Skip to main content
Log in

A multi-locus backbone tree for Pestalotiopsis, with a polyphasic characterization of 14 new species

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

Pestalotiopsis is a taxonomically confused, pathogenic and chemically creative genus requiring a critical re-examination using a multi-gene phylogeny based on ex-type and ex-epitype cultures. In this study 40 isolates of Pestalotiopsis, comprised of 28 strains collected from living and dead plant material of various host plants from China were studied by means of morphology and analysis of ITS, β–tubulin and tef1 gene sequence data. Based on molecular and morphological data we describe 14 new species (Pestalotiopsis asiatica, P. chinensis, P. chrysea, P. clavata, P. diversiseta, P. ellipsospora, P. inflexa, P. intermedia, P. linearis, P. rosea, P. saprophyta, P. umberspora, P. unicolor and P. verruculosa) and three species are epitypified (P. adusta, P. clavispora and P. foedans). Of the 10 gene regions (ACT, β-tubulin, CAL, GPDH, GS, ITS, LSU, RPB 1, SSU and tef1) utilized to resolve cryptic Pestalotiopsis species, ITS, β–tubulin and tef1 proved to be the better markers. The other gene regions were less useful due to poor success in PCR amplification and/or in their ability to resolve species boundaries. As a single gene tef1 met the requirements for an ideal candidate and functions well for species delimitation due to its better species resolution and PCR success. Although β-tubulin showed fairly good differences among species, a combination of ITS, β-tubulin and tef1 gene data gave the best resolution as compared to single gene analysis. This work provides a backbone tree for 22 ex-type/epitypified species of Pestalotiopsis and can be used in future studies of the genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18
Fig. 19
Fig. 20
Fig. 21
Fig. 22
Fig. 23
Fig. 24
Fig. 25
Fig. 26

Similar content being viewed by others

References

  • Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16

    Article  Google Scholar 

  • Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977

    Article  PubMed  CAS  Google Scholar 

  • Barnes I, Roux J, Coetzee MPA, Wingfield MJ (2001) Characterization of Seiridium spp. associated with cypress canker based on ȕ-tubulin and histone sequences. Plant Dis 85:317–321

    Article  CAS  Google Scholar 

  • Barr ME (1975) Pestalosphaeria, a new genus in the Amphisphaeriaceae. Mycologia 67:187–194

    Article  Google Scholar 

  • Barr ME (1990) Prodromus to nonlichenized, pyrenomycetous members of class Hymenoascomycetes. Mycotaxon 39:43–184

    Google Scholar 

  • Bate-Smith EC, Metcalfe CR (1957) Leucanthocyanins.3. The nature and systematic distribution of tannin in dicotyledonous plants. J Linn Soc (Bot) 55:669–705

    Article  Google Scholar 

  • Bridge PD, Spooner BM, Roberts PJ (2005) The impact of molecular data in fungal systematics. Adv Bot Res 42:33–67

    Article  CAS  Google Scholar 

  • Cai L, Giraud T, Zhang N, Begerow D, Cai G, Shivas RG (2011) The evolution of species concepts and species recognition criteria in plant pathogenic fungi. Fungal Divers 50:121–133

    Article  Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    Article  CAS  Google Scholar 

  • Chomnunti P, Schoch CL, Aguirre-Hudson B, Ko Ko TW, Hongsanan S, Jones EBG, Kodsueb R, Phookamsak R, Chukeatirote E, Bahkali AH, Hyde KD (2011) Capnodiaceae. Fungal Divers 51:103–134

    Article  PubMed  Google Scholar 

  • Crous PW, Verkley GJM, Christensen M, Castañeda-Ruiz RF, Groenewald JZ (2012) How important are conidial appendages? Persoonia 28:126–137

    Google Scholar 

  • Das R, Chutia M, Das K, Jha DK (2010) Factors affecting sporulation of Pestalotiopsis disseminata causing grey blight disease of Persea bombycina Kost., the primary food plant of muga silkworm. Crop Prot 29:963–968

    Article  Google Scholar 

  • Dennis RWG (1995) Fungi of the South East England. Royal Botanic Gardens, Kew

    Google Scholar 

  • Ding G, Liu S, Guo L, Zhou Y, Che Y (2008) Antifungal metabolites from the plant endophytic fungus Pestalotiopsis foedan. J Nat Prod 71:615–618

    Google Scholar 

  • Douanla-Meli C, Langer E (2009) Pestalotiopsis theae (Ascomycota, Amphisphaeriaceae) on seeds of Diospyros crassiflora (Ebenaceae). Mycotaxon 107:441–448

    Article  Google Scholar 

  • Druzhinina IS, Kopchinskiy AG, Komoń M, Bissett J, Szakacs G, Kubicek CP (2005) An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet Biol 42:813–828

    Article  PubMed  CAS  Google Scholar 

  • Ellis MB, Ellis JP (1997) Microfungi on land plants: an identification handbook, 2nd edn (New Enlarged). Richmond Publishing

  • Espinoza JG, Briceno EX, Keith LM, Latorre BA (2008) Canker and Twig Dieback of blueberry caused by Pestalotiopsis spp. and a Truncatella sp. in Chile. Plant Dis 92:1407–1414

  • Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Geiser DM, Jiménez-Gasco M, Kang S, Makalowska I, Veeraraghavan N, Ward TJ, Zhang N, Kuldau GA, O’Donnell K (2004) FUSARIUM-ID v. 1.0: A DNA sequence database for identifying Fusarium. Eur J Plant Pathol 110:473–479

    Article  CAS  Google Scholar 

  • Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330

    PubMed  CAS  Google Scholar 

  • Guba EF (1961) Monograph of Pestalotia and Monochaetia. Harvard University Press, Cambridge

    Google Scholar 

  • Guerber JC, Liu B, Correll JC, Johnston PR (2003) Characterization of diversity in Colletotrichum acutatum sensu lato by sequence analysis of two gene introns, mtDNA and intron RFLPs, and mating compatibility. Mycologia 95:872–895

    Article  PubMed  CAS  Google Scholar 

  • Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis (Palmae) using morphological and molecular techniques. New Phytol 147:617–630

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hu HL, Jeewon R, Zhou DQ, Zhou TX, Hyde KD (2007) Phylogenetic diversity of endophytic Pestalotiopsis species in Pinus armandii and Ribes spp.: evidence from rDNA and β- tubulin gene phylogenies. Fungal Divers 24:1–22

    CAS  Google Scholar 

  • Hyde KD, Bussaban B, Paulus B, Crous PW, Lee S, McKenzie EHC, Photita W, Lumyong S (2007) Diversity of saprobic microfungi. Biodivers Conserv 16:7–35

    Article  Google Scholar 

  • Jeewon R, Liew ECY, Simpson JA, Hodgkiss IJ, Hyde KD (2003) Phylogenetic significance of morphological characters in the taxonomy of Pestalotiopsis species. Mol Phylogenet Evol 27:372–383

    Google Scholar 

  • Kang JC, Hyde KD, Kong RYC (1999) Studies on the Amphisphaeriales. The Amphisphaeriaceae (sensu stricto). Mycol Res 103:53–64

    Article  Google Scholar 

  • Kang JC, Kong RYC, Hyde KD (1998) Studies on the Amphisphaeriales I. Amphisphaeriaceae (sensu stricto) and its phylogenetic relationships inferred from 5.8 S rDNA and ITS2 sequences. Fungal Divers 1:147–157

    Google Scholar 

  • Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:276–285

    Google Scholar 

  • Keith LM, Velasquez ME, Zee FT (2006) Identification and characterization of Pestalotiopsis spp. causing scab disease of guava, Psidium guajava in Hawaii. Plant Dis 90:16–23

    Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data. J Mol Evol 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kohlmeyer J, Kohlmeyer VB (2001) Fungi on Juncus roemerianus 16. More new coelomycetes, including Tetranacriella gen. nov. Bot Mar 44:147–156

    Article  Google Scholar 

  • Ko Ko T, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120

    Article  Google Scholar 

  • Lee S, Crous PW, Wingfield MJ (2006) Pestalotioid fungi from Restionaceae in the Cape Floral Kingdom. Stud Mycol 55:175–187

    Article  PubMed  Google Scholar 

  • Li E, Jiang L, Guo L, Zhang H, Che Y (2008) Pestalachlorides A–C, antifungal metabolites from the plant endophytic fungus Pestalotiopsis adusta. Bioorg Med Chem 16:7894–7899

    Google Scholar 

  • Liu AR, Chen SC, Wu SY, Xu T, Guo LD, Jeewon R, Wei JG (2010) Cultural studies coupled with DNA based sequence analyses and its implication on pigmentation as a phylogenetic marker in Pestalotiopsis taxonomy. Mol Phylogenet Evol 57:528–535

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Hall BD (2004) Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Natl Acad Sci 101:4507–4512

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–808

    Article  PubMed  CAS  Google Scholar 

  • Liu AR, Xu T, Guo LD (2007) Molecular and morphological description of Pestalotiopsis hainanensis sp. nov., a new endophyte from a tropical region of China. Fungal Divers 24:23–36

    Google Scholar 

  • Lombard L, Crous PW, Wingfield BD, Wingfield MJ (2010) Phylogeny and systematics of the genus Calonectria. Stud Mycol 66:31–69

    Google Scholar 

  • Maharachchikumbura SSN, Guo LD, Chukeatirote E, Bahkali AH, Hyde KD (2011) Pestalotiopsis–morphology, phylogeny, biochemistry and diversity. Fungal Divers 50:167–187

    Article  Google Scholar 

  • Maharachchikumbura SSN, Chukeatirote E, Guo LD, Crous PW, McKenzie EHC, Hyde KD (2012a) Pestalotiopsis species associated with Camellia sinensis (tea). Mycotaxon (in press)

  • Maharachchikumbura SSN, Guo LD, Chukeatirote E, McKenzie EHC, Hyde KD (2012b) A destructive new disease of Syzygium samarangense in Thailand caused by the new species Pestalotiopsis samarangensis. Trop plant pathol (in press)

  • Maas JL (1971) Hyalotia pistacina a new species and a notes on Pestalotiopsis thujae. Mycologia 63:663–668

    Article  Google Scholar 

  • Moriya S, Inoue S, Ohkuma M, Yaovapa T, Kohjima T, Suwanarit P, Sangwanti U, Vongkaluang C, Noparatnaraporn N, Kudo T (2005) Fungal community analysis of fungal gardens in termite nests. Microbes Environ 20:243–252

    Article  Google Scholar 

  • Myllys L, Stenroos S, Thell A (2002) New genes for phylogenetic studies of lichenized fungi: glyceraldehyde-3-phosphate dehydrogenase and beta-tubulin genes. Lichenologist 34:237–246

    Article  Google Scholar 

  • Nag Rag TR (1993) Coelomycetous anamorphs with appendage bearing conidia. Mycologue, Waterloo

  • O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116

    Article  PubMed  Google Scholar 

  • O’Donnell K, Nirenberg H, Aoki T, Cigelnik E (2000) A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience 41:61–78

    Article  Google Scholar 

  • O’Donnell K et al (2010) Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J Clin Microbiol 48:3708–3718

    Article  PubMed  Google Scholar 

  • Page RDM (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    Google Scholar 

  • Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K, Chukeatirote E, Hyde KD (2010) Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Divers 44:33–43

    Google Scholar 

  • Rehner SA, Samuels GJ (1994) Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycol Res 98:625–634

    Article  CAS  Google Scholar 

  • Rehner SA (2001) Primers for Elongation Factor 1-alpha (EF1-alpha). http://ocid.nacse.org/research/deephyphae/EF1primer.pdf

  • Roger AJ, Sandblom O, Doolittle WF, Philippe H (1999) An evaluation of elongation factor 1 alpha as a phylogenetic marker for eukaryotes. Mol Biol Evol 16:218–233

    Article  PubMed  CAS  Google Scholar 

  • Saccardo PA (1902) Deuteromycetes, melanconiaceae, phragmasporae, monochaetia. Sylloge Fungorum 16:1017

    Google Scholar 

  • Saccardo PA (1914) Fungi italici. Ann Mycol 12:310

    Google Scholar 

  • Saccardo PA (1931) Deuteromycetes, melanconiaceae, monochaetia. Sylloge Fungorum 25:610

    Google Scholar 

  • Santos JM, Correia VG, Phillips AJL (2010) Primers for mating-type diagnosis in Diaporthe and Phomopsis: their use in teleomorph induction in vitro and biological species definition. Fungal Biology 114:255–270

    Google Scholar 

  • Schoch CL et al (2009) The ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239

    Article  PubMed  CAS  Google Scholar 

  • Schoch CL et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA. doi:10.1073/pnas.1117018109, Available at: www.pnas.org/cgi/doi/10.1073/pnas.1117018109

  • Stephenson SA, Green JR, Manners JM, Maclean DJ (1997) Cloning and characterisation of glutamine synthetase from Colletotrichum gloeosporioides and demonstration of elevated expression during pathogenesis on Stylosanthes guianensis. Curr Genet 31:447–454

    Article  PubMed  CAS  Google Scholar 

  • Steyaert RL (1949) Contributions à l’étude monographique de Pestalotia de Not. et Monochaetia Sacc. (Truncatella gen. nov. et Pestalotiopsis gen. nov.). Bull Jard Bot Brux 19:285–354

    Article  Google Scholar 

  • Strobel G, Li JY, Ford E, Worapong J, Gary IB, Hess WM (2000) Pestalotiopsis jesteri, sp. nov. an endophyte from Fragraea bodenii Wernh, a common plant in the southern highlands of Papua New Guinea. Mycotaxon 76:257–266

    Google Scholar 

  • Strobel G, Ford E, Worapong J, Harper JK, Arif AM, Grant DM, Fung PC, Chau MW (2002) Isopestacin, an isobenzofuranone from Pestalotiopsis microspora, possessing antifungal and antioxidant activities. Phytochemistry 60:179–183

    Article  PubMed  CAS  Google Scholar 

  • Strobel G, Yang XS, Sears J, Kramer R, Sidhu RS, Hess WM (1996) Taxol from Pestalotiopsis microspora of Taxus wallachiana. Microbiology 142:435–440

    Article  PubMed  CAS  Google Scholar 

  • Summerell BA, Laurence MH, Liew ECY, Leslie JF (2010) Biogeography and phylogeography of Fusarium: a review. Fungal Divers 44:3–13

    Google Scholar 

  • Swofford DL (2002) PAUP* 4.0: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland

    Google Scholar 

  • Tanaka K, Endo M, Hirayama K, Okane I, Hosoya T, Sato T (2011) Phylogeny of Discosia and Seimatosporium, and introduction of Adisciso and Immersidiscosia genera nova. Persoonia 26:85–98

    Article  PubMed  CAS  Google Scholar 

  • Tejesvi MV, Kini KR, Prakash HS, Subbiah V, Shetty HS (2007a) Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Divers 24:37–54

    Google Scholar 

  • Tejesvi MV, Nalini MS, Mahesh B, Prakash HS, Kini KR, Shetty HS, Subbiah V (2007b) New hopes from endophytic fungal secondary metabolites. Bol Soc Quím de Méx 1(1):19–26

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Thongkantha S, Lumyong S, McKenzie EHC, Hyde KD (2008) Fungal saprobes and pathogens occurring on tissues of Dracaena lourieri and Pandanus spp. in Thailand. Fungal Divers 30:149–169

    Google Scholar 

  • Udayanga D, Liu XZ, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers (in press)

  • Venkatasubbaiah P, Grand LF, Dyke CGV (1991) A new species of Pestalotiopsis on Oenothera. Mycologia 83:511–513

    Article  Google Scholar 

  • Wei JG, Xu T (2004) Pestalotiopsis kunmingensis, sp. nov., an endophyte from Podocarpus macrophyllus. Fungal Divers 15:247–254

    Google Scholar 

  • Wei JG, Xu T, Guo LD, Liu AR, Zhang Y, Pan XH (2007) Endophytic Pestalotiopsis species associated with plants of Podocarpaceae, Theaceae and Taxaceae in southern China. Fungal Divers 24:55–74

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Wikee S, Cai L, Pairin N, McKenzie EHC, Su YY, Chukeatirote E, Thi HN, Bahkali AH, Moslem MA, Abdelsalam K (2011) Colletotrichum species from jasmine (Jasminum sambac). Fungal Divers 46:171–182

    Google Scholar 

  • Wu CG, Tseng HY, Chen ZC (1982) Fungi inhabiting on Schoenoplectus triqueter (L.) Palla (I). Taiwania 27:35–38

    Google Scholar 

  • Xu J, Ebada SS, Proksch P (2010) Pestalotiopsis a highly creative genus: chemistry and bioactivity of secondary metabolites. Fungal Divers 44:15–31

    Article  Google Scholar 

  • Yasuda F, Kobayashi T, Watanabe H, Izawa H (2003) Addition of Pestalotiopsis spp. to leaf spot pathogens of Japanese persimmon. J Gen Plant Pathol 69:29–32

    Article  Google Scholar 

  • Zhao GC, Li N (1995) Thirty-four species of pestalotiopsis in Yunnan. J Northeast For Univ 23:21–33

    Google Scholar 

  • Zhang J, Xu T, Ge Q (2002) Notes on Pestalotiopsis from southern China. Mycotaxon 85:91–99

    Google Scholar 

  • Zhang Y, Hyde KD (2008) Epitypification: should we epitypify? J Zhejiang Univ Sci B 9:842–846

    Article  PubMed  CAS  Google Scholar 

  • Zhang YM, Maharachchikumbura SSN, McKenzie EHC, Hyde KD (2012a) A novel species of Pestalotiopsis causing leaf spots of Trachycarpus fortunei. Cryptogamie mycol (in press)

  • Zhang YM, Maharachchikumbura SSN, McKenzie EHC, Hyde KD (2012b) Pestalotiopsis camelliae sp. nov. associated with grey blight of Camellia japonica in China (unpublished)

  • Zhou D, Hyde KD (2001) Host-specificity, host-exclusivity and host-recurrence in saprobic fungi. Mycol Res 105:1449–1457

    Article  Google Scholar 

Download references

Acknowledgments

We thank Thailand Research Fund (grant: BRG5280002); The National Research Council of Thailand (grant for Pestalotiopsis No: 55201020008); Mae Fah Luang University (grant for Pestalotiopsis No: 55101020004); The National Natural Science Foundation of China (grant: 30930005); the Knowledge Innovation Program of the Chinese Academy of Sciences (grant: KSCX2-YW-Z-0935); Mushroom Research Foundation, Chiang Mai, Thailand; State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China and the King Saud University for supporting this research. We kindly acknowledge Novozymes, CGMCC and ICMP for providing cultures and BPI, CUP and NY herbaria for providing type materials for this study.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Liang-Dong Guo or Kevin D. Hyde.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maharachchikumbura, S.S.N., Guo, LD., Cai, L. et al. A multi-locus backbone tree for Pestalotiopsis, with a polyphasic characterization of 14 new species. Fungal Diversity 56, 95–129 (2012). https://doi.org/10.1007/s13225-012-0198-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-012-0198-1

Keywords

Navigation