Fungal Diversity

, Volume 51, Issue 1, pp 279–296 | Cite as

Major clades in tropical Agaricus

  • Ruilin Zhao
  • Samantha Karunarathna
  • Olivier Raspé
  • Luis A. Parra
  • Jacques Guinberteau
  • Magalie Moinard
  • André De Kesel
  • Gérard Barroso
  • Régis Courtecuisse
  • Kevin D. Hyde
  • Atsu K. Guelly
  • Dennis E. Desjardin
  • Philippe Callac


Agaricus (Basidiomycota) is a genus of saprobic fungi that includes edible cultivated species such as Agaricus bisporus, the button mushroom. There has been considerable ecological, nutritional and medicinal interest in the genus, yet the extent of its diversity remains poorly known, particularly in subtropical and tropical areas. Classification of tropical species has for a large part followed the classification of temperate species. The objective of our study was to examine to what extent this system of classification is appropriate for tropical Agaricus species. Species from temperate sections were therefore compared to the major clades of tropical species using a phylogenetic approach. ITS1 + 2 sequence data from 128 species were used in the phylogenetic analysis. Specimens included four species of genera closely related to Agaricus, 38 temperate species representing the eight classical sections of the genus, and 86 putative species of Agaricus from tropical areas of Africa, Asia and the Americas. Bayesian and maximum likelihood analyses produced relatively congruent trees and almost identical clades. Our data show that (i) only about one-third of tropical species belong to the classical sections based on temperate species; the systematics of the genus therefore needs to be expanded; (ii) among the remaining two-thirds of tropical species, those from the Americas and those from Africa and/or Asia group in distinct clades, suggesting that secondary diversification occurred in these two areas; (iii) in contrast, several clades of classical sections contain American and African + Asian species along with temperate species. In this study, we used approximately 50 distinct species from a small area of northern Thailand, most probably being novel species. This diversity indicates that Agaricus is a species-rich genus in the tropics as well as in temperate regions. The number of species and the hypothetical paleotropical origin of the genus are discussed.


Agaricus Basidiomycota Tropical biodiversity Biogeography ITS Phylogeny 



The authors are grateful to Jean-Pierre Fiard, Else Vellinga, Gerardo Mata, Marina Capelari, Marc-André Lachance, Rick Kerrigan, Peter Wenzel, Dario De Franceschi, Vincent Lefort, Stephane Welti and Saturnino (Nino) Santamaría. This work was supported by an Integration Research Grant from the European Distributed Institute of Taxonomy (EDIT).

The National Science Foundation (USA) (PEET-grant DEB-0118776 to Desjardin), the National Natural Science Foundation of China (Project ID: 31000013), and the project “value added products from Basidiomycetes: Putting Thailand’s biodiversity to use” (BRN049/2553) are thanked for providing partial support to this research. The Global Research Network for Fungal Biology and King Saud University are also thanked for support.


  1. Angeli JPF, Ribeiro R, Gonzaga MLC, Soares S de A, Ricardo MPSN, Tsuboy MS, Stidl R, Knasmueller S, Linhares RE, Mantovani MS (2006) Protective effects of β-glucan extracted from Agaricus brasiliensis against chemically induced DNA damage in human lymphocytes. Cell Biol Toxicol 22:285–291Google Scholar
  2. Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: A fast, accurate and powerful alternative. Syst Biol 55:539–52PubMedCrossRefGoogle Scholar
  3. Bas C (1991) A short introduction to the ecology, taxonomy and nomenclature of the genus Agaricus. In: Van Grievsen LJLD (ed) Genetics and breeding of Agaricus. Proceedings of the First International Seminar on Mushroom Science. Pudoe Wageningen pp 21–24Google Scholar
  4. Baker RED, Dale WT (1951) Fungi of Trinidad & and Tobago. Mycol Papers 33:1–123Google Scholar
  5. Berkeley MJ, Broome CE (1871) The fingi of Ceylon (Hymenomycetes from Agaricus to Cantharellus. J Linn Soc 9:494–567Google Scholar
  6. Bernarshaw S, Lyberg T, Hetland G, Johnson E (2007) Effect of an extract of the mushroom Agaricus blazei Murill on expression of adhesion molecular and production of reactive oxygen species in monocytes and granulocytes in human whole blood ec vivo Acta Pathologica. Microbiol Immunol 115(6):719–725Google Scholar
  7. Callac P, Billette C, Imbernon M, Kerrigan RW (1993) Morphological, genetic, and interfertility analyses reveal a novel, tetrasporic variety of Agaricus bisporus from the Sonoran desert of California. Mycologia 85:835–851CrossRefGoogle Scholar
  8. Capelari M, Rosa LH, Lachance M-A (2006) Description and affinities of Agaricus martineziensis, a rare species. Fungal Diversity 21:11–18Google Scholar
  9. Challen MP, Kerrigan RW, Callac P (2003) A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae. Mycologia 95(1):61–73PubMedCrossRefGoogle Scholar
  10. Chevenet F, Brun C, Banuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees BMC. Bioinformatics 7:439PubMedGoogle Scholar
  11. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  12. Geml J, Geiser DM, Royse DJ (2004) Molecular evolution of Agaricus species based on IST and LSU rDNA sequences. Mycol Prog 3(2):157–176CrossRefGoogle Scholar
  13. Geml J, Laursen GA, Taylor DL (2008) Molecular diversity assessment of artic and boreal Agaricus taxa. Mycologia 100(4):577–589PubMedCrossRefGoogle Scholar
  14. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  15. Hama O, Maes E, Guissou M-L, Ibrahim DM, Barage M, Parra LA, Raspé O, De Kesel A (2010) Agaricus subsaharianus, une nouvelle espèce comestible et consommée au Niger, au Burkina Faso et en Tanzanie. Cryptogamie, Mycologie 31:221–234Google Scholar
  16. Heinemann P (1956a) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II Agaricus Fr ss. Bull Jard Bot État 26:1–127CrossRefGoogle Scholar
  17. Heinemann P (1956b) Flore Iconographique des Champignons du Congo, 5º fascicule : Agaricus I. Ministère de l’Agriculture-Jardin Botanique de l’État BruxellesGoogle Scholar
  18. Heinemann P (1956c) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II Agaricus, Note complémentaire. Bull Jard Bot État 26:325–333CrossRefGoogle Scholar
  19. Heinemann P (1957) Flore Iconographique des Champignons du Congo, 6º fascicule : Agaricus II et Pilosace. Ministère de l’Agriculture-Jardin Botanique de l’État BruxellesGoogle Scholar
  20. Heinemann P (1961) Agarici Austro-Americani I Agaricus of Trinidad. Kew Bull 15:231–248CrossRefGoogle Scholar
  21. Heinemann P (1962a) Agarici Austro-Americani II Agaricus de Bolivie. Bull Jard Bot État 32:1–21CrossRefGoogle Scholar
  22. Heinemann P (1962b) Agarici Austro-Americani III Trois Agaricus de la Jamaïque. Bull Jard Bot État 32:23–28CrossRefGoogle Scholar
  23. Heinemann P (1962c) Agarici Austro-Americani IV Quatre Agaricus de Venezuela. Bull Jard Bot État 32:155–161CrossRefGoogle Scholar
  24. Heinemann P (1971) Quelques Psalliotes du Congo-Brazzaville. Cah Maboké 9:5–10Google Scholar
  25. Heinemann P (1978) Essai d’une clé de determination des genres Agaricus et Micropsalliota. Sydowia 30:6–37Google Scholar
  26. Heinemann P (1980) Les genres Agaricus et Micropsalliota en Malaisie et en Indonésie. Bull Jard Bot Belg 50:3–68CrossRefGoogle Scholar
  27. Heinemann P (1982) Quelques Psalliotes de Nouvelle Guinée (Papua New Guinea). Bull Jard Bot Belg 52:405–413CrossRefGoogle Scholar
  28. Heinemann P (1984) Agarici Austro-Americani VII. Agariceae des zones tempérées de l’Argentine et du Chili. Bull Jard Bot Belg 60:331–370CrossRefGoogle Scholar
  29. Heinemann P (1988) Novitates generis Micropsalliotae (Agaricaceae). Bull Jard Bot Belg 60:540–543CrossRefGoogle Scholar
  30. Heinemann P (1990) Agaricus singaporensis sp. nov. Bull Jard Bot Belg 60:417–419CrossRefGoogle Scholar
  31. Heinemann P (1993) Agarici Austro-Americani VIII Agaricaceae des régions intertropicales d’Amérique du Sud. Bull Jard Bot Belg 62:355–384CrossRefGoogle Scholar
  32. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  33. Kerrigan RW (2005) Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia 97(1):12–24PubMedCrossRefGoogle Scholar
  34. Kerrigan RW (2007) Lectotypification of Agaricus brunnescens. Mycologia 99(6):906–915PubMedCrossRefGoogle Scholar
  35. Kerrigan RW, Callac P, Challen M, Guinberteau J, Parra LA (2006 “2005”) Agaricus section Xanthodermatei: a phylogenetic reconstruction with commentary on taxa. Mycologia 97(6):1292–1315Google Scholar
  36. Kerrigan RW, Callac P, Parra LA (2008) New and rare taxa in Agaricus section Bivelares (Duploannulati). Mycologia 100(6):876–892PubMedCrossRefGoogle Scholar
  37. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, Tenthth edn. CABI publishing, WallingfordGoogle Scholar
  38. Largeteau ML, Callac P, Navarro-Rodriguez A-M, Savoie J-M (2011) Diversity in the ability of Agaricus bisporus wild isolates to fruit at high temperature (25°C). Fungal Biology, doi: 10.1016/j.funbio.2011.08.004
  39. Moncalvo JM, Vilgalys R, Redhead SA, Johnson JE, James TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E, Baroni TJ, Thorn RG, Jacobsson S, Clémencon H, Miller OK Jr (2002) One hundred seventeen clades of Euagarics. Mol Phylogen Evo l23:357–400CrossRefGoogle Scholar
  40. Murrill WA (1918) Agaricaceae of tropical North America VIII. Mycologia 10:62–85CrossRefGoogle Scholar
  41. Murrill WA (1942) New fungi from Florida. Lloydia 5(2):136–157Google Scholar
  42. Murrill WA (1945) New Florida fungi. Quart J Florida Acad Sci 8(2):175–198Google Scholar
  43. Murrill WA (1946) New and interesting Florida fungi. Lloydia 9(4):315–330Google Scholar
  44. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for multiple sequence alignments. J Mol Biol 302:205–217PubMedCrossRefGoogle Scholar
  45. Parra LA (2008) Agaricus L Allopsalliota Nauta & Bas. Pars 1 Edizioni Candusso Alassio, ItalyGoogle Scholar
  46. Parra LA, Villarreal M, Esteve-Raventos F (2002) Agaricus endoxanthus una specie tropicale trovata in Spagna. Rivista Micol 45(3):225–233Google Scholar
  47. Pegler DN (1966) Tropical African Agaricales. Persoonia 4(2):73–124Google Scholar
  48. Pegler DN (1968) Studies on African Agaricales I. Kew Bull 21:499–533CrossRefGoogle Scholar
  49. Pegler DN (1969) Studies on African Agaricales II. Kew Bull 23:219–249CrossRefGoogle Scholar
  50. Pegler DN (1977) A preliminary Agaric flora of east Africa. Kew Bull Add Series 6:1–615Google Scholar
  51. Pegler DN (1983) Agaric flora of the Lesser Antilles. Kew Bull Add Series 9:1–667Google Scholar
  52. Pegler DN (1986) Agaric flora of Sri Lanka. Kew Bull Add Series 12:1–519Google Scholar
  53. Pegler DN, Rayner RW (1969) A contribution to the Agaric flora of Kenya. Kew Bull 23:347–412CrossRefGoogle Scholar
  54. Peterson KR, Desjardin ED, Hemmes DE (2000) Agaricales of the Hawaiian Islands. 6. Agaricxaceae I. Agariceae: Agaricus and Melanophyllum. Sydowia 52(2):204–257Google Scholar
  55. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  56. Rambaut A, Drummond AJ (2007) Tracer v1.5, Available from
  57. Rick J (1906) Pilze aus Rio Grande do Sul (Brazilien). Broteria 5:5–53Google Scholar
  58. Rick J (1919) Contributio II ad monographiam Agaricinorum Brasiliensium. Broteriaser Bot 17:101–111Google Scholar
  59. Rick J (1920) Contributio ad monographiam Agaricinorum Brasiliensium. Broteria ser Bot 18:48–63Google Scholar
  60. Rick J (1930) Contributio IV ad monographiam Agaricinorum Brasiliensium. Broteria ser Bot 24:97–118Google Scholar
  61. Rick J (1939) Agarici Riograndenses IV. Lilloa 4(1):75–104Google Scholar
  62. Rick J (1961) Basidiomycetes Eubasidii in Rio Grande do Sul—Brasilia 5 Agaricaceae. Iheringia ser Bot 8:296–450Google Scholar
  63. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  64. Saghai-Maroof MA, Solima KM, Jorgenson RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018PubMedCrossRefGoogle Scholar
  65. Vellinga EC, Sysouphanthong P, Hyde KD (2011) The family of Agaricaceae: phylogenies and two new white-spored genera. Mycologia 103(3):494–509PubMedCrossRefGoogle Scholar
  66. Wasser SP (2002) Family Agaricaceae (FR.) Cohn of Israel mycobiota I. Tribe Agariceae Pat., ed Nevo E & Volz PA, A.R.G. Gantner Verlag K.G., Ruggell, LiechtensteinGoogle Scholar
  67. 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 315–322Google Scholar
  68. Zhao R, Desjardin DE, Soytong K, Perry BA, Hyde KD (2010) A monograph of Micropsalliota in Northern Thailand based on morphological and molecular data. Fungal Divers 45:33–79CrossRefGoogle Scholar

Copyright information

© Kevin D. Hyde 2011

Authors and Affiliations

  • Ruilin Zhao
    • 1
  • Samantha Karunarathna
    • 2
  • Olivier Raspé
    • 3
  • Luis A. Parra
    • 4
  • Jacques Guinberteau
    • 5
  • Magalie Moinard
    • 5
  • André De Kesel
    • 3
  • Gérard Barroso
    • 5
  • Régis Courtecuisse
    • 6
  • Kevin D. Hyde
    • 2
    • 7
  • Atsu K. Guelly
    • 8
  • Dennis E. Desjardin
    • 9
  • Philippe Callac
    • 5
  1. 1.Key Laboratory of Forest Disaster Warning and Control in Yunnan Province, Faculty of Conservation BiologySouthwest Forestry UniversityKunmingChina
  2. 2.School of ScienceMae Fah Luang UniversityChiang RaiThailand
  3. 3.National Botanic Garden of BelgiumMeiseBelgium
  4. 4.Aranda de DueroSpain
  5. 5.INRAVillenave d’OrnonFrance
  6. 6.Département de botanique, Faculté des sciences pharmaceutiques et biologiquesLilleFrance
  7. 7.Botany and Microbiology Department, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  8. 8.Département de Botanique, Faculté des Sciences, Université de LoméLoméTogo
  9. 9.Department of BiologySan Francisco State UniversitySan FranciscoUSA

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