WSMBMP
Bulletin Number 13. July 31th, 2015


Updating Genetic Resources in the Genus Agaricus

Philippe Callac
INRA, UR1264, MycSA, CS 20032, BP81, F-33882 Villenave d’Ornon, France

callac@bordeaux.inra.fr

    We have entered a molecular era in which the number of described Agaricus species is rapidly increasing. The question that arises is to establish if the new species can be cultivated. There is also the question of edibility, which in most cases is unknown. The approach has first been to classify these new species and then to test in cultivation those species in sections that are already known to contain cultivatable edible species. The present short review focuses on the new species introduced since 2000. It is not necessary to explain the rules of the nomenclature knowing that it is sometime difficult for non-taxonomists to understand why the name of a species can change. However, to be complete, Table I includes all the taxa named or renamed to my knowledge since 2000 and the corresponding references [1-30].

New taxa in the genus Agaricus
    From 2000 to the end of June 2015, 56 species, one subspecies and one variety have been described and assigned to the genus Agaricus. Among these 58 taxa new to science, 20 were found in Asia, 19 in Europe, 10 in Oceania, four in North America, one in Africa, and three in more than one  continents (N. Am. + Eur., Asia + Eur., Africa + Asia). This distribution does not reflect the occurrence of the genus but areas where field work or certain groups of species have been better investigated, mainly though five contexts: (i) in Europe, for completion of a monumental monograph [2, 30], species of the poorly known section Minores have been characterized thanks to molecular data; (ii) in Australia, efforts have been focused on the interesting secotioid species [4, 5] of which the sporocarp has evolved towards a gasteroid state (puffball); (iii) in tropical areas, following a study evidencing a palaeotropical clade (i.e. tropical Africa and Asia) named TRI [31], the Agaricus section Brunneopicti corresponding to this clade has been revisited [18, 24]; (iv) in Thailand through an inventory of Agaricus species in progress [1,3, 7, 9, 21]; and (v) in China also through such species inventories in several provinces [14, 15, 20]. In fact, with the exception of A. pachydermis, sequences of the nrDNA-ITS region are available for all the new taxa. These sequences characterize them and, using phylogenetic analyses, the 58 new taxa were classified in nine sections of the genus: 19 in Minores, 9 Xanthodermatei, 8 Bivelares, 7 Brunneopicti, 7 Arvenses, 5 Nigrobrunnescentes, 1 Agaricus, 1 Spissicaules and 1 unclassified. The section Nigrobrunnescentes is one of the three monophyletic groups that previously constituted the polyphyletic section Sanguinolenti. Among the 58 taxa, 16 are from tropical areas, mostly from Asia. Many other putative new species from tropical areas have been sequenced and included in the analyses, but more collections and/or comparative studies are required to formally describe and name them. It is expected that many new species from tropical areas (mainly Thailand), from China, and also from North America will be proposed soon since for the latter a monograph will be published (Kerrigan R.W., in press).
    In addition, since 2000, three new combinations and seven new names have been also proposed; four of these ten species have been renamed because they were secotioid species previously classified in different genera. We note that among the 12 secotioid species of Agaricus that were recently described or renamed, eight belong to the closely related sections Minores or Arvenses and might be edible, as are other species of the section Arvenses. We successfully cultivated A. aridicola (J. Guinberteau & P. Callac, unpublished data), but did not consume it. Finally, the potential interest of these secotioid Agaricus remains to be investigated.

Which are the sections of interest?
    Commercially cultivated species belong either to section Bivelares including A. bisporus (the button mushroom)and A. bitorquis, or to section Arvenses including A. subrufescens (the almond mushroom) or A. arvensis. Species of sections Minores have rarely been been tested for edibility, but some of them merit more attention. Species of sections Agaricus and Nigrobrunnescentes should be particularly interesting because they are edible, tasty and consumed in many countries, but they generally failed in fruiting tests. Agaricus pseudoargenticus has been successfully cultivated; this species should be closely related to A. lanipes and A. impudicus [32]; these two species were previously placed in the section Sanguinolenti, but belong to the sections Spissicaules and Subrutilescentes, respectively. At least two species of the section Brunneopicti are locally consumed, A. subsaharianus and A. bingensis, but it is not recommended to consider all the species of this section as edible because some of them have a phenol-like odor and could be poisonous as can be the species of the section Xanthodermatei in which phenol is responsible of gastro-intestinal symptoms [18]. Finally, we will focus here on section Bivelares and Arvenses.

Section Bivelares
    The two new species A. cupressophilus and A. tlaxcalensis joined A. cupressicola in the new subsection Cupressorum. Agaricus cupressophilus fruited on compost substrate [16 see Fig. 8], A. tlaxcalensis was not tested, and A. cupressicola also fruited [33 see Fig. 2f]. Similarly, most of the species of the subsection Bivelares can fructify on standard compost substrate used for A. bisporus. It is of course the case for the new homothallic variety A. bisporus var. eurotetrasporus which produce haploid sporocarps [17, 33 see Fig. 2e]. However, in the A. devoniensis complex two strains of the new subspecies bridghamii failed to fruit while all 19 isolates of the subspecies devoniensis from France, Greece and USA fruited [33 see Fig. 2a, 34]. In the latter subspecies, genetic improvement of strains is promising since genetic resources are diversified and a part of the strains are typically heterokaryotic. The new homothallic species A. agrinferus can fruit on compost substrate [16, 33 see Fig. 2d as A. subfloccosus] as its homothallic sister species A. subfloccosus [35, 36, 37]. The new species A. subsubensis fruited easily [16]. No information is presently available concerning the ability for fruiting of the two new species recently reported from China A. taeniatus and A. sinodeliciosus.In conclusion, five of the eight new taxa have been tested for their ability to fruit on compost and four of them fruited.

Section Arvenses
    Among the seven new species described in this section only A. flocculosipes has been reported as fruiting on compost substrate [38]. This species was initially described from Thailand and Mayotte Island [21] and has recently been recorded from China [20].
    In other respects, it can be notified that the known geographical distribution range of the medicinal species A. subrufescens recently extended to Asia with specimens collected in Thailand and in China [20, 31, 39]. The ITS sequences of these collections were identical or very similar to the sequences of the specimens of Hawaii that were considered as divergent from the European and Americas samples [40]. In spite of this divergence samples from Brazil, France and Thailand remained interfertile [41].

Conclusions
     Among 58 new taxa described since 2000, 15 belong to sections Bivelares or Arvenses, only five were tested in cultivation on compost substrate, and four of them fruited. This demonstrates how long is the road between field work and the mushroom farm [42]. A first reason might be that collectors were unable to isolate strains. A second reason is that taxonomists would not always realize the interest of their discoveries as the mushroom farmers would not realize always the potential of these new species. As a result, species of potential interest are often described without strain isolation and when strains are isolated they often lie unused in collections. A third reason is that strains have been isolated from certain species but are still being evaluated. The genus Agaricus contains more than 400 recognized species and possibly several hundred will be discovered in the next few years. It will be challenging to manage these new data.

Acknowledgements
    My colleagues Kevin D. Hyde and Luis A. Parra are acknowledged for their corrections to the manuscript.

References
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Table I. List of taxa named or renamed since 2000

Taxon name

Section

Continent

Ref.

New species, subspecies or varietya

 

 

 

Agaricus parvibicolor

Minores

Asia

[1]

Agaricus sodalis

Minores

Asia

[1]

Agaricus edmondoi

Minores

Europe

[2]

Agaricus friesianus

Minores

Europe

[2]

Agaricus gemlii

Minores

Europe

[2]

Agaricus jacobi

Minores

Europe

[2]

Agaricus kerriganii

Minores

Europe

[2]

Agaricus marisae

Minores

Europe

[2]

Agaricus matrum

Minores

Europe

[2]

Agaricus greuteri

Minores

Europe

[2]

Agaricus arrillagarum

Minores

Europe

[2]

Agaricus callacii

Minores

Europe

[2]

Agaricus megalosporus

Minores

Asia

[3]

Agaricus colpeteii S

Minores

Oceania

[4]

Agaricus lamelliperditus S

Minores

Oceania

[4]

Agaricus chartaceus S

Minores

Oceania

[5]

Agaricus wariatode S

Minores

Oceania

[5]

Agaricus pachydermis S

Minores

Oceania

[5]

Agaricus campbellensis

Minores

Oceania

[6]

Agaricus bisporiticus

Xanthodermatei

Asia

[7]

Agaricus fuscopunctatus

Xanthodermatei

Asia

[7]

Agaricus moelleroides

Xanthodermatei

Europe

[2]

Agaricus biannulatus

Xanthodermatei

Europe

[8]

Agaricus murinocephalus

Xanthodermatei

Asia

[9]

Agaricus parvitigrinus

Xanthodermatei

Europe

[10]

Agaricus xanthodermulus

Xanthodermatei

Europe

[10]

Agaricus tollocanensis

Xanthodermatei

N. America

[11]

Agaricus laskibarii

Xanthodermatei

Europe

[12]

Agaricus freirei

Xanthodermatei

Europe

[13]

Agaricus sinodeliciosus

Bivelares

Asia

[14]

Agaricus taeniatus

Bivelares

Asia

[15]

Agaricus agrinferus

Bivelares

Europe,
N. America.

[16]

Agaricus subsubensis

Bivelares

N. America

[16]

Agaricus cupressophilus

Bivelares

N. America

[16]

Agaricus tlaxcalensis

Bivelares

N. America

[16]

Agaricus devoniensis subsp. bridghamii

Bivelares

N. America

[16]

Agaricus bisporus var. eurotetrasporus

Bivelares

Europe

[17]

Agaricus niveogranulatus

Brunneopicti

Asia

[18]

Agaricus brunneosquamulosus

Brunneopicti

Asia

[18]

Agaricus sordidocarpus

Brunneopicti

Asia

[18]

Agaricus toluenolens

Brunneopicti

Asia

[18]

Agaricus chiangmaiensis

Brunneopicti

Asia

[1]

Agaricus megacystidiatus

Brunneopicti

Asia

[1]

Agaricus subsaharianus

Brunneopicti

Africa

[19]

Agaricus guizhouensis

Arvenses

Asia

[20]

Agaricus longistipes

Arvenses

Asia

[20]

Agaricus megalocarpus

Arvenses

Asia

[20]

Agaricus indistinctus

Arvenses

Europe

[2]

Agaricus flocculosipes

Arvenses

Asia, Africa

[21]

Agaricus eburneocanus S

Arvenses

Oceania

[5]

Agaricus subantarcticus

Arvenses

Oceania

[6]

Agaricus desjardinii

Nigrobrunnescentes

Asia

[14]

Agaricus caballeroi

Nigrobrunnescentes

Europe

[22]

Agaricus erythrosarx S

Nigrobrunnescentes

Oceania

[5]

Agaricus padanus

Nigrobrunnescentes

Europe, Asia

[23]

Agaricus flavicentrus

Agaricus

Asia

[24]

Agaricus hanthanaensis

Spissicaules

Asia

[24]

Agaricus inilleasper S

Non-classified

Oceania

[5]

Renamed species (comb. nov. or nom. nov.)

 

 

 

Agaricus pallens comb. nov.

Minores

Europe

[2]

Agaricus iesu-et-marthae nom. nov.

Minores

Europe

[2]

Agaricus aridicola nom. nov. S

Minores

Europe, Asia

[25]

Agaricus huijsmanii nom. nov.

Minores

Europe

[26]

Agaricus brunneopunctatus nom. nov.

Brunneopicti

Africa

[18]

Agaricus macrolepis comb. nov.

Arvenses

Europe

[26]

Agaricus inapertus nom. nov. S

Arvenses

N. America

[27]

Agaricus deserticola nom. nov. S

TRIVb

N. America

[28]

Agaricus melanosporus comb. nov.S

Non-classified

Oceania

[5]

Agaricus bohusianus nom. nov.

Non-classified

Europe

[29]

New or renamed section or subsection

 

 

 

Agaricus section Bivelares

 

 

[30]

Agaricus [section Bivelares] subsection Cupressorum

 

 

[16]

Agaricus section Sanguinolenti

 

 

[30]

Agaricus subsection Sylvatici

 

 

[30]

Agaricus subsection Bohusia

 

 

[30]

a Sections are ordered by greatest numbers of new species, and within each section species are in chronological order with the most recently introduced species first.
b TRIV = tropical clade IV, see [31]




The WSMBMP Bulletin is the official electronic publication of the World Society for Mushroom Biology and Mushroom Products. The bulletin is intended to keep members informed about Council activities and to share general information about mushrooms. It is designed to allow communication between society members and alert them about new topics and opportunities related to mushrooms. Society members and general public are kindly invited to submit letters, comments and information of interest for the mushroom community to be published in the bulletin. Please submit your contributions electronically in free format to the editors José E. Sanchez esanchez@ecosur.mx, John Buswelljabuswell2003@yahoo.co.uk, Daniel J. Royse djr4@psu.edu or Helen Grogan helen.grogan@teagasc.ie.


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