015, Ma et al. 2017 (morphology and phylogeny).

Table 1 DNA barcodes available for Cladosporium. Ex-type/ex-epitype/ex-neotype/ex-lectotype strains are in bold and marked with an asterisk (*). Voucher strains are also in bold. Species confirmed with pathogenicity studies are marked with #.

Species Isolate ITS tef1 act
Cladosporium acalyphae CBS 125982* HM147994 HM148235 HM148481
C. aciculare CBS 140488* KT600411 KT600509 KT600607
C. aerium CBS 143356* MF472897 MF473324 MF473747
C. aggregatocicatricatum# CBS 140493* KT600448 KT600547 KT600645
C. alboflavescens CBS 140690* LN834420 LN834516 LN834604
C. allicinum CBS 121624* EF679350 EF679425 EF679502
C. allii CBS 101.81 JN906977 JN906983 JN906996
C. angulosum CBS 140692* LN834425 LN834521 LN834609
C. angustiherbarum CBS 140479* KT600378 KT600475 KT600574
C. angustisporum CBS 125983* HM147995 HM148236 HM148482
C. angustiterminale CBS 140480* KT600379 KT600476 KT600575
C. antarcticum CBS 690.92* EF679334 EF679405 EF679484
C. anthropophilum CBS 140685* LN834437 LN834533 LN834621
C. aphidis CBS 132182* JN906978 JN906984 JN906997
C. arthropodii CBS 124043* JN906979 JN906985 JN906998
C. asperulatum# CBS 126340* HM147998  HM148239 HM148485
C. australiense CBS 125984* HM147999 HM148240 HM148486
C. austroafricanum CBS 140481* KT600381 KT600478 KT600577
C. austrohemisphaericum CBS 140482* KT600382 KT600479 KT600578
C. basiinflatum# CBS 822.84* HM148000 HM148241 HM148487
C. chalastosporoides CBS 125985* HM148001 HM148242 HM148488
C. chasmanthicola CBS 142612* KY646221 KY646227 KY646224
C. chubutense CBS 124457* FJ936158 FJ936161 FJ936165
C. cladosporioides# CBS 112388* HM148003 HM148244 HM148490
C. colocasiae# CBS 386.64* HM148067 HM148310 HM148555
C. colombiae CBS 274.80B* FJ936159 FJ936163 FJ936166
C. coloradense CBS 143357* MF472945 MF473372 MF473795
C. crousii CBS 140686* LN834431 LN834527 LN834615
C. cucumerinum# CBS 171.52* HM148072 HM148316 HM148561
C. cycadicola CBS 137970* KJ869122 KJ869236 KJ869227
C. delicatulum CBS 126344* HM148081 HM148325 HM148570
C. domesticum CBS 143358* MF472955 MF473382 MF473805
C. dominicanum CBS 119415* DQ780353 JN906986 EF101368
C. echinulatum# CBS 123191 JN906980 JN906987 JN906999
C. endophyticum MFLUCC 17-0599* MG646956 MG646988
C. entadae MFLUCC 17-0919* MK347728
C. europaeum CBS 134914* HM148056 HM148298 HM148543
C. exasperatum CBS 125986* HM148090 HM148334 HM148579
C. exile CBS 125987* HM148091 HM148335 HM148580
C. fildesense ChFC-554* JX845290 MN233633 MN233632
C. flabelliforme CBS 126345* HM148092 HM148336 HM148581
C. flavovirens CBS 140462* LN834440 LN834536 LN834624
C. floccosum# CBS 140463* LN834416 LN834512 LN834600
C. funiculosum CBS 122129* HM148094 HM148338 HM148583
C. fusiforme CBS 119414* DQ780388 JN906988 EF101372
C. gamsianum CBS 125989* HM148095 HM148339 HM148584
C. globisporum# CBS 812.96* HM148096 HM148340 HM148585
C. grevilleae CBS 114271* JF770450 JF770472 JF770473
C. halotolerans CBS 119416* DQ780364 JN906989 EF101397
C. hebeiense# JZB390001* MG516597 MG516595 MG516593
C. herbaroides# CBS 121626* EF679357 EF679432 EF679509
C. herbarum# CBS 121621* EF679363 EF679440 EF679516
C. hillianum CBS 125988* HM148097 HM148341 HM148586
C. inversicolor CBS 401.80* HM148101 HM148345 HM148590
C. ipereniae CBS 140483* KT600394 KT600491 KT600589
C. iranicum# CBS 126346* HM148110 HM148354 HM148599
C. iridis# CBS 138.40* EF679370 EF679447 EF679523
C. kenpeggii# CBS 142613* KY646222 KY646228 KY646225
C. langeronii CBS 189.54* DQ780379 JN906990 EF101357
C. lebrasiae CBS 138283* KJ596568 KJ596583 KJ596631
C. licheniphilum CBS 125990* HM148111 HM148355 HM148600
C. limoniforme# CBS 140484* KT600397 KT600494 KT600592
C. longicatenatum CBS 140485* KT600403 KT600500 KT600598
C. longissimum CBS 300.96* DQ780352 EU570259 EF101385
C. lycoperdinum CBS 126347 HM148112 HM148356 HM148601
C. macrocarpum# CBS 121623* EF679375 EF679453 EF679529
C. magnoliigena MFLUCC 18-1559* MK347813 MK340864
C. michoacanense CBS 143588* LT907958 LT907945 LT907961
C. montecillanum CBS 140486* KT600406 KT600504 KT600602
C. myrtacearum CBS 126350* HM148117 HM148361 HM148606
C. needhamense CBS 143359* MF473142 MF473570 MF473991
C. neerlandicum CBS 143360* KP701887 KP701764 KP702010
C. neolangeronii CBS 797.97* MF473143 MF473992
C. neopsychrotolerans CGMCC 3.18031* KX938383 KX938400 KX938366
C. omanense SQUCC 13165* MH725789 MH716047 MH716046
C. ossifragi CBS 842.91* EF679381 EF679459 EF679535
C. oxysporum# CBS 125991 HM148118 HM148362 HM148607
C. paracladosporioides CBS 171.54* HM148120 HM148364 HM148609
C. parahalotolerans CBS 139585* KP701955 KP701832 KP702077
C. paralimoniforme CGMCC 3.18103* KX938392 KX938409 KX938375
C. parapenidielloides CBS 140487* KT600410 KT600508 KT600606
C. parasubtilissimum CBS 143361* MF473170 MF473593 MF474018
C. passiflorae# COAD 2135* MH682175 MH724943 MH729795
C. passifloricola COAD 2140* MH724948 MH729800
C. penidielloides CBS 140489* KT600412 KT600510 KT600608
C. perangustum# CBS 125996* HM148121 HM148365 HM148610
C. phaenocomae CBS 128769* JF499837 JF499875 JF499881
C. phlei# CBS 358.69* JN906981 JN906991 JN907000
C. phyllactiniicola CBS 126352* HM148150 HM148394 HM148639
C. phyllophilum CBS 125992* HM148154 HM148398 HM148643
C. pini-ponderosae CBS 124456* FJ936160 FJ936164 FJ936167
C. prolongatum CGMCC 3.18036* KX938394 KX938411 KX938377
C. pseudiridis CBS 116463* EF679383 EF679461 EF679537
C. pseudochalastosporoides CBS 140490* KT600415 KT600513 KT600611
C. pseudocladosporioides# CBS 125993* HM148158 HM148402 HM148647
C. psychrotolerans CBS 119412* DQ780386 JN906992 EF101365
C. pulvericola CBS 143362* MF473226 MF473648 MF474075
C. puyae CBS 274.80A* KT600418 KT600516 KT600614
C. ramotenellum# CBS 121628* EF679384 EF679462 EF679538
C. rectoides CBS 125994* HM148193 HM148438 HM148683
C. rhusicola CBS 140492* KT600440 KT600539 KT600637
C. ruguloflabelliforme CBS 140494* KT600458 KT600557 KT600655
C. rugulovarians CBS 140495* KT600459 KT600558 KT600656
C. salinae CBS 119413* DQ780374 JN906993 EF101390
C. scabrellum CBS 126358* HM148195 HM148440 HM148685
C. silenes CBS 109082* EF679354 EF679429 EF679506
C. sinense CBS 143363* MF473252 MF473675 MF474102
C. sinuatum CGMCC 3.18096* KX938385 KX938402 KX938368
C. sinuosum CBS 121629* EF679386 EF679464 EF679540
C. sloanii CBS 143364* MF473253 MF473676 MF474103
C. soldanellae CBS 132186* JN906982 JN906994 JN907001
C. sphaerospermum# CBS 193.54* DQ780343 EU570261 EF101380
C. spinulosum CBS 119907* EF679388 EF679466 EF679542
C. subcinereum CBS 140465* LN834433 LN834529 LN834617
C. subinflatum CBS 121630* EF679389 EF679467 EF679543
C. subtilissimum# CBS 113754* EF679397 EF679475 EF679551
C. subuliforme# CBS 126500* HM148196 HM148441 HM148686
C. succulentum CBS 140466* LN834434 LN834530 LN834618
C. tenellum# CBS 121634* EF679401 EF679479 EF679555
C. tenuissimum# CBS 125995* HM148197 HM148442 HM148687
C. tianshanense CGMCC 3.18033* KX938381 KX938364
C. tuberosum CBS 140693* LN834417 LN834513 LN834601
C. uredinicola ATCC 46649 AY251071 HM148467 HM148712
C. uwebraunianum CBS 143365* MF473306 MF473729 MF474156
C. variabile# CBS 121635* EF679402 EF679480 EF679556
C. varians CBS 126362* HM148224 HM148470 HM148715
C. velox CBS 119417* DQ780361 JN906995 EF101388
C. verrucocladosporioides CBS 126363* HM148226 HM148472 HM148717
C. verruculosum CGMCC 3.18099* KX938388 KX938405 KX938371
C. versiforme CBS 140491* KT600417 KT600515 KT600613
C. vicinum CBS 143366* MF473311 MF473734 MF474161
C. vignae# CBS 121.25 HM148227 HM148473 HM148718
C. welwitschiicola CBS 142614* KY646223 KY646229 KY646226
C. westerdijkiae CBS 113746* HM148061 HM148303 HM148548
C. wyomingense CBS 143367* MF473315 MF473738 MF474165
C. xanthochromaticum CBS 140691* LN834415 LN834511 LN834599
C. xylophilum CBS 125997* HM148230 HM148476 HM148721
Toxicocladosporium banksiae CBS 128215* HQ599598   LT821371

Fig 2 Phylogram generated from Maximum Likelihood analysis based on ITS, tef1 and act sequenced data. Bootstrap support values ≥75% and Bayesian posterior probabilities ≥0.95 are given near the nodes. The ex-type (ex-epitype) and voucher strains are in bold. The tree is rooted with Toxicocladosporium banksiae CBS 128215.

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