Skip to main content
Log in

Major clades in tropical Agaricus

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

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.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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 22:285–291

  • Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: A fast, accurate and powerful alternative. Syst Biol 55:539–52

    Article  PubMed  Google Scholar 

  • 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 21–24

  • Baker RED, Dale WT (1951) Fungi of Trinidad & and Tobago. Mycol Papers 33:1–123

    Google Scholar 

  • Berkeley MJ, Broome CE (1871) The fingi of Ceylon (Hymenomycetes from Agaricus to Cantharellus. J Linn Soc 9:494–567

    Google Scholar 

  • 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):719–725

    Google Scholar 

  • 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 85:835–851

    Article  Google Scholar 

  • Capelari M, Rosa LH, Lachance M-A (2006) Description and affinities of Agaricus martineziensis, a rare species. Fungal Diversity 21:11–18

    Google Scholar 

  • Challen MP, Kerrigan RW, Callac P (2003) A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae. Mycologia 95(1):61–73

    Article  PubMed  CAS  Google Scholar 

  • Chevenet F, Brun C, Banuls AL, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees BMC. Bioinformatics 7:439

    PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Geml J, Geiser DM, Royse DJ (2004) Molecular evolution of Agaricus species based on IST and LSU rDNA sequences. Mycol Prog 3(2):157–176

    Article  Google Scholar 

  • Geml J, Laursen GA, Taylor DL (2008) Molecular diversity assessment of artic and boreal Agaricus taxa. Mycologia 100(4):577–589

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • 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 31:221–234

    Google Scholar 

  • Heinemann P (1956a) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II Agaricus Fr ss. Bull Jard Bot État 26:1–127

    Article  Google Scholar 

  • Heinemann P (1956b) Flore Iconographique des Champignons du Congo, 5º fascicule : Agaricus I. Ministère de l’Agriculture-Jardin Botanique de l’État Bruxelles

  • Heinemann P (1956c) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II Agaricus, Note complémentaire. Bull Jard Bot État 26:325–333

    Article  Google Scholar 

  • Heinemann P (1957) Flore Iconographique des Champignons du Congo, 6º fascicule : Agaricus II et Pilosace. Ministère de l’Agriculture-Jardin Botanique de l’État Bruxelles

  • Heinemann P (1961) Agarici Austro-Americani I Agaricus of Trinidad. Kew Bull 15:231–248

    Article  Google Scholar 

  • Heinemann P (1962a) Agarici Austro-Americani II Agaricus de Bolivie. Bull Jard Bot État 32:1–21

    Article  Google Scholar 

  • Heinemann P (1962b) Agarici Austro-Americani III Trois Agaricus de la Jamaïque. Bull Jard Bot État 32:23–28

    Article  Google Scholar 

  • Heinemann P (1962c) Agarici Austro-Americani IV Quatre Agaricus de Venezuela. Bull Jard Bot État 32:155–161

    Article  Google Scholar 

  • Heinemann P (1971) Quelques Psalliotes du Congo-Brazzaville. Cah Maboké 9:5–10

    Google Scholar 

  • Heinemann P (1978) Essai d’une clé de determination des genres Agaricus et Micropsalliota. Sydowia 30:6–37

    Google Scholar 

  • Heinemann P (1980) Les genres Agaricus et Micropsalliota en Malaisie et en Indonésie. Bull Jard Bot Belg 50:3–68

    Article  Google Scholar 

  • Heinemann P (1982) Quelques Psalliotes de Nouvelle Guinée (Papua New Guinea). Bull Jard Bot Belg 52:405–413

    Article  Google Scholar 

  • Heinemann P (1984) Agarici Austro-Americani VII. Agariceae des zones tempérées de l’Argentine et du Chili. Bull Jard Bot Belg 60:331–370

    Article  Google Scholar 

  • Heinemann P (1988) Novitates generis Micropsalliotae (Agaricaceae). Bull Jard Bot Belg 60:540–543

    Article  Google Scholar 

  • Heinemann P (1990) Agaricus singaporensis sp. nov. Bull Jard Bot Belg 60:417–419

    Article  Google Scholar 

  • Heinemann P (1993) Agarici Austro-Americani VIII Agaricaceae des régions intertropicales d’Amérique du Sud. Bull Jard Bot Belg 62:355–384

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Kerrigan RW (2005) Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia 97(1):12–24

    Article  PubMed  Google Scholar 

  • Kerrigan RW (2007) Lectotypification of Agaricus brunnescens. Mycologia 99(6):906–915

    Article  PubMed  CAS  Google Scholar 

  • 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):1292–1315

    Google Scholar 

  • Kerrigan RW, Callac P, Parra LA (2008) New and rare taxa in Agaricus section Bivelares (Duploannulati). Mycologia 100(6):876–892

    Article  PubMed  CAS  Google Scholar 

  • Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the fungi, Tenthth edn. CABI publishing, Wallingford

    Google Scholar 

  • 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

  • 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 l23:357–400

    Article  Google Scholar 

  • Murrill WA (1918) Agaricaceae of tropical North America VIII. Mycologia 10:62–85

    Article  Google Scholar 

  • Murrill WA (1942) New fungi from Florida. Lloydia 5(2):136–157

    Google Scholar 

  • Murrill WA (1945) New Florida fungi. Quart J Florida Acad Sci 8(2):175–198

    Google Scholar 

  • Murrill WA (1946) New and interesting Florida fungi. Lloydia 9(4):315–330

    Google Scholar 

  • Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for multiple sequence alignments. J Mol Biol 302:205–217

    Article  PubMed  CAS  Google Scholar 

  • Parra LA (2008) Agaricus L Allopsalliota Nauta & Bas. Pars 1 Edizioni Candusso Alassio, Italy

  • Parra LA, Villarreal M, Esteve-Raventos F (2002) Agaricus endoxanthus una specie tropicale trovata in Spagna. Rivista Micol 45(3):225–233

    Google Scholar 

  • Pegler DN (1966) Tropical African Agaricales. Persoonia 4(2):73–124

    Google Scholar 

  • Pegler DN (1968) Studies on African Agaricales I. Kew Bull 21:499–533

    Article  Google Scholar 

  • Pegler DN (1969) Studies on African Agaricales II. Kew Bull 23:219–249

    Article  Google Scholar 

  • Pegler DN (1977) A preliminary Agaric flora of east Africa. Kew Bull Add Series 6:1–615

    Google Scholar 

  • Pegler DN (1983) Agaric flora of the Lesser Antilles. Kew Bull Add Series 9:1–667

    Google Scholar 

  • Pegler DN (1986) Agaric flora of Sri Lanka. Kew Bull Add Series 12:1–519

    Google Scholar 

  • Pegler DN, Rayner RW (1969) A contribution to the Agaric flora of Kenya. Kew Bull 23:347–412

    Article  Google Scholar 

  • Peterson KR, Desjardin ED, Hemmes DE (2000) Agaricales of the Hawaiian Islands. 6. Agaricxaceae I. Agariceae: Agaricus and Melanophyllum. Sydowia 52(2):204–257

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.5, Available from http://tree.bio.ed.ac.uk/software/tracer/

  • Rick J (1906) Pilze aus Rio Grande do Sul (Brazilien). Broteria 5:5–53

    Google Scholar 

  • Rick J (1919) Contributio II ad monographiam Agaricinorum Brasiliensium. Broteriaser Bot 17:101–111

    Google Scholar 

  • Rick J (1920) Contributio ad monographiam Agaricinorum Brasiliensium. Broteria ser Bot 18:48–63

    Google Scholar 

  • Rick J (1930) Contributio IV ad monographiam Agaricinorum Brasiliensium. Broteria ser Bot 24:97–118

    Google Scholar 

  • Rick J (1939) Agarici Riograndenses IV. Lilloa 4(1):75–104

    Google Scholar 

  • Rick J (1961) Basidiomycetes Eubasidii in Rio Grande do Sul—Brasilia 5 Agaricaceae. Iheringia ser Bot 8:296–450

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • 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 81:8014–8018

    Article  PubMed  CAS  Google Scholar 

  • Vellinga EC, Sysouphanthong P, Hyde KD (2011) The family of Agaricaceae: phylogenies and two new white-spored genera. Mycologia 103(3):494–509

    Article  PubMed  Google Scholar 

  • 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, Liechtenstein

  • 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 

  • 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 45:33–79

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philippe Callac.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, R., Karunarathna, S., Raspé, O. et al. Major clades in tropical Agaricus . Fungal Diversity 51, 279–296 (2011). https://doi.org/10.1007/s13225-011-0136-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-011-0136-7

Keywords

Navigation