Abstract
In 2007, Toxicocladosporium was established as new dematiaceous fungal genus in the family Cladosporiaceae that includes numerous plant pathogenic, epiphytic, endophytic, and saprobic fungi. A subsequent investigation on members of leaf-inhabiting fungi in Iran resulted in the identification of two new species belonging to the genus Toxicocladosporium associated with Eucalyptus leaves, described here as T. crousianum and T. eucalyptorum spp. nov. These novel taxa form independent lineages distinct from other taxa, based on morphological and multi-locus phylogenetic analyses. Detailed descriptions and illustrations of these two new taxa are presented. Additionally, the genus Toxicocladosporium represents a new fungal record for Iran.
Similar content being viewed by others
Data availability
All sequence data generated in this study (Table 1) are available at GenBank (https://www.ncbi.nlm.nih.gov/genbank/). Alignments used for phylogenetic analysis included in supplementary file.
References
Abdollahzadeh J, Groenewald JZ, Coetzee MPA, Wingfield MJ, Crous PW (2020) Evolution of lifestyles in Capnodiales. Stud Mycol 95:381–414
Alfenas RF, Lombard L, Pereira OL, Alfenas AC, Crous PW (2014) Diversity and potential impact of Calonectria species in Eucalyptus plantations in Brazil. Stud Mycol 80:89–130
Andjic V, Maxwell A, Hardy GES, Burgess TI (2016) New cryptic species of Teratosphaeria on Eucalyptus in Australia. IMA Fungus 7(2):253–263
Bakhshi M, Arzanlou M (2017) Multigene phylogeny reveals a new species and novel records and hosts in the genus Ramularia from Iran. Mycol Prog 16:703–712
Bakhshi M, Braun U (2022) Acericercospora hyrcanica gen. et sp. nov. (Mycosphaerellaceae) and Paramycocentrospora acericola gen. et sp. nov. (Dothidotthiaceae) on maple trees in Hyrcanian forests. Mycol Prog 21(8). https://doi.org/10.1007/s11557-022-01824-x
Bakhshi M, Arzanlou M, Babai-Ahari A, Groenewald JZ, Crous PW (2014) Multi-gene analysis of Pseudocercospora spp. from Iran. Phytotaxa 184:245–264
Bakhshi M, Arzanlou M, Zare R, Groenewald JZ, Crous PW (2019) New species of Septoria associated with leaf spot diseases in Iran. Mycologia 111(6):1056–1071
Bakhshi M, Zare R, Braun U, Taheri H (2021a) Polyphasic taxonomy of four passalora-like taxa occurring on fruit and forest trees. Mycol Prog 20:1157–1173
Bakhshi M, Zare R, Jafary H, Arzanlou M, Rabbani nasab H (2021b) Phylogeny of three Ramularia species occurring on medicinal plants of the Lamiaceae. Mycol Prog 20 (1):27–38
Ball JB (1995) Development of Eucalyptus plantations—an overview. In: White K, Ball J, Kashio M (eds) Proceedings of the Regional Expert Consultation on Eucalyptus Vol. I (Bangkok, Thailand 4–8 October 1993). FAO Regional Office for Asia and the Pacific, Bangkok, pp 15–27
Barber PA, Crous PW, Groenewald JZ, Pascoe IG, Keane P (2011) Reassessing Vermisporium (Amphisphaeriaceae), a genus of foliar pathogens of eucalypts. Persoonia 27:90–118
Barberán A, Ladau J, Leff JW, Pollard KS, Menninger HL, Dunn RR, Fierer N (2015) Continental-scale distributions of dust-associated bacteria and fungi. Proc Natl Acad Sci 112:5756–5761
Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401
Bezerra JD, Sandoval-Denis M, Paiva LM, Silva GA, Groenewald JZ, Souza-Motta CM, Crous PW (2017) New endophytic Toxicocladosporium species from cacti in Brazil, and description of Neocladosporium gen. nov. IMA Fungus 8:77–97
Bonadonna L, Briancesco R, Coccia AN, Fonda A, Rosa AL, Meloni P, Paradiso R, Paduano S, Semproni M (2014) Valutazione delle caratteristiche microbiologiche di inchiostri per tatuaggi in confezioni integre e dopo l’apertura. Microbiologia Medica 29(2):4807
Braun U, Nakashima C, Bakhshi M, Zare R, Shin HD, Alves RF, Sposito M (2020) Taxonomy and phylogeny of cercosporoid ascomycetes on Diospyros spp. with special emphasis on Pseudocercospora spp. Fungal Syst Evol 6:95–127
Brockerhoff EG, Jactel H, Parrotta JA, Ferraz SF (2013) Role of eucalypt and other planted forests in biodiversity conservation and the provision of biodiversity-related ecosystem services. For Ecol Manag 301:43–50
Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556
Cheewangkoon R, Crous PW, Hyde KD, Groenewald JZ, To-Anan C (2008) Species of Mycosphaerella and related anamorphs on Eucalyptus leaves from Thailand. Persoonia 21:77–91
Chen S, Lombard L, Roux J, Xie Y, Wingfield MJ, Zhou XD (2011) Novel species of Calonectria associated with Eucalyptus leaf blight in Southeast China. Persoonia 26:1–12
Crous PW, Gams W, Stalpers JA et al (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22
Crous PW, Braun U, Schubert K, Groenewald JZ (2007) Delimiting Cladosporium from morphologically similar genera. Stud Mycol 58:33–56
Crous PW, Wingfield MJ, Groenewald JZ (2009) Niche sharing reflects a poorly understood biodiversity phenomenon. Persoonia 22:83–94
Crous PW, Groenewald JZ, Roets F (2010a) Fungal planet 57. Toxicocladosporium protearum. Persoonia 25:134–135
Crous PW, Groenewald JZ, Shivas RG, McTaggart AR (2010b) Fungal Planet 63. Toxicocladosporium banksiae. Persoonia 25:146–147
Crous PW, Summerell BA, Shivas RG et al (2011) Fungal planet description sheets: 92–106. Persoonia 27:130–162
Crous PW, Shivas RG, Wingfield MJ et al (2012a) Fungal planet description sheets: 128–153. Persoonia 29:146–201
Crous PW, Summerell BA, Shivas RG et al (2012b) Fungal planet description sheets: 107–127. Persoonia 28:138–182
Crous PW, Wingfield MJ, Guarro J et al (2013) Fungal planet description sheets: 154–213. Persoonia 31:188–296
Crous PW, Shivas RG, Quaedvlieg WV et al (2014) Fungal planet description sheets: 214–280. Persoonia 32:184–306
Crous PW, Wingfield MJ, Richardson DM et al (2016) Fungal planet description sheets: 400–468. Persoonia 36:316–458
Crous PW, Verkley GJM, Groenewald JZ, Houbraken J (eds) (2019a) Fungal biodiversity. Westerdijk Lab Man Ser 1:1–425
Crous PW, Wingfield MJ, Cheewangkoon R et al (2019b) Foliar pathogens of eucalypts. Stud Mycol 94:125–298
Crous PW, Cowan DA, Maggs-Kölling G et al (2021a) Fungal planet description sheets: 1182–1283. Persoonia 46:313–528
Crous PW, Osieck ER, Jurjevi Ž et al (2021b) Fungal planet description sheets: 1284–1382. Persoonia 47:178–374
de Hoog GSD, van den Ende AHGG (1998) Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41:183–189
Farr DF, Rossman AY (2022) Fungal databases, U.S. National Fungus Collections, ARS, USDA. Available from https://nt.ars-grin.gov/fungaldatabases. Accessed 10 May 2022
Fotedar R, Sandoval-Denis M, Kolecka A, Zeyara A, Al Malki A, Al Shammari H, Al Marri M, Kaul R, Boekhout T (2019) Toxicocladosporium aquimarinum sp. nov, Toxicocladosporium qatarense sp. nov., isolated from marine waters of the Arabian Gulf surrounding Qatar. Int J Syst Evol Microbiol 69(10):2992–3000
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549
Lombard L, Chen S, Mou X, Zhou XD, Crous PW, Wingfield MJ (2014) New species, hyper-diversity and potential importance of Calonectria spp. from Eucalyptus in South China. Stud Mycol 80:151–188
Maddison WP, Maddison DR (2018) Mesquite: a modular system for evolutionary analysis. Version 3.61. http://mesquiteproject.org. Accessed 26 Dec 2019
McCarthy CB, Diambra LA, Rivera Pomar RV (2011) Metagenomic analysis of taxa associated with Lutzomyia longipalpis, vector of visceral leishmaniasis, using an unbiased high-throughput approach. PLoS Negl Trop Dis 5(9):e1304
Möller E, Bahnweg G, Sandermann H, Geiger HH (1992) A simple and efficient protocol for isolation of high molecular weight DNA from filamentous fungi, fruit bodies, and infected plant tissues. Nucleic Acids Res 20:6115–6116
Nugenta LK, Sangvichenb E, Sihanonthc P, Ruchikachorn N, Whalley AJ (2006) A revised method for the observation of conidiogenous structures in fungi. Mycologist 20:111–114
Nylander JAA (2004) MrModeltest v 2.0. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala
Old KM, Wingfield MJ, Yuan ZQ (2003) A manual of diseases in Eucalyptus in South East Asia. Centre for International Forestry Research (CIFOR), Bogor
Piñar G, Sterflinger K, Pinzari F (2015) Unmasking the measles-like parchment discoloration: molecular and microanalytical approach. Environ Microbiol 17:427–443
Potts BM, Pederick LA (2000) Morphology, phylogeny, origin, distribution and genetic diversity of eucalypts. CSIRO Publishing, Australia, pp 11–34
Rayner RW (1970) A mycological colour chart. CMI and British Mycological Society, Kew, Surrey, England, 34 pp
Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Sandoval-Denis M, Sutton DA, Martin-Vicente A, Cano-Lira JF, Wiederhold N, Guarro J, Gené J (2015) Cladosporium species recovered from clinical samples in the United States. J Clin Microbiol 53(9):2990–3000
Satoh K, Yamazaki T, Nakayama T, Umeda Y, Alshahni MM, Makimura M, Makimura K (2016) Characterization of fungi isolated from the equipment used in the International Space Station or Space Shuttle. J Microbiol Immunol 60(5):295–302
Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b 10. Sinauer Associates, Sunderland
Thornhill AH, Crisp MD, Külheim C, Lam KE, Nelson LA, Yeates DK, Miller JT (2019) A dated molecular perspective of eucalypt taxonomy, evolution and diversification. Aust Syst Bot 32(1):29–48
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246
White TJ, Bruns T, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylognetics. In: Innis MA, Gelfand DH, Sninsky JJ, White JW (eds) A guide to molecular methods and applications. Academic Press, New York, pp 315–322
Acknowledgements
The authors gratefully acknowledge Prof. Dr. Pedro W. Crous (Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands) for his valuable comments on the manuscript and Prof. Dr. Uwe Braun (Martin-Luther-University, Halle, Germany) for his helpful advice on the nomenclature. We are obliged to the Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), for financial support.
Funding
This research was financially supported by Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO).
Author information
Authors and Affiliations
Contributions
Experiments, morphological, and molecular analyses were conducted by Mounes Bakhshi. Rasoul Zare and Hossein Jafary contributed to the data analyses of the taxa and funding acquisition. The first draft of the manuscript was written by Mounes Bakhshi and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript and have agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Roland Kirschner
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Fig. 1
Consensus phylogram (50% majority rule) resulting from a Bayesian analysis of the LSU sequence alignment using MrBayes 3.2.6. The scale bar indicates 0.05 expected changes per site. The tree was rooted to Neocladosporium leucadendri (CBS 131317) (JPG 642 kb)
Supplementary Fig. 2
Consensus phylogram (50% majority rule) resulting from a Bayesian analysis of the ITS sequence alignment using MrBayes 3.2.6. The scale bar indicates 0.05 expected changes per site. The tree was rooted to Neocladosporium leucadendri (CBS 131317) (JPG 588 kb)
Supplementary Fig. 3
Consensus phylogram (50% majority rule) resulting from a Bayesian analysis of the ACT sequence alignment using MrBayes 3.2.6. The scale bar indicates 0.05 expected changes per site. The tree was rooted to Neocladosporium leucadendri (CBS 131317) (JPG 572 kb)
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bakhshi, M., Zare, R. & Jafary, H. Toxicocladosporium crousianum and T. eucalyptorum, two new foliar fungi associated with Eucalyptus trees. Mycol Progress 21, 77 (2022). https://doi.org/10.1007/s11557-022-01826-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11557-022-01826-9