Advertisement

Mycological Progress

, Volume 15, Issue 10–11, pp 1093–1117 | Cite as

Species diversity of Pseudocercospora from Far East Asia

  • Chiharu Nakashima
  • Keiichi Motohashi
  • Chi-Yu Chen
  • Johannes Z. Groenewald
  • Pedro W. Crous
Original Article

Abstract

This study reflects on the monophyly of, and species diversity within, the genus Pseudocercospora in Far East Asia. Morphological characteristics and phylogenetic analyses of Pseudocercospora species were based on type specimens and ex-type cultures, which were collected from Japan and Taiwan. A phylogenetic tree was generated from multi-locus DNA sequence data of the internal transcribed spacer regions of the nrDNA cistron (ITS), partial actin (actA), and partial translation elongation factor 1-alpha (tef1), as well as the partial DNA-directed RNA polymerase II second largest subunit (rpb2). Based on these results, Pseudocercospora amelanchieris on Amelanchier and Ps. iwakiensis on Ilex were newly described from Japan, and a further 22 types (incl. two neo-, five lecto-, and 15 epitypes), were designated. The genus Pseudocercospora as presently circumscribed was found to be monophyletic, while the secondary barcodes, actA, tef1, and rpb2 were shown to be well suited to delimitate species within the genus.

Keywords

Epitypification New species Phylogenetic relationship Species criteria Taxonomy 

Notes

Acknowledgments

This work was supported by grants to the first author by JSPS KAKENHI (grant #17780122, 24780149), JSPS Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation (S2507), Institute for fermentation, Osaka and Genebank, National Institute of Agrobiological Science, Japan.

Supplementary material

11557_2016_1231_MOESM1_ESM.pdf (134 kb)
ESM. 1 A subtree extracted from Fig. 1 (PDF 134 kb)

References

  1. Bagyanarayana G, Braun U (1999) Phytopathogenic micromycetes from India (II). Sydowia 51:1–19Google Scholar
  2. Bakhshi M, Arzanlou M, Babai-Ahari A, Groenewald JZ, Crous PW (2014) Multi-gene analysis of Pseudocercospora spp. from Iran. Phytotaxa 184:245–264CrossRefGoogle Scholar
  3. Braun U (1995) A monograph of Cercosporella, Ramularia and allied genera (phytopathogenic hyphomycetes). Vol. 1. Eching: IHW VerlagGoogle Scholar
  4. Braun U, Crous PW, Nakashima C (2014) Cercosporoid fungi (Mycosphaerellaceae) 2. Species on monocots (Acoraceae to Xyridaceae, excluding Poaceae). IMA Fungus 5:203–390CrossRefPubMedPubMedCentralGoogle Scholar
  5. Braun U, Crous PW, Nakashima C (2015a) Cercosporoid fungi (Mycosphaerellaceae) 3. Species on monocots (Poaceae, true grasses). IMA Fungus 6:25–97CrossRefPubMedPubMedCentralGoogle Scholar
  6. Braun U, Crous PW, Nakashima C (2015b) Cercosporoid fungi (Mycosphaerellaceae) 4. Species on dicots (Acanthaceae to Amaranthaceae). IMA Fungus 6:373–469CrossRefPubMedPubMedCentralGoogle Scholar
  7. Braun U, Crous PW, Nakashima C (2016a) Cercosporoid fungi (Mycosphaerellaceae) 5. Species on dicots (Anacardiaceae to Annonaceae). IMA Fungus 7:161–216CrossRefPubMedPubMedCentralGoogle Scholar
  8. Braun U, Hönig L, Schwaß R (2016b) New records of foliicolous micromycetes from the Chinese Jiangxi Province. Schlechtendalia 30:1–7Google Scholar
  9. Braun U, Nakashima C, Crous PW (2013) Cercosporoid fungi (Mycosphaerellaceae) 1. Species on other fungi, Pteridophyta and Gymnospermae. IMA Fungus 4(2):265–345Google Scholar
  10. Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556CrossRefGoogle Scholar
  11. Chupp C (1954) A monograph of the fungus genus Cercospora. Charles Chupp, IthacaGoogle Scholar
  12. Crous PW (2009) Taxonomy and phylogeny of the genus Mycosphaerella and its anamorph. Fungal Divers 38:1–24Google Scholar
  13. Crous PW, Braun U (1996) Cercosporoid fungi from South Africa. Mycotaxon 57:233–321Google Scholar
  14. Crous PW, Braun U (2003) Mycosphaerella and its Anamorphs. 1. Names published in Cercospora and Passalora. CBS Biodiversity Series no. 1, Utrecht, CBS-KNAW Fungal Biodiversity CentreGoogle Scholar
  15. Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas Plant Pathol 34:463–470CrossRefGoogle Scholar
  16. Crous PW, Groenewald JZ, Shivas RG (2010) Pseudocercospora nephrolepidicola. Fungal Planet 59. Persoonia 25:138–139Google Scholar
  17. Crous PW, Braun U, Hunter GC, Verkley GJM, Shin HD, Nakashima C, Groenewald JZ (2013) Phylogenetic lineages in Pseudocercospora. Stud Mycol 75:37–114CrossRefPubMedGoogle Scholar
  18. Crous PW, Hawksworth DL, Wingfield MJ (2015) Identifying and naming plant-pathogenic fungi: past, present, and future. Annu Rev Phytopathol 53:247–267CrossRefPubMedGoogle Scholar
  19. de Hoog GS, Gerrits van den Ende AHG (1998) Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41:183–189CrossRefPubMedGoogle Scholar
  20. den Breeÿen A, Groenewald JZ, Verkley GJM, Crous PW (2006) Morphological and molecular characterisation of Mycosphaerellaceae associated with the invasive weed, Chromolaena odorata. Fungal Divers 23:89–110Google Scholar
  21. Deighton FC (1976) Studies on Cercospora and allied genera. VI. Pseudocercospora Speg., Pantospora Cif. and Cercoseptoria Petr. Mycol Pap 140:1–168Google Scholar
  22. Deighton FC (1979) Studies on Cercospora and allied genera. VII. New species and redispositions. Mycol Pap 144:1–56Google Scholar
  23. Deighton FC (1983) Studies on Cercospora and allied genera. VIII. Further notes on Cercoseptoria and some new species and redispositions. Mycol Pap 151:1–13Google Scholar
  24. Deighton FC (1987) New species of Pseudocercospora and Mycovellosiella, and new combinations into Pseudocercospora and Phaeoramularia. Trans Br Mycol Soc 88:365–391CrossRefGoogle Scholar
  25. Deighton FC (1990) Observations on Phaeoisariopsis. Mycol Res 94:1096–1102CrossRefGoogle Scholar
  26. Guatimosim E, Schwartsburd PB, Barreto RW, Crous PW (2016) Novel fungi from an ancient niche: cercosporoid and related sexual morphs on ferns. Persoonia 37:106–141Google Scholar
  27. Guo YL (1995) Four new species of Pseudocercospora. Mycosystema 7:119–127, “1994”Google Scholar
  28. Guo YL, Hsieh WH (1995) The genus Pseudocercospora in China. Mycosyst Monogr Ser 2:1–388Google Scholar
  29. Guo YL, Liu XJ (1992) Studies on the genus Pseudocercospora in China VI. Mycosystema 5:99–108Google Scholar
  30. Hasegawa M, Kishino H, Yano T (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefPubMedGoogle Scholar
  31. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192CrossRefGoogle Scholar
  32. Hsieh WH, Goh TK (1990) Cercospora and similar fungi from Taiwan. Maw Chang Book Co., TaipeiGoogle Scholar
  33. Katsuki S (1965) Cercosporae of Japan. Trans Mycol Soc Jpn, Extra Issue 1:1–100Google Scholar
  34. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  35. Kirschner R (2013) A new species and new records of cercosporoid fungi from ornamental plants in Taiwan. Mycol prog 13:483–491CrossRefGoogle Scholar
  36. Kirschner R, Liu LC (2014) Mycosphaerellaceous fungi and new species of Venustosynnema and Zasmidium on ferns and fern allies in Taiwan. Phytotaxa 176:309–323CrossRefGoogle Scholar
  37. Kirschner R, Wang H (2015) New species and records of mycosphaerellaceous fungi from living fern leaves in East Asia. Mycol Prog 14:65. doi: 10.1007/s11557-015-1085-4 CrossRefGoogle Scholar
  38. Kishino H, Hasegawa H (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179CrossRefPubMedGoogle Scholar
  39. Liang C, Jayawardena RS, Zhang W, Wang X, Liu M, Liu L, Zang C, Xu X, Hyde KD, Yan J, Li X, Zhao K (2016) Identification and characterization of Pseudocercospora species causing grapevine leaf spot in China. J Phytopathol 164:75–85CrossRefGoogle Scholar
  40. Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808CrossRefPubMedGoogle Scholar
  41. McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Van Reine WFP, Smith GF, Wiersema JH, Turland NJ (2012) International Code of Nomenclature for algae, fungi, and plants (Melbourne Code). Regnum Vegetabile 154. Koeltz Scientific Books, KönigsteinGoogle Scholar
  42. Motohashi K, Araki I, Nakashima C (2008) Four new species of Phyllosticta, one new species of Pseudocercospora, and one new combination in Passalora from Japan. Mycoscience 49(2):138–146Google Scholar
  43. Nakashima C, Kobayashi T (2000) Addition and reexamination of Japanese species belonging to the genus Cercospora and allied genera. III. Species described by Japanese mycologist (2). Mycoscience 41:25–31CrossRefGoogle Scholar
  44. Nakashima C, Tanda S, Kobayashi T (2002) Addition and reexamination of Japanese species belonging to the genus Cercospora and allied genera. IV. Newly recorded species from Japan (1). Mycoscience 43:95–102CrossRefGoogle Scholar
  45. Nakashima C, Horie H, Kobayashi T (2004) Addition and reexamination of Japanese species belonging to the genus Cercospora and allied genera. VI. Four Pseudocercospora species from Ohshima Island. Mycoscience 45:49–55CrossRefGoogle Scholar
  46. Nakashima C, Araki I, Kobayashi T (2011) Addition and re-examination of Japanese species belonging to the genus Cercospora and allied genera. X: Newly recorded species from Japan (5). Mycoscience 52:253–259CrossRefGoogle Scholar
  47. Park JH, Hong SB, Kim BS, Kim JY, Shin HD (2015) Pseudocercospora leaf spot caused by Pseudocercospora nymphaeacea on Nymphaea tetragona. Trop Plant Pathol 40:401–404CrossRefGoogle Scholar
  48. Parreira DF, da Silva M, Pereira OL, Soares DJ, Barreto RW (2014) Cercosporoid hyphomycetes associated with Tibouchina herbacea (Melastomataceae) in Brazil. Mycol Prog 13:691–702Google Scholar
  49. Phengsintham P, Braun U, McKenzie EHC, Chukeatirote E, Cai L, Hyde KD (2013a) Monograph of cercosporoid fungi from Thailand. Plant Pathol Quar J Fungal Biol 3:19–90Google Scholar
  50. Phengsintham P, Chukeatirote E, McKenzie EHC, Hyde KD, Braun U (2013b) Monograph of cercosporoid fungi from Laos. Curr Res Environ Appl Mycol 3:34–158Google Scholar
  51. Pons N, Sutton BC (1988) Cercospora and similar fungi on yams (Dioscorea species). Mycol Pap 160:1–78Google Scholar
  52. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43CrossRefGoogle Scholar
  53. Ronquist F, Teslenko M, van der Mark P, Ayres D, 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 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  54. Shin HD, Kim JD (2001) Cercospora and allied genera from Korea. Plant Pathogens of Korea 7:1–303Google Scholar
  55. Shivas RG, Marney TS, Tan YP, McTaggart AR (2015) Novel species of Cercospora and Pseudocercospora (Capnodiales, Mycosphaerellaceae) from Australia. Fungal Biol 119:362–369CrossRefPubMedGoogle Scholar
  56. Silva M, Barreto RW, Pereira OL, Freitas NM, Groenewald JZ, Crous PW (2016) Exploring fungal mega-diversity: Pseudocercospora from Brazil. Persoonia 37:142–172Google Scholar
  57. Sung GH, Sung JM, Hywel-Jones NL, Spatafora JW (2007) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 44:1204–1223CrossRefPubMedGoogle Scholar
  58. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  59. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Res 11:914–921CrossRefGoogle Scholar
  61. Togashi K, Katsuki S (1952) New or noteworthy Cercosporae from Japan. Bot Mag Tokyo 65:18–26CrossRefGoogle Scholar
  62. Videira SI, Groenewald JZ, Kolecka A, van Haren L, Boekhout T, Crous PW (2015) Elucidating the Ramularia eucalypti species complex. Persoonia 34:50–64CrossRefPubMedGoogle Scholar
  63. Videira SI, Groenewald JZ, Braun U, Shin HD, Crous PW (2016). All that glitters is not Ramularia. Studies in Mycology 83 doi: 10.1016/j.simyco.2016.06.001
  64. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocol: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  65. Wingfield MJ, De Beer ZW, Slippers B, Wingfield BD, Groenewald JZ, Lombard L, Crous PW (2012) One fungus, one name promotes progressive plant pathology. Mol Plant Pathol 13:604–613CrossRefPubMedGoogle Scholar
  66. Yen JM (1979) Etude sur les champignons parasites du sud-est Asiatique. 33. Les Cercospora de Formose V. Les Pseudocercospora. Bull Soc Mycol Fr 94:386, “1978”Google Scholar
  67. Yen JM, Lim G (1980) Cercospora and allied genera of Singapore and the Malay Peninsula. Gard Bull (Singapore) 33:151–263Google Scholar
  68. Zharkikh A (1994) Estimation of evolutionary distances between nucleotide sequences. J Mol Evol 39:315–329CrossRefPubMedGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Graduate school of BioresourcesMie UniversityMieJapan
  2. 2.Faculty of Regional Environment ScienceTokyo University of AgricultureTokyoJapan
  3. 3.Department of Plant PathologyNational Chung Hsing UniversityTaichungTaiwan
  4. 4.CBS-KNAW Fungal Biodiversity CentreUtrechtThe Netherlands

Personalised recommendations