Phytotaxa 202 (3): 185–197
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Copyright © 2015 Magnolia Press
ISSN 1179-3155 (print edition)
Article
PHYTOTAXA
ISSN 1179-3163 (online edition)
http://dx.doi.org/10.11646/phytotaxa.202.3.2
Edible species of Agaricus (Agaricaceae) from Xinjiang Province (Western China)
ZHUO-REN WANG1, LUIS A PARRA2, PHILIPPE CALLAC3, JUN-LIANG ZHOU4,5, WEN-JIN FU6, SAN-HAN
DUI6, KEVIN D HYDE7,8,9 & RUI-LIN ZHAO 4*
1
College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei Province 430070, China
Avda. Padre Claret 7, 5º G, 09400 Aranda de Duero, Burgos, Spain
3
INRA, UR1264, MycSA, CS 20032, BP81, F-33882 Villenave d’Ornon, France
4
The State Key Lab of Mycology, Institute of Microbiology, Chinese Academic of Science, Beijing 100101, China
5
Institute of Microbiology, Beijing Forestry University, Beijing 100083, China
6
Institute of Agricultural Science, Agricultural Division 5 of Xinjiang Production and Construction Corps, Bortala, Xinjiang Province,
China
7
School of Science, Mae Fah Luang University, Chiang Rai 57100, Thailand
8
Institute of Excellence in Fungal Research, and School of Science, Mae Fah Luang
University, Chiang Rai 57100, Thailand
9
Department of Botany and Microbiology, College of Science, King Saud University, Riyadh 1145, Saudi Arabia
* Corresponding author: zhaoruilin@gmail.com
2
Abstract
Agaricus is a genus of macrofungi containing species with high edible and medicinal values. A survey of Agaricus species
carried out around the Ebinur Lake, in Xinjiang Province of China, in 2012, yielded 19 collections that exhibited a red discolouration when bruised. Morphological and phylogenetic comparison with species of five sections of Agaricus possessing
the red discolouration trait showed that the specimens belonged to four species. Two species, A. sinodeliciosus sp. nov. and
A. bitorquis in section Bivelares and A. desjardinii sp. nov. and A. padanus in section Nigrobrunnescentes, both sections
being monophyletic. The two new species proposed are described and illustrated and all species are compared with similar
taxa or previous records. Agaricus padanus is reported outside Italy for the first time. All species are edible and consumed
by locals, and appear to be adapted to relatively dry, cold and sandy habitats. Like A. bitorquis, A. sinodeliciosus produces
large, delicious semihypogeous basidiomata in such conditions; it is therefore a good potential candidate for domestication
and industrial production.
Keywords: taxonomy, phylogeny, ITS, cultivatable mushrooms
Introduction
The genus Agaricus L., the type genus of the Agaricaceae contains important edible and medicinal species (Largeteau
et al. 2011; Wisitrassameewong et al. 2012; Camelini et al. 2013; Thawthong et al. 2014). Significant examples are
A. subrufescens Peck and A. bisporus (J.E. Lange) Imbach; the latter commonly known as the button mushroom, is
reported to account for 32% of the total world production of cultivated mushrooms in 1997 (Chang 1999).
The classification of Agaricus species was previously mainly based on temperate area species of the north
hemisphere and comprised eight widely accepted sections (Parra 2008, 2013). Several potentially new sections were
revealed by phylogenetic analysis of ITS sequence data (Zhao et al. 2011), but they comprised exclusively tropical and
some subtropical species. There have been several recent studies on Agaricus with several new species reported from
Australia, China and Thailand (Chen et al. 2012, 2015; Karunarathna et al. 2014; Lebel 2013; Gui et al. 2015; Lebel
& Syme 2012; Li et al. 2014; Thongklang et al. 2014; Zhao et al. 2012, 2013).
A survey of Agaricus species was carried out around Lake Ebinur, in Bortala, Xinjiang Province of China, in
2012. This is the westernmost part of China near the border with Kazakhstan, where the main vegetation types are
grasslands, desert steppes and moorlands with a continental dry climate (temperature on average from -12°C in January
to 15°C in July). Morphological and phylogenetic analyses of the collections revealed four species; Agaricus desjardinii
Z.R. Wang, K.D. Hyde & R.L. Zhao sp. nov. and A. padanus Lancon. in section Nigrobrunnescentes K. P. Peterson,
Desjardin, & Hemmes; and A. sinodeliciosus Z.R. Wang & R.L. Zhao sp. nov. and A. bitorquis (Quél.) Sacc. in section
Bivelares (Kauffman) L.A. Parra. The aim of this paper is to introduce the new taxa and describe the new collections.
Accepted by Masoomeh Ghobad-Nejhad: 12 Feb. 2015; published: 13 Mar. 2015
185
(Geml et al. 2008); however maybe these species do not support both cold and dryness or they do not fruit at the same
time.
The species from sections Bivelares have high nutritional value. The consumed species in section Sanguinolenti
(e.g. A. sylvaticus) and in section Nigrobrunnescentes (e.g. A. lilaceps) are considered as very tasty. However their
cultivation on standard substrates has been limited or failed due to their slow mycelium growth rate (Hildén 2013).
The four species reported here are consumed by locals in western China. The medium to large sized basidiomata and
good taste of A. sinodeliciosus and A. bitorquis make them attractive and rewarding when collected, although this often
requires digging since they are typically semihypogeous. Agaricus bitorquis is the only commercial cultivated species
of the four taxa collected in this study. Attempts to cultivate these species is being carried out, and we have already
obtained some encouraging results for A. sinodeliciosus.
Acknowledgments
The National Natural Science Foundation of China (Project ID: 31000013, 31360014 and 31470152 to Rui-Lin Zhao),
the Bio-Asie project “Inventory and taxonomy of Agaricus species in Thailand, Laos, Malaysia and Yunnan (China);
domestication and evaluation of species of nutritional or medicinal interest”, and Project of Science and Technology
Department of Hubei Province, China (ID: 52206-04046 to Zhuo-Ren Wang) are acknowledged for their support this
study. Dr. Richard W. Kerrigan is also thanked for his suggestions on this paper. Dr. István Nagy is thanked for lending
us a specimen of A. biberi for this research. Thanks are extended to the Thailand Research Fund grant (BRG 5580009)
under the research grant entitled “Taxonomy, Phylogeny and Biochemistry of Thai Basidiomycetes” for financial
support.
References
Callac, P., Billette, C., Imbernon, M. & Kerrigan, R.W. (1993) Morphological, genetic, and interfertility analyses reveal a novel, tetrasporic
variety of Agaricus bisporus from the Sonoran Desert of California. Mycologia 85: 335–351.
http://dx.doi.org/10.2307/3760617
Camelini, C.M., Rezzadori, K., Benedetti, S., Proner, M.C., Fogaça, L., Azambuja, A.A., Giachini, A.J., Rossi, M.J. & Petrus, J.C.C.
(2013) Nanofiltration of polysaccharides from Agaricus subrufescens. Applied Microbiology and Biotechnology 97: 9993–10002.
http://dx.doi.org/10.1007/s00253-013-5241-y
Cappelli, A. (1984) Agaricus L.: Fr. (Psalliota Fr.). Libreria editrice Biella Giovanna, Saronno, Italy, 558 pp.
Challen, M.P., Kerrigan, R.W. & Callac, P. (2003) A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae.
Mycologia 95: 61–73.
http://dx.doi.org/10.2307/3761962
Chang, S.T. (1999) World production of edible and medicinal mushrooms in 1997 with emphasis on Lentinus edodes (Berk.) Sing. in
China. International Journal of Medicinal Mushrooms 1: 291–301.
http://dx.doi.org/10.1615/IntJMedMushr.v1.i4.10
Chen, J., Zhao, R.L., Karunarathna, S., Callac, P., Raspé, O., Bahkali, A.H. & Hyde, K.D. (2012) Agaricus megalosporus: a new species
in section Minores. Cryptogamie Mycologie 33: 145–155.
http://dx.doi.org/10.7872/crym.v33.iss2.2012.145
Chen, J., Zhao, R.L., Parra, L.A., Guelly, A.K., Kesel, A.D., Rapior, S., Hyde, K.D., Chukeatirote, E. & Callac, P. (2015) Agaricus section
Brunneopicti: a phylogenetic reconstruction with descriptions of four new taxa. Phytotaxa 192: 145–168.
http://dx.doi.org/10.11646/phytotaxa.192.3.2
Didukh, M. (2004) New data on rare and debatable species of the family Agaricaceae (Fr.) Cohn. Ukrainian Botanical Journal 61:
89–99.
Didukh, M., Vilgalys, R., Wasser, S.P., Isikhuemhen, O.S. & Nevo, E. (2005) Notes on Agaricus section Duploannulati using molecular
and morphological data. Mycological Research 109: 729–740.
http://dx.doi.org/10.1017/S0953756205002443
Edgar, R.C. (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–
1797.
AGARICUS (AGARICACEAE)
Phytotaxa 202 (3) © 2015 Magnolia Press • 195
http://dx.doi.org/10.1093/nar/gkh340
Edgar, R.C. (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC bioinformatics 5:
113.
http://dx.doi.org/10.1186/1471-2105-5-113
Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specifity for Basidiomycetes: application to identification of mycorrhizae
and rusts. Molecular Ecology 2: 113–118.
http://dx.doi.org/10.1111/j.1365-294X.1993.tb00005.x
Geml, J., Laursen, G.A. & Taylor, L.D. (2008) Molecular diversity assessment of arctic and boreal Agaricus taxa. Mycologia 100: 577–
589.
http://dx.doi.org/10.3852/07-042R1
Gui, Y., Zhu, G.S., Callac, P., Hyde, K.D., Parra, L.A., Chen, J., Yang, T.J., Huang, W.B., Gong, G.L. & Liu, Z.Y. (2015) Agaricus section
Arvenses: three new species in highland subtropical Southwest China. Fungal Biology 119 (2–3): 79–94.
http://dx.doi.org/10.1016/j.funbio.2014.10.005
Guinberteau, J., Callac, P. & Boisselet, P. (1998) Inventaire des communautés fongiques liées au Cupressus macrocarpa en zone littorale
atlantique et données récentes sur les populations sauvages d’Agaricus bisporus. Bulletin de la Société Mycologique de France 114:
19–38.
Heinemann, P. (1978) Essai d’une clé de determination des genres Agaricus et Micropsalliota. Sydowia 30: 6–37.
Heinemann, P. (1980) Les genres Agaricus et Micropsalliota en Malaisie et en Indonésie. Bulletin du Jardin Botanique National de
Belgique 50: 3–68.
http://dx.doi.org/10.2307/3667774
Heinemann, P. (1986) Agarici austroamericani VI. Apercu sur les Agaricus de Patagonie et de la terre de Feu. Bulletin du Jardin Botanique
National de Belgique 56: 417–446.
http://dx.doi.org/10.2307/3668202
Heinemann, P. (1990) Agarici austroamericani VII: Agariceae des zones tempérées de 1’Argentine et du Chili. Bulletin du Jardin Botanique
National de Belgique 60: 331–370.
http://dx.doi.org/10.2307/3668225
Hildén, K., Mäkelä, M.R., Lankinen, P. & Lundell, T. (2013) Agaricus bisporus and related Agaricus species on lignocellulose production
of manganese peroxidase and multicopper oxidases. Fungal Genetics and Biology 55: 32–41.
http://dx.doi.org/10.1016/j.fgb.2013.02.002.
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayesian: Bayesian inferance of phylogeny. Biometrics 17: 754–755.
Huelsenbeck, J.P., Ronquist, F. & Bollback, J.P. (2001) Bayesian inference of phylogeny and in its impact on evolutionary biology. Science
294: 2310–2314.
http://dx.doi.org/10.1126/science.1065889
Karunarathna S.C., Guinberteau, J., Chen, J.,Vellinga, E.C., Zhao, R.L., Chukeatirote, E., Yan, J.Y., Hyde, K.D., & Callac, P. (2014) Two
New Species in Agaricus Tropical Clade I. Chiang Mai Journal of Science 41: 771–780.
Kerrigan, R.W. (1986) Agaricales of California. Vol. 6. Agaricaceae. Mad River Press, Eureka, California, America. 1–62 pp.
Kerrigan, R.W., Callac, P. & Parra, L.A. (2008) New and rare taxa in Agaricus section Bivelares (Duploannulati). Mycologia 100: 876–
892.
http://dx.doi.org/10.3852/08-019
Lanconelli, L. (2002) Agaricus padanus sp. nov. Rivista di Micologia 45: 29–37.
Largent, D.L. (1986a) How to identify mushrooms to genus vol. 1. Macroscopic Features. Mad River Press, Eureka, California, 166 pp.
Largent, D.L. (1986b) How to identify mushrooms to genus vol. 3. Microscopic Features. Mad River Press, Eureka, California, 148 pp.
Largeteau, M.L., Llarena-Hernández, R.C., Regnault-Roger, C. & Savoie, J.-M. (2011) The medicinal Agaricus mushroom cultivated in
Brazil: biology, cultivation and non-medicinal valorization. Applied Microbiology and Biotechnology 92: 897–907.
http://dx.doi.org/10.1007/s00253-011-3630-7
Lebel, T. (2013) Two new species of sequestrate Agaricus (section Minores) from Australia. Mycological Progress 12: 699–707.
http://dx.doi.org/10.1007/s11557-012-0879-x
Lebel, T. & Syme, A. (2012) Sequestrate species of Agaricus and Macrolepiota from Australia: new species and combinations and their
position in a calibrated phylogeny. Mycologia 104: 496–520.
http://dx.doi.org/10.3852/11-092
Li, S.F., Xi, Y.L., Qi, C.X., Liang, Q.Q., Wei, S.L., Li, G.J., Zhao, D., Li, S.J. & Wen H.A. (2014) Agaricus taeniatus sp. nov., a new
member of Agaricus sect. Bivelares from northwest China. Mycotaxon 129: 187–196.
http://dx.doi.org/10.5248/129.187
Michalak, S. (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity and Evolution 12: 335–337.
196 • Phytotaxa 202 (3) © 2015 Magnolia Press
WANG ET AL.
http://dx.doi.org/10.1007/s13127-011-0056-0
Nauta, M.M. (2001) Agaricus L. and Allopsalliota Nanta et Bas. In: Noordeloos, M.E., Kyuper, T.W. & Vellinga E.C. (Eds.) Flora Agaricina
Neerlandica, Critical monographs on families of Agarics and Boleti occurring in the Netherlands. Vol. 5 Family Agaricaceae. A.A.
Balkema Publishers, Lisse, pp. 23–62.
Parra, L.A. (2008) Agaricus L. Allopsalliota, Nauta & Bas, Fungi Europaei, Volume 1. Edizioni Candusso, Alassio, 824 pp.
Parra, L.A. (2013) Agaricus L. Allopsalliota, Nauta & Bas, Fungi Europaei, Volume 1A. Candusso Edizioni s.a.s. Alassio, 1168 pp.
Parra, L.A., Muñoz, G. & Callac, P. (2014) Agaricus caballeroi sp. nov., una nueva especie de la sección Nigrobrunnescentes recolectada
en España. Micologia e Vegetazione Mediterranea 29: 21–38.
Peterson, K.R., Desjardin, D.E. & Hemmes, D.E. (2000) Agaricales of the Hawaiian Islands. 6. Agaricaceae L. Agariceae: Agaricus and
Melanophyllum. Sydowia 52: 204–257.
Ronquist, F. & Heulsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–
1574.
http://dx.doi.org/10.1093/bioinformatics/btg180
Samgina, D.I. & Nam, G.A. (1989) Novyĭ vid iz roda Agaricus L.: Fr. Izvestiya Akademii Nauk Kazakhskoĭ SSR Seriya Biologicheskaya 156:
78–80.
Thawthong, A., Karunarathna, S.C., Thongklang, N., Chukeatirote, E., Kakumyan, P., Chamyuang, S., Rizal, M. Mortimer, P.E., Xu, J.C.,
Callac, P. & Hyde, K.D. (2014) Discovering and Domesticating Wild Tropical Cultivatable Mushrooms. Chiang Mai Journal of
Science 41: 731–764.
Thongklang, N., Nawaz, R., Khalid, A.N., Chen, J., Hyde, K.D., Zhao, R.L., Parra, L.A., Hanif, M. , Moinard, M. & Callac, P. (2014)
Morphological and molecular characterization of three Agaricus species from tropical Asia (Pakistan, Thailand) reveals a new group
in section Xanthodermatei. Mycologia 106: 1220–1232.
http://dx.doi.org/10.3852/14-076
White, T.J., Bruns, T.L., Lee, S. & Taylor, J.W. (1990) Application and direct sequencing of fungal ribosomal RNA genes for phylogenetics.
In: Innis, M.A., Gefand, D.H., Sninsky, J.J. & White, J.T. (Eds.) PCR Protocols: A Guide to Methods and Applications. Academic
Press, San Diego, 482 pp.
http://dx.doi.org/10.1016/B978-0-12-372180-8.50042-1
Wisitrassameewong, K., Karunarathna, S., Thongklang, N., Zhao, R.L., Callac, P., Moukha, S., Ferandon, C., Chukeatirote, E. & Hyde,
K.D. (2012) Agaricus subrufescens: A review. Saudi Journal of Biological Sciences 19: 131–146.
http://dx.doi.org/10.1016/j.sjbs.2012.01.003
Zhao, R.L., Desjardin, D.E., Callac, P., Parra, L.A., Guinbereau, J., Soytong, K., Karunarathna, S., Zhang, Y. & Hyde, K.D. (2013) Two
species of Agaricus sect. Xanthodermatei from Thailand. Mycotaxon 122: 187–195.
http://dx.doi.org/10.5248/122.187
Zhao, R.L., Hyde, K.D., Desjardin, D.E., Raspé, O., Soytong, K., Guinberteau, J., Karunarathna, S.C. & Callac, P. (2012) Agaricus
flocculosipes sp. nov., a new potentially cultivatable species from the palaeotropics. Mycoscience 53: 300–311.
http://dx.doi.org/10.1007/S10267-011-0169-5
Zhao, R.L., Karunarathna, S., Raspé, O., Parra, L.A., Guinberteau, J., Moinard, M., Kesel, A.D., Barroso, G., Courtecuisse, R., Hyde,
K.D., Guelly, A.K., Desjardin, D.E. & Callac, P. (2011) Major clades in tropical Agaricus. Fungal Diversity 51: 279–296.
http://dx.doi.org/10.1007/s13225-011-0136-7
AGARICUS (AGARICACEAE)
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Luis Carlos Martinez Parra