Evidence for amphithallism and broad geographical hybridization potential among Agaricus subrufescens isolates from Brazil, France, and Thailand

Fungal Biology

Volumn 118, Issue 12, 2014, Pages 1013-1023

  Thongklang, Naritsada ^a   Hoang, Eric ^b   Rodriguez Estrada, Alma E ^c   Sysouphanthong, Phongeun ^a   Moinard, Magalie ^b   Hyde, Kevin D ^a   Kerrigan, Richard W ^d   Foulongne Oriol, Marie ^b   Callac, Philippe ^b  

^a MAE FAH LUANG UNIVERSITY   (Thailand)

^b CEMAGREF   (France)

^c AURORA UNIVERSITY   (United States)

^d Sylvan Biosciences   (United States)

Author keywords

Interfertility; Life cycle; Meiosporogenesis; Postmeiotic mitosis; Pseudohomothallism

Indexed keywords

EDIBLE SPECIES; FERTILITY; FUNGUS; GEOGRAPHICAL DISTRIBUTION; HYBRIDIZATION; LIFE CYCLE; MEDICINAL PLANT; MUSHROOM; OCEANIA ECOZONE;

ASIA; EUROPE; NORTH AMERICA;

AGARICUS SUBRUFESCENS;

FUNGAL DNA; GENETIC MARKER;

AGARICUS; BRAZIL; CLASSIFICATION; FRANCE; GENE LOCUS; GENETIC MARKER; GENETICS; GENOTYPING TECHNIQUE; GEOGRAPHY; HYBRIDIZATION; ISOLATION AND PURIFICATION; PHYLOGEOGRAPHY; THAILAND;

AGARICUS; BRAZIL; DNA, FUNGAL; FRANCE; GENETIC LOCI; GENETIC MARKERS; GENOTYPING TECHNIQUES; GEOGRAPHY; HYBRIDIZATION, GENETIC; PHYLOGEOGRAPHY; THAILAND;

EID: 84912559636     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2014.10.004     Document Type: Article

References (54)

1. Arrillaga P., Parra L.A. El género Agaricus L. en España. XI. Agaricus subrufescens, primera cita para España. Boletin Sociedad Micologica de Madrid 2006, 30:201-207.
2. Brian C., Pirobe L., Guinberteau J. Amelioration de differentes espèces de champignons comestibles. Mushroom Science 1981, 11:715-723.
3. Burnett J.H., Boulter M.E. The mating systems of fungi II. Mating systems of the gasteromycetes, Mycocalia denudata and M. duriaeana. New Phytologist 1963, 62:217-236.
4. Callac P., Billette C., Imbernon M., Kerrigan R.W. Morphological, genetic, and interfertility analyses reveal a novel, tetrasporic variety of Agaricus bisporus from the Sonoran desert of California. Mycologia 1993, 85:835-851.
5. Callac P., Imbernon M., Kerrigan R.W., Olivier J.M. The two life cycles of Agaricus bisporus. Mushroom Biology and Mushroom Product. Proceedings of the 2nd International Conference 1996 1996, 57-66. University Park, The Pennsylvania State University. D.J. Royse (Ed.).
6. Callac P., Desmerger C., Kerrigan R.W., Imbernon M. Conservation of genetic linkage with map expansion in distantly related crosses of Agaricus bisporus. FEMS Microbiology Letters 1997, 146:235-240.
7. Calvo-Bado L., Noble R., Challen M., Dobrovin-Pennington A., Elliott T. Sexuality and Genetic Identity in the Agaricus Section Arvenses. Applied and Environment Microbiology 2000, 66:728-734.
8. Challen M.P., Elliott T.J. Segregation of genetic markers in the two-spored secondary homothallic basidiomycete Coprinus bilanatus. Theoretical and Applied Genetics 1989, 78:601-607.
9. Cappelli A. Approccio al Genere Agaricus - IV. Rivista di Micologia 2011, 1:2-27.
10. Elliott T.J. Comparative sexuality in Agaricus species. Journal of General Microbiology 1978, 107:113-122.
11. Evans H.J. Nuclear behavior in the cultivated mushroom, Agaricus bisporus. Microbiology 1959, 145:1105-1113.
12. Firenzuoli F., Gori L., Lombardo G. The medicinal mushroom Agaricus blazei Murrill: review of literature and pharmaco-toxicological problems. Evidence-Based Complementary and Alternative Medicine 2008, 5:3-15.
13. Foulongne-Oriol M., Spataro C., Cathalot V., Monllor S., Savoie J.M. An expanded genetic linkage map of Agaricus bisporus based on AFLP, SSR and CAPS markers sheds light on the recombination behaviour of the species. Fungal Genetics and Biology 2010, 47:226-236.
14. Foulongne-Oriol M., Lapalu M., Férandon C., Spataro C., Ferrer N., Amslem J., Savoie J.M. The first set of expressed sequence tags (EST) from the medicinal mushroom Agaricus subrufescens delivers resource for gene discovery and marker development. Applied Microbiology and Biotechnology 2014, 98:7879-7892.
15. Giraud T., Yockteng R., Lopez-Villavicencio M., Refrégier G., Hood M.E. Invited Mini-Review: the mating system of Microbotryum violaceum: selfing under heterothallism. Eukaryotic cell 2008, 7:765-775.
16. Herreira K.M.S., Alves E., Costa M.D., Dias E.S. Electron microscopy studies of basidiosporogenesis in Agaricus brasiliensis. Mycologia 2012, 104:1272-1280.
17. Jacobson K.M., Miller O.K. Postmeiotic mitosis in the basidia of Suillus granulatus: implications for population structure and dispersal biology. Mycologia 1994, 86:511-516.
18. James T.Y., Kues U., Rehner S.A., Vilgalys R. Evolution of the gene encoding mitochondrial intermediate peptidase and its cosegregation with the A mating-type locus of mushroom fungi. Fungal Genetics and Biology 2004, 41:381-390.
19. Kamzolkina O.V., Volkova V.N., Kozlova M.V., Pancheva E.V., Dyakov Y.T., Callac P. Karyological evidence for meiosis in the three different types of life cycles existing in Agaricus bisporus. Mycologia 2006, 98:763-770.
20. Kerrigan R.W. Agaricus of North America 2015, New York Botanical Garden Press, Bronx, New York, (in press).
21. Kerrigan R.W. Agaricus subrufescens, a cultivated edible and medicinal mushroom, and its synonyms. Mycologia 2005, 100:876-892.
22. Kerrigan R.W., Ross I.K. Dynamic aspects of basidiospore number variation in Agaricus. Mycologia 1987, 79:204-215.
23. Kerrigan R.W., Baller L.M., Horgen P.A., Anderson J.B. Strategies for the efficient recovery of Agaricus bisporus homokaryons. Mycologia 1992, 84:575-579.
24. Kerrigan R.W., Royer J.C., Baller L.M., Kohli Y., Horgen P.A., Anderson J.B. Meiotic behavior and linkage relationships in the secondarily homothallic fungus Agaricus bisporus. Genetics 1993, 133:225-236.
25. Kerrigan R.W., Imbernon M., Callac P., Billette C., Olivier J.M. The heterothallic life cycle of Agaricus bisporus var. burnettii, and the inheritance of its tetrasporic trait. Experimental Mycology 1994, 18:193-210.
26. Kerrigan R.W., Callac P., Parra L.A. New and rare taxa in Agaricus section Bivelares (Duploannulati). Mycologia 2008, 100:876-892.
27. Kües U., James T.Y., Vilgalys R., Challen M.P. The chromosomal region containing pab-1, mip, and the A mating type locus of the secondary homoallelic homobasidiomycete Coprinus bilanatus. Current Genetics 2001, 39:16-24.
28. Kühner R. Variation of nuclear behavior in the homobasidiomycetes. Transactions of the British Mycological Society 1977, 68:1-16.
29. Lange M. Species concepts in the genus Coprinus. Dansk Botanisk Arkiv Udgivet af Dansk Botanisk Forening 1952, 14:1-140.
30. Liu Y.L., Whelen S., Hall B.D. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 1999, 16:1799-1808.
31. Lamoure D. Indices of useful in formations for incompatibility tests in basidiomycetes. V. - Agaricales sensu lato. Cryptogamie Mycologie 1989, 10:41-80.
32. °C). Fungal Biology 2011, 115:1186-1195.
33. Llarena Hernández R.C., Largeteau M., Farnet A.M., Minvielle N., Regnault-Roger C., Savoie J.M. Phenotypic variability in cultivars and wild strains of Agaricus brasiliensis and Agaricus subrufescens. Proceedings of the 7th International Conference on Mushroom Biology and Mushroom Products 2011, vol. 2:38-49. http://www.wsmbmp.org/Previous_Conference:7.html.
34. Llarena-Hernández R.C., Largeteau M.L., Farnet A.M., Fouloungne-Oriol M., Minvielle N., Regnault-Roger C., Savoie J.M. Potential of European wild strains of Agaricus subrufescens for productivity and quality on wheat straw based compost. World Journal of Microbiology and Biotechnology 2013, 29:1243-1253.
35. Llarena-Hernández R.C., Largeteau M.L., Ferrer N., Regnault-Roger C., Savoie J.M. Optimization of the cultivation conditions for mushroom production with European wild strains of Agaricus subrufescens and Brazilian cultivars. Journal of the Science of Food and Agriculture 2014, 94:77-84.
36. Ludwig E. Pilzkompendium 2: 61 2007, Fungicon-Verlag, Berlin.
37. Matheny P.B., Wang Z., Binder M., Curtis J.M., Lim Y.W., Nilsson R.H., Hughes K.W., Hofstetter V., Ammirati J.F., Schoch C.L., Langer E., Langer G., McLaughlin D.J., Wilson A.W., Frøslev T., Ge Z.W., Kerrigan R.W., Slot J.C., Yang Z.L., Baroni T.J., Fischer M., Hosaka K., Matsuura K., Seidl M.T., Vauras J., Hibbett D.S. Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Molecular Phylogenetics and Evolution 2007, 43:430-451.
38. Mizuno T., Hagiwara T., Nakamura T., Ito H., Shimura K., Sumiya T., Asakura A. Antitumor activity and some properties of water-soluble polysaccharides from 'Himematsutake', the fruiting body of Agaricus blazei Murill. Agricultural and Biological Chemistry 1990, 54:2889-2896.
39. Mizuno T., Inagaki R., Kanao T., Hagiwara T., Nakamura T., Ito H., Shimura K., Sumiya T., Asakura A. Antitumor activity and some properties of water-insoluble hetero-glycans from 'Himematsutake', the fruiting body of Agaricus blazei Murill. Agricultural and Biological Chemistry 1990, 54:2897-2905.
40. Morin E., Kohler A., Baker A.R., Foulongne-Oriol M., Lombard V., Nagy L.G., Ohm R.A., Patyshakuliyeva A., Brun A., Aerts A.L., Bailey A.M., Billette C., Coutinho P.M., Deakin G., Doddapaneni H., Floudas D., Grimwood J., Hilden K., Kues U., LaButti K.M., Lapidus A., Lindquist E.A., Lucas S.M., Murat C., Riley R.W., Salamov A.A., Schmutz J., Subramanian V., Wosten H.A.B., Xu J., Eastwood D.C., Foster G.D., Sonnenberg A.S.M., Cullen D., de Vries R.P., Lundell T., Hibbett D.S., Henrissat B., Burton K.S., Kerrigan R.W., Challen M.P., Grigoriev I.V., Martin F. Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:17501-17506.
41. Ota Y., Fukuda K., Suzuki K. The nonheterothallic life cycle of Japanese Armillaria mellea. Mycologia 1998, 90:396-405.
42. Parra L.A. Agaricus L. Allopsalliota Nauta & Bas. (Parte II) 2013, Candusso, Alassio, Italy.
43. Peterson K.R., Desjardin D.E., Hemmes D.E. Agaricales of the Hawaiian Islands. 6. Agaricaceae I: Agariceae: Agaricus and Melanophyllum. Sydowia 2000, 52:204-257.
44. Raper C.A., Raper J.R., Miller R.E. Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 1972, 64:1088-1117.
45. Raper C.A. Sexuality and life cycle of the edible, wild Agaricus bitorquis. Microbiology 1976, 95:54-66.
46. Sequeira L. Nuclear phenomena in the basidia and basidiospores of Omphalia flavida. Mycologia 1954, 46:470-483.
47. Souza Dias E., Abe C., Schwan R.F. Truths and myths about the mushroom Agaricus blazei. Scientia Agricola 2004, 61:545-549.
48. Souza Dias E., Gontijo Labory C.R., Herrera K.M.S., Alves A.A., Torres G.A., Rinker D.L. Cytological studies of Agaricus brasiliensis. World Journal of Microbiology and Biotechnology 2008, 24:2473-2479.
49. White T.J., Bruns T., Lee S., Taylor J.W. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a guide to methods and applications 1990, 315-322. Academic, New York. M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White (Eds.).
50. Wisitrassameewong K., Karunarathna S.C., Thongklang N., Zhao R., Callac P., Chukeatirote E., Bahkali A.H., Hyde K.D. Agaricus subrufescens: new to Thailand. Chiang Mai Journal of Science 2012, 39:281-291.
51. Wisitrassameewong K., Karunarathna S.C., Thongklang N., Zhao R., Callac P., Moukha S., Férandon C., Chukeatirote E., Hyde K.D. Agaricus subrufescens: a review. Saudi Journal of Biological Sciences 2012, 19:131-146.
52. Xu J., Kerrigan R.W., Horgen P.A., Anderson J.B. Localization of the Mating Type Gene in Agaricus bisporus. Applied and Environmental Microbiology 1993, 59:3044-3049.
53. Zhao R., Karunarathna S., Raspé O., Parra L.A., Guinberteau J., Moinard M., De Kesel A., Barroso G., Courtecuisse R., Hyde K.D., Guelly A.K., Desjardin D.E., Callac P. Major clades in tropical Agaricus. Fungal Diversity 2011, 51:279-296.
54. Zied D.C., Pardo-Gimenez A., Savoie J.M., Pardo-Gonzalez J.R., Callac P. "Indoor" method of composting and genetic breeding of the strains to improve yield and quality of the almond mushroom Agaricus subrufescens. Proceedings of the 7th International Conference on Mushroom Biology and Mushroom Products 2011, vol. 1:419-427. http://www.wsmbmp.org/Previous_Conference:7.html.