Fungal Diversity

, 50:121 | Cite as

The evolution of species concepts and species recognition criteria in plant pathogenic fungi

  • Lei Cai
  • Tatiana Giraud
  • Ning Zhang
  • Dominik Begerow
  • Guohong Cai
  • Roger G. Shivas


In this paper, we review historical and contemporary species concepts and species recognition criteria for plant pathogenic fungi. Previous incongruent and unstable classification based on subjective and changing criteria have led to some confusion, especially amongst plant pathologists. The goal of systematics is to provide an informative and robust framework that stands the test of time. The taxonomic histories of Cercospora, Colletotrichum, Fusarium, as well as the rust and smut fungi, are used as examples, to show how concepts and criteria used to delimit and recognize species have changed. Through these examples we compare the Genealogical Concordance Phylogenetic Species Recognition, an extension of the Phylogenetic Species Criterion, with other species recognition criteria and show that it provides a better discrimination for delimiting species. A rapidly increasing number of cryptic species are being discovered amongst plant pathogenic fungi using the Genealogical Concordance Phylogenetic Species Recognition, and it is important to determine their host range, the severity of diseases they cause and their biosecurity significance. With rapidly expanding global trade it has become imperative that we develop effective and reliable protocols to detect these previously unrecognized pathogens.


Cryptic species Species complex Microbotryum Pucciniomycotina Ustilaginomycotina Speciation Taxonomy 


  1. Aguileta G, Marthey S, Chiapello H, Lebrun M-H, Rodolphe F, Fournier E, Gendrault-Jacquemard A, Giraud T (2008) Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol 57:613–627PubMedGoogle Scholar
  2. Aime MC, Matheny PB, Henk DA, Frieders EM, Nilsson RH, Piepenbring M, McLaughlin DJ, Szabo LJ, Begerow D, Sampaio JP, Bauer R, Weiß M, Oberwinkler F, Hibbett DS (2006) An overview of the higher-level classification of Pucciniomycotina based on combined analyses of nuclear large and small subunit rDNA sequences. Mycologia 98:896–905PubMedGoogle Scholar
  3. Anderson JB, Korhonen K, Ullrich RC (1980) Relationships between European and North American biological species of Armillaria mellea. Exp Mycol 4:87–95Google Scholar
  4. Anderson JB, Bailey SS, Pukkia PJ (1989) Variation in ribosomal DNA among biological species of Armillaria, a genus of root-infecting fungi. Evolution 43:1652–1662Google Scholar
  5. Anderson JB, Ullrich RC (1978) Biological species of Armillaria mellea in North America. Mycologia 71:402–414Google Scholar
  6. Aoki T, O’donnell K, Scandiani M (2005) Sudden death syndrome of soybean in South America is caused by four species of Fusarium: Fusarium brasiliense sp. nov., F. cuneirostrum sp. nov., F. tucumaniae, and F. virguliforme. Mycoscience 46:162–183Google Scholar
  7. Aveskamp MM, Gruyter J de, Woudenberg JHC, Verkley GJM, Crous PW (2010) Highlights of the Didymellaceae: a polyphasic approach to characterize Phoma and related pleosporalean genera. Stud Mycol 65:1–60Google Scholar
  8. Baker HG (1947) Infection of species of Melandrium by Ustilao violacea (Pers.) Fuckel and the transmission of the resultant disease. Ann Bot 11:333–348Google Scholar
  9. Bauer R, Oberwinkler F, Vánky K (1997) Ultrastructural markers ans ststematics in smut fungi and allied taxa. Can J Bot 75:1273–1314Google Scholar
  10. Bauer R, Vánky K, Begerow D, Oberwinkler F (1999) Ustilaginomycetes on Selaginella. Mycologia 91:475–484Google Scholar
  11. Bauer R, Begerow D, Sampaio JP, Weiß M, Oberwinkler F (2006) The simple-septate basidiomycetes: a synopsis. Mycol Prog 5:41–66Google Scholar
  12. Begerow D, Bauer R, Oberwinkler F (1997) Phylogenetic studies on the nuclear large subunit ribosomal DNA of smut fungi and related taxa. Can J Bot 75:2045–2056Google Scholar
  13. Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placement of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60Google Scholar
  14. Begerow D, Lutz M, Oberwinkler F (2002) Implications of molecular characters for the phylogeny of the genus Entyloma. Mycol Res 106:1392–1399Google Scholar
  15. Begerow D, Stoll M, Bauer R (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98:906–916PubMedGoogle Scholar
  16. Begerow D, Nilsson H, Unterseher M, Maier W (2010) Current state and perspectives of fungal DNA barcoding and rapid identification procedures. Appl Microbiol Biotechnol 87:99–108Google Scholar
  17. Booth C (1971) The Genus Fusarium. Commonwealth Mycological Institute, Kew, Surrey, England: 1-237.Google Scholar
  18. Braun U (1995) A monograph of Cercosporella, Ramularia and allied genera (Phytopathogenic Hyphomycetes). Vol. 1. IHW-Verlag, Eching bei, München: 1-333Google Scholar
  19. Braun U, Melnik VA (1997) Cercosporoid fungi from Russia and adjacent countries. Russian Academy of Sciences, Proceedings of the Komarov Botanical Institute 20:1–112Google Scholar
  20. Bucheli E, Gautschi B, Shykoff JA (2000) Host-specific differentiation in the anther smut fungus Microbotryum violaceum as revealed by micosatellites. J Evol Biol 13:188–198Google Scholar
  21. Cai L, Hyde KD, Taylor PWJ, Weir B, Waller J, Abang MM, Zhang JZ, Yang YL, Phoulivong S, Liu ZY, Prihastuti H, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers 39:183–204Google Scholar
  22. Cannon PF, Buddie AG, Bridge PD (2008) The typification of Colletotrichum gloeosporioides. Mycotaxon 104:189–204Google Scholar
  23. Cano J, Guarro J, Gene J (2004) Molecular and morphological identification of Colletotrichum species of clinical interest. J Clin Microbiol 42:2450–2454Google Scholar
  24. Carefoot GL, Sprott ER (1967) Famine on the wind. Rand McNally, ChicagoGoogle Scholar
  25. Castlebury LA, Carris LM, Vánky K (2005) Phylogenetic analysis of Tilletia and allied genera in order Tilletiales (Tstilaginomycetes; Exobasidiomycetidae) based on large subunit nuclear rDNA sequences. Mycologia 97:888–900Google Scholar
  26. Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathol 60:2–14Google Scholar
  27. Chupp C (1954) A monograph of the fungus genus Cercospo Ithaca, New York, authorGoogle Scholar
  28. Corda ACI (1831) Die Pilze Deutschlands (ed. J. Sturm). Deutschlands Flora, 3. Abtheilung 3: 1-144Google Scholar
  29. Corlett M (1991) An annotated list of the published names in Mycosphaerella and Sphaerella. Mycol Mem 18:1–328Google Scholar
  30. Covert SF, Aoki T, O’Donnell K, Starkey D, Holliday A, Geiser DM, Cheung F, Town C, Strom A, Juba J, Scandiani M, Yang XB (2007) Sexual reproduction in the soybean sudden death syndrome pathogen Fusarium tucumaniae. Fungal Genet Biol 44:799–807PubMedGoogle Scholar
  31. Coyne J, Orr HA (1997) Patterns of speciation in Drosophila revisited. Evolution 51:295–303Google Scholar
  32. Cracraft J (1983) Species concepts and speciation analysis. In Current Ornithology, Vol. 1, pp. 159–187. Plenum Press, New YorkGoogle Scholar
  33. Crouch JA, Beirn LA (2009) Anthracnose of cereals and grasses. Fungal Divers 39:19–44Google Scholar
  34. Crouch JA, Clarke BB, White JF, Hillman BI (2009) Systematic analysis of falcate-spored graminicolous Colletotrichum and a description of six new species from warm-season grasses. Mycologia 101:717–732PubMedGoogle Scholar
  35. Crous PW, Braun U (1996) Cercosporoid fungi from South Africa. Mycotaxon 57:233–321Google Scholar
  36. Crous PW, Braun U (2003) Mycosphaerella and its anamorphs: 1. Names published in Cercospora and Passalora. CBS Biodiversity Series 1: 1-571Google Scholar
  37. Crous PW, Groenewald JZ (2005) Hosts, species and genotypes: opinions versus data. Australas Plant Pathol 34:463–470Google Scholar
  38. Crous PW, Aptroot A, Kang JC, Braun U, Wingfield MJ (2000) The genus Mycosphaerella and its anamorphs. Stud Mycol 45:107–121Google Scholar
  39. Crous PW, Kang JC, Braun U (2001) A phylogenetic redefinition of anamorph genera in Mycosphaerella based on ITS rDNA sequence and morphology. Mycologia 93(6):1081–1101Google Scholar
  40. Crous PW, Summerell BA, Carnegie AJ, Wingfield MJ, Hunter GC, Burgess TI, Andjic V, Barber PA, Groenewald JZ (2009) Unravelling Mycosphaerella: do you believe in genera? Persoonia 23:99–118PubMedGoogle Scholar
  41. Cummins GB, Hiratsuka Y (2003) Illustrated Genera of Rust Fungi. 3rd ed. APS Press. The American Phythopathological Society. St. Paul, MinnesotaGoogle Scholar
  42. Damm U, Woudenberg JHC, Cannon PF, Crous PW (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers 39:45–87Google Scholar
  43. de Bary HA (1853) Untersuchungen über die Brandpilze und die durch sie verursachten Krankheiten der Pflanzen mit Rücksicht auf das Getreide und andere Nutzpflanzen. Habilitationsschrift.Google Scholar
  44. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):879–886PubMedGoogle Scholar
  45. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford Univ. Press, New York, pp 57–75Google Scholar
  46. de Vienne DM, Refrégier G, Hood ME, Guigue A, Devier B, Vercken E, Smadja C, Deseille A, Giraud T (2009a) Hybrid sterility and inviability in the parasitic fungal species complex Microbotryum. J Evol Biol 22:683–698PubMedGoogle Scholar
  47. de Vienne D, Hood M, Giraud T (2009b) Phylogenetic determinants of potential host shifts in fungal pathogens. J Evol Biol 22:2532–2541PubMedGoogle Scholar
  48. Deighton FC (1967) Studies on Cercospora and allied genera. II. Passalora, Cercosporidium, and some species of Fusicladium on Euphorbia. Mycological Papers 112:1–80Google Scholar
  49. Deighton FC (1973) Studies on Cercospora and allied genera. IV. Cercosporella Sacc., Pseudocercosporella gen. nov. and Pseudocercosporidium gen. nov. Mycological Papers 133:1–62Google Scholar
  50. Deighton FC (1976) Studies on Cercospora and allied genera. VI. Pseudocercospora Speg., Pantospora Cif. and Cercoseptoria. Mycological Papers 140:1–168Google Scholar
  51. Deighton FC (1979) Studies on Cercospora and allied genera. VII. New species and redispositions. Mycological Papers 144:1–56Google Scholar
  52. Dettman JR, Jacobson DJ, Taylor JW (2003a) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720PubMedGoogle Scholar
  53. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003b) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution 57:2721–2741PubMedGoogle Scholar
  54. Dignani MC, Anaissie E (2004) Human fusariosis. Clin Microbiol Infect 10:67–75PubMedGoogle Scholar
  55. Fajola AO (1978) Cultural studies in Cercospora taxonomy: I. Interrelationships between some species from Nigeria. Nova Hedwigia 29:912–921Google Scholar
  56. Fischer von Waldheim A (1869) Beiträge zur biologie und Entwicklungsgeschichte der Ustilagineen. Jahrbuch für wissenschaftliche Botanik 7:61–144Google Scholar
  57. Fishman L, Wyatt R (1999) Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723–1733Google Scholar
  58. Fournier E, Giraud T, Albertini C, Brygoo Y (2005) Partition of the Botrytis cinerea complex in France using multiple gene genealogies. Mycologia 97:1251–1267PubMedGoogle Scholar
  59. Fries E (1821) Systema mycologicum 1. Gryphiswaldae, MauritiusGoogle Scholar
  60. Fuckel KWGL (1863) Fungi rhenani exiccati, Fasc. I–IV. Hedwigia 2:132–136Google Scholar
  61. Gao X, Jackson TA, Lambert KN, Li S, Hartman GL, Niblack TL (2004) Detection and quantification of Fusarium solani f. sp glycines in soybean roots with real-time quantitative polymerase chain reaction. Plant Disease 88:1372–1380Google Scholar
  62. Gaümann E (1959) Die Rostpilze Mitteleuropas. Bücheler, BernGoogle Scholar
  63. Geiser DM, Jimenez-Gasco MD, Kang SC, 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 110:473–479Google Scholar
  64. Giraud T (2006) Selection against migrant pathogens: the immigrant inviability barrier in pathogens. Heredity 97:316–318PubMedGoogle Scholar
  65. Giraud T, Villaréal LMMA, Austerlitz F, Gac ML, Lavigne C (2006) Importance of the life cycle in host race formation and sympatric speciation in parasites. Phytopathology 96:280–287PubMedGoogle Scholar
  66. Giraud T, Refrégier G, de Vienne DM, Le Gac M, Hood ME (2008a) Speciation in fungi. Fungal Genet Biol 45:791–802PubMedGoogle Scholar
  67. Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME (2008b) Mating system of the anther smut fungus, Microbotryum violaceum. Eukaryotic Cell 7:765–775PubMedGoogle Scholar
  68. Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 25:387–395PubMedGoogle Scholar
  69. Gladieux P, Byrnes E, Fisher M, Aguileta G, Heitman J, GiraudT. (2010) Epidemiology and evolution of fungal pathogens, in plants and animals in T. M., ed. Genetics and Evolution of Infectious Diseases. ElsevierGoogle Scholar
  70. Gladieux P, Vercken E, Fontaine MC, Hood ME, Jonot O, Couloux A, Giraud T (2011) Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28:459–471PubMedGoogle Scholar
  71. Glienke C, Pereira OL, Stringari D, Fabris J, Kava-Cordeiro V, Galli-Terasawa L, Cunnington J, Shivas RG, Groenewald JZ, Crous PW (2011) Endophytic and pathogenic Phyllosticta species, with reference to those associated with Citrus Black Spot. Persoonia 26:47–56Google Scholar
  72. Goodwin SB, Dunkle LD, Dunkle LD, Zismann VL (2001) Phylogenetic analysis of Cercospora and Mycosphaerella based on the internal transcribed spacer region of ribosomal DNA. Phytopathology 91(7):648–658PubMedGoogle Scholar
  73. Groenewald M, Groenewald JZ, Crous PW (2005) Distinct species exist within the Cercospora apii morphotype. Phytopathology 95(8):951–959PubMedGoogle Scholar
  74. Groenewald M, Groenewald JZ, Braun U, Crous PW (2006a) Host range of Cercospora apii and C. beticola and description of C. apiicola, a novel species from celery. Mycologia 98(2):275–285PubMedGoogle Scholar
  75. Groenewald M, Groenewald JZ, Harrington TC, Abeln ECA, Crous PW (2006b) Mating type gene analysis in apparently asexual Cercospora species is suggestive of cryptic sex. Fungal Genet Biol 43(12):813–825PubMedGoogle Scholar
  76. Guo YL, Hsieh WH (1995) The genus Pseudocercospora in China. Mycosystema Monographicum Series 2:1–388Google Scholar
  77. Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655Google Scholar
  78. Hendrichs M, Begerow D, Bauer R, Oberwinkler F (2005) The genus Anthracoidea (Basidiomycota, Ustilaginales): A molecular phylogenetic approach using LSU rDNA sequences. Mycol Res 109:31–40Google Scholar
  79. Hey J (2006) On the failure of modern species concepts. Trends Ecol Evol 21:447–450PubMedGoogle Scholar
  80. Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Lumbsch HT, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai Y-C, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson K-H, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo J-M, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüßler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao Y-J, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547PubMedGoogle Scholar
  81. Hsieh WH, Goh TK (1990) Cercospora species and similar fungi from Taiwan. Maw Chang Book Company, TaiwanGoogle Scholar
  82. Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H (2009a) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17Google Scholar
  83. Hyde KD, Cai L, Cannon PF, Crouch JA, Crous PW, Damm U, Goodwin PH, Chen H, Johnston PR, Jones EBG, Liu ZY, McKenzie EHC, Moriwaki J, Noireung P, Pennycook SR, Pfenning LH, Prihastuti H, Sato T, Shivas RG, Taylor PWJ, Tan YP, Weir BS, Yang YL, Zhang JZ (2009b) Colletotrichum - names in current use. Fungal Divers 39:147–182Google Scholar
  84. Hyde KD, Chomnunti P, Crous PW, Groenewald JZ, Damm U, KoKo TW, Shivas RG, Summerell BA, Tan YP (2010) A case for re-inventory of Australia’s plant pathogens. Persoonia 25:50–60PubMedGoogle Scholar
  85. James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom Schizophyllum commune. Evolution 53:1665–1677Google Scholar
  86. Johnson EM, Valleau WD (1949) Synonomy in some common species of Cercospora. Phytopathology 39:763–770Google Scholar
  87. Johnson JA, Harrington TC, Engelbrecht CJB (2005) Phylogeny and taxonomy of the North American clade of the Ceratocystis fimbriata complex. Mycologia 97:1067–1092PubMedGoogle Scholar
  88. Jülich W (1981) Higher taxa of basidiomycetes. Bibliotheca Mycologia 85:1–485Google Scholar
  89. Kirk AM, Cannon PF, David JC, Stalpers JA (2001) Dictionary of the Fungi, 9th edn. CABI Publishing, UKGoogle Scholar
  90. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi. (10th ed.). CAB InternationalGoogle Scholar
  91. Kiss L, Pintye A, Kovács GM, Jankovics T, Fongtaine MC, Harvey N, Xu X, Nicot PC, Bardin M, Shykoff JA, Giraud T (2011) Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Mol Ecol 20:1492–1507PubMedGoogle Scholar
  92. Kohn LM (2005) Mechanisms of fungal speciation. Annu Rev Phytopathol 43:279–308PubMedGoogle Scholar
  93. Koufopanou V, Burt A, Szaro T, Taylor JW (2001) Gene genealogies, cryptic species, and molecular evolution in the human pathogen Coccidioides immitis and relatives (Ascomycota, Onygenales). Mol Biol Evol 18:1246–1258PubMedGoogle Scholar
  94. Kuehne HA, Murphy HA, Francis CA, Sniegowski PD (2007) Allopatric divergence, secondary contact and genetic isolation in wild yeast populations. Curr Biol 17:407–411PubMedGoogle Scholar
  95. Kumar DSS, Hyde KD (2004) Biodiversity and tissue-recurrence of endophytic fungi from Tripterygium wilfordii. Fungal Divers 17:69–90Google Scholar
  96. Kvas M, Marasas WFO, Wingfield BD, Wingfield MJ, Steenkamp ET (2009) Diversity and evolution of Fusarium species in the Gibberella fujikuroi complex. Fungal Divers 34:1–21Google Scholar
  97. Le Gac M, Hood ME, Fournier E, Giraud T (2007a) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61:15–26PubMedGoogle Scholar
  98. Le Gac M, Hood ME, Giraud T (2007b) Evolution of reproductive isolation within a parasitic fungal complex. Evolution 61:1781–1787PubMedGoogle Scholar
  99. Le Gac M, Giraud T (2008) Existence of a pattern of reproductive character displacement in Basidiomycota but not in Ascomycota. J Evol Biol 21:761–772PubMedGoogle Scholar
  100. Leslie JF, Summerell BA (2006) The Fusarium laboratory manual. Blackwell, IowaGoogle Scholar
  101. Levy L, Castlebury LA, Carris LM, Meyer RJ, Pimentel G (2001) Internal transcribed spacer sequence-based phylogeny and polymerase chain reaction-restriction fragment length polymorphism differentiation of Tilletia walkeri and T. indica. Phytopathology 91:935–940PubMedGoogle Scholar
  102. Link HF (1809) Observationes in ordines plantarum naturales. Dissertatio I. Gesellschaft der Naturforschenden Freunde Berlin, Magazin der Neuesten Entdeckungen in der gesammten. Naturkunde 3:3–42Google Scholar
  103. Liro JL (1924) Die Ustilagineen Finnlands I. Ann Acad Sci Fenn A 17:1–636Google Scholar
  104. Liu XY, Duan JX, Xie XM (2007) Colletotrichum yunnanense sp. nov., a new endophytic species from Buxus sp. Mycotaxon 100:137–144Google Scholar
  105. Lutz M, Göker M, Piatek M, Kemler M, Begerow D, Oberwinkler F (2005) Anther smuts of Caryophyllaceae: molecular characters indicate host-dependent species delimitation. Mycol Prog 4:225–238Google Scholar
  106. Lutz M, Piatek M, Kemler M, Chlebicki A, Oberwinkler F (2008) Anther smuts of Caryophyllaceae: molecular analyses reveal further new species. Mycol Res 112:1280–1296Google Scholar
  107. Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny of the rust fungi: an approach using nuclear large subunit ribosomal DNA sequences. Can J Bot 81:12–23Google Scholar
  108. Marasas WFO, Nelson PE, Toussoun TA (1984) Toxigenic Fusarium species: identity and mycotoxicology. Pennsylvania State University Press, University ParkGoogle Scholar
  109. Matuo T, Snyder WC (1973) Use of morphology and mating populations in the identification of formae speciales in Fusarium solani. Phytopathology 63:562–565Google Scholar
  110. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  111. McTaggart AR (2010) Systematics of the Ustilato-Sporisorium-Macalpinomyces complex of smut fungi. PhD thesis. Queensland University of Technology, Brisbane, Australia.Google Scholar
  112. Micheli PA (1729) Nova plantarum genera. Firenze: Bernardo Paperini: 1-234Google Scholar
  113. Nelson PE, Tousson TA, Marasas WFO (1983) Fusarium species: an illustrated manual for identification. Pennylvania State University Press, University ParkGoogle Scholar
  114. O’Donnell K (2000) Molecular phylogeny of the Nectria haematococca-Fusarium solani species complex. Mycologia 92:919–938Google Scholar
  115. O’Donnell K, Cigelnik E, Nirenberg HI (1998) Molecular systematics and phylogeography of the Gibberella fujikuroi species complex. Mycologia 90:465–493Google Scholar
  116. O’Donnell K, Kisler HC, Tacke BK, Casper HH (2000) Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc Natl Acad Sci USA 97:7905–7910PubMedGoogle Scholar
  117. O’Donnell K, Ward TJ, Geiser DM, Corby Kistler H, Aoki T (2004) Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet Biol 41:600–623PubMedGoogle Scholar
  118. Park B, Park J, Cheong KC, Choi J, Jung K, Kim D, Lee YH, Ward TJ, O’Donnell K, Geiser DM, Kang S (2011) Cyber infrastructure for Fusarium: three integrated platforms supporting strain identification, phylogenetics, comparative genomics and knowledge sharing. Nucleic Acids Res 39:D640–D646PubMedGoogle Scholar
  119. Pascoe IG, Priest MJ, Shivas RG, Cunnington JH (2005) Spores of Tilletia ehrhartae, a smut of Ehrharta calycina, are common contaminants of Australian wheat grain, and a potential source of confusion with Tilletia indica, the cause of Karnal bunt of wheat. Plant Pathol 54:161–168Google Scholar
  120. Peever T (2007) Role of host specificity in the speciation of Ascochyta pathogens of cool season food legumes. Eur J Plant Pathol 119:119–126Google Scholar
  121. Perlin MH (1996) Pathovars of Formae speziales of Microbotryum violaceum differ in electrophoretic karyotype. Int J Plant Sci 157:447–452Google Scholar
  122. Persoon CH (1801) Synopsis methodica fungorum. Apud Henricum Dieterich, Gottingae, pp 1–708Google Scholar
  123. Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic fungi of wild banana (Musaacuminata) at Doi Suthep Pui National Park, Thailand. Mycol Res 105:1508–1513Google Scholar
  124. Photita W, Lumyong S, Lumyong P, McKenzieEHC HKD (2003) Saprobic fungi on dead wild banana. Mycotaxon 85:345–356Google Scholar
  125. Photita W, Taylor PWJ, Ford R, Hyde KD, Lumyong S (2005) Morphological and molecular characterization of Colletotrichum species from herbaceous plants in Thailand. Fungal Divers 18:117–133Google Scholar
  126. 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 44:33–43Google Scholar
  127. Pollack FG (1987) An annotated compilation of Cercospora names. Mycol Mem 12:1–212Google Scholar
  128. Pons N, Sutton BC (1988) Cercospora and similar fungi on yams (Dioscorea spp.). Mycol Papers 160:1–78Google Scholar
  129. Prévost IB (1807) Memoire sur la cause immédiate de la carie. MontaubanGoogle Scholar
  130. Prihastuti H, Cai L, Chen H, Hyde KD (2009) Characterization of Colletotrichum species associated with coffee berries in Chiang Mai, Thailand. Fungal Divers 39:89–109Google Scholar
  131. Pringle A, Baker DM, Platt JK, Wares JP, Latgé JP, Taylor JW (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59:1886–1899PubMedGoogle Scholar
  132. Reynolds DR (1993) The fungal holomorph: an overview. In: Reynolds DR, Taylor JW (eds) The fungal Holomorph: Mitotic, Meiotic and Pleomorphic Speciation in Fungal Systematics. CAB International, Wallingford, pp 15–25Google Scholar
  133. Rossman AY, Palm-Hernández ME (2008) Systematics of plant pathogenic fungi: why it matters. Plant Dis 92:1376–1386Google Scholar
  134. Rupe JC (1989) Frequency and pathogenicity of Fusarium solani recovered from soybeans with Sudden-Death Syndrome. Plant Dis 73:581–584Google Scholar
  135. Seier MK, Morin L, van der Merwe M, Evans HC, Romero Á (2009) Are the microcyclic rust species Puccinia melampodii and Puccinia xanthii conspecific. Mycol Res 113:1271–1282PubMedGoogle Scholar
  136. Shivas RG, Hyde KD (1997) Biodiversity of plant pathogenic fungi in the tropics. In: Hyde KD (ed) Biodiversity of tropical microfungi. Hong Kong University Press, Hong Kong, pp 47–56Google Scholar
  137. Shivas RG, Tan YP (2009) A taxonomic re-assessment of Colletotrichum acutatum, introducing C. fioriniae comb. et stat. nov. and C. simmondsii sp. nov. Fungal Divers 39:111–122Google Scholar
  138. Schubert K, Groenewald JZ, Braun U, Dijksterhuis J, Starink M, Hill CF, Zalar P, de Hong GS, Crous PW (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Stud Mycol 58:105–156Google Scholar
  139. Snyder WC, Hansen HN (1941) The species concept in Fusarium with reference to section Martiella. Am J Bot 28:738–742Google Scholar
  140. Snyder WC, Hansen HN (1945) The species concept in Fusarium with reference to Discolor and other sections. Am J Bot 32:657–666Google Scholar
  141. Starkey DE, Ward TJ, Aoki T, Gale LR, Kisler HC (2007) Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet Biol 44:1191–1204PubMedGoogle Scholar
  142. Stewart EL, Liu ZW, Crous PW, Szabo LJ (1999) Phylogenetic relationships among some cercosporoid anamorphs of Mycosphaerella based on rDNA sequence analysis. Mycol Res 103:1491–1499Google Scholar
  143. Stoll M, Piepenbring M, Begerow D, Oberwinkler F (2003) Molecular phylogeny of Ustilago and Sporisorium species (Basidiomycota, Ustilaginales) based on internal transcribed spacer (ITS) sequences. Can J Bot 81:976–984Google Scholar
  144. Stoll M, Begerow D, Oberwinkler F (2005) Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109:342–356Google Scholar
  145. Su YY, Noireung P, Liu F, Hyde KD, Moslem MA, Bahkalii AH, Abe-Elsalam KA, Cai L (2011) Epitypification of Colletotrichum musae, the causative agent of banana anthracnose. Mycosciense. doi:10.1007/s10267-011-0120-9
  146. Summerell BA, Laurence MH, Liew ECY, Leslie JF (2010) Biogeography and phylogeography of Fusarium: a review. Fungal Divers 44:3–13Google Scholar
  147. Sutton BC (1980) The coelomycetes. Commonwealth Mycological Institute, Kew, pp 1–696Google Scholar
  148. Sutton BC (1992) The genus Glomerella and its anamorph Colletotrichum. In: Bailey JA, Jeger MJ (eds) Colletotrichum: biology, pathology and control. CAB International, Wallingford, pp 1–26Google Scholar
  149. Taylor JW, Jacobson DJ, Fisher MC (1999) The evolution of asexual fungi: Reproduction, speciation and classification. Annu Rev Phytopathol 37:197–246PubMedGoogle Scholar
  150. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32PubMedGoogle Scholar
  151. Taylor JW, Turber E, Townsend JP, Dettman JR, Jacobson D (2006) Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi. Phil Trans R Soc B Biol Sci 361:1947–1963Google Scholar
  152. Tessmann DJ, Charudattan R, Kistler HC, Rosskopf EN (2001) A molecular characterization of Cercospora species pathogenic to water hyacinth and emendation of C-piaropi. Mycologia 93(2):323–334Google Scholar
  153. Tharp BC (1917) Texas parasitic fungi. Mycologia 9:105–124Google Scholar
  154. Tillet M (1755) Dissertation sur la cause qui corrompt et noircit le bled dans les épis; et sur les moyens de prévenir ces accidens. BordeauxGoogle Scholar
  155. To-Anun C, Hidayat I, Meeboon J (2011) Genus Cercospora in Thailand: taxonomy and phylogeny (with a dichotomous key to species). Plant Pathology & Quarantine 1:11–87Google Scholar
  156. Tode HJ (1790) Fungi Mecklenbergensis Selecti 1: 1-64Google Scholar
  157. Toussoun TA, Nelson PE (1975) Variation and speciation in the fusaria. Annu Rev Phytopathol 13:71–82Google Scholar
  158. Tulasne LR, Tulasne C (1847) Mémoire sur les Ustilaginées comparées aux Uredinées. Annales des Sciences Naturelles. Botanique et Biologie Végétale 3:12–126Google Scholar
  159. van Putten WH, Elzinga JA, Biere A (2007) Host fidelity of the pollinator guilds of Silene dioica and Silene latifolia: possible consequences for sympatric host race differentiation of a vectored plant disease. Int J Plant Sci 168:421–434Google Scholar
  160. Vánky K (2002) Illustrated Genera of Smut Fungi. APS Press, MinnesotaGoogle Scholar
  161. Vánky K (2003) The smut fungi (ustilaginomycetes) of Sporobolus (Poaceae). Fungal Divers 14:205–241Google Scholar
  162. Vánky K (2006) The smut fungi (Ustilaginomycetes) of Restionaceae s. lat. Mycol Balc 3:19–46Google Scholar
  163. Vanky K, Lutz M (2007) Revision of some Thecaphora species (Ustilaginomycotina) on Caryophyllaceae. Mycol Res 111:1207–1219Google Scholar
  164. Vestal EF (1933) Pathogenicity, host response and control of Cercospora leaf spot of sugar beet. Iowa Agric Exp Stn Res Bull 168:43–72Google Scholar
  165. von Arx JA (1957) Die Arten der Gattung Colletotrichum Cda. Phytopathologische Zeitschrift 29:414–468Google Scholar
  166. Waller JM, Bridge PD, Black R, Hakiza G (1993) Characterization of the coffee berry disease pathogen. Colletotrichum kahawae sp. nov. Mycol Res 97:989–994Google Scholar
  167. Weir BS, Johnston PR (2010) Characterisation and neotypification of Gloeosporium kaki Hori as Colletotrichum horii nom. nov. Mycotaxon 111:209–219Google Scholar
  168. Wollenweber HW, Reinking OA (1935) Die Fusarien, ihre Beschreiburg, Schadwirkung, ud Bekampfung. Verlag Paul Parey, Berlin, pp 1–335Google Scholar
  169. Wulandari NF, To-anun C, Hyde KD, Duong LM, de Gruyter J, Meffert JP, Groenewald JZ, Crous PW (2009) Phyllosticta citriasiana sp. nov., the cause of Citrus tan spot of Citrus maxima in Asia. Fungal Divers 34:23–39Google Scholar
  170. Yamaoka Y (2002) Artificial culture of rust fungi. Yet-to-be-cultured microorganisms and culture collections: 14-17 (in Japanese)Google Scholar
  171. Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DM (2006) Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 44:2186–2190PubMedGoogle Scholar
  172. Zillig H (1921) Über spezialisierte Formen beim Antherenbrand, Ustilago violacea (Pers.) Tuck. Zentralbl Bakteriol II 53:33–74Google Scholar

Copyright information

© Kevin D. Hyde 2011

Authors and Affiliations

  • Lei Cai
    • 1
  • Tatiana Giraud
    • 2
  • Ning Zhang
    • 3
  • Dominik Begerow
    • 4
  • Guohong Cai
    • 3
  • Roger G. Shivas
    • 5
  1. 1.State Key Laboratory of MycologyInstitute of Microbiology, Chinese Academy of SciencesBeijingPeople’s Republic of China
  2. 2.Ecologie, Systématique et EvolutionOrsay cedexFrance
  3. 3.Department of Plant Biology and Pathology, RutgersThe State University of New JerseyNew BrunswickUSA
  4. 4.Ruhr-Universität BochumBochumGermany
  5. 5.Plant Pathology HerbariumAgri-Science QueenslandDutton ParkAustralia

Personalised recommendations