Research Article |
Corresponding author: Ratchadawan Cheewangkoon ( ratchadawan.c@cmu.ac.th.com ) Corresponding author: Rui-Lin Zhao ( zhaorl@im.ac.cn ) Academic editor: Zai-Wei Ge
© 2018 Mao-Qiang He, Boontiya Chuankid, Kevin D. Hyde, Ratchadawan Cheewangkoon, Rui-Lin Zhao.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
He M-Q, Chuankid B, Hyde KD, Cheewangkoon R, Zhao R-L (2018) A new section and species of Agaricus subgenus Pseudochitonia from Thailand. MycoKeys 40: 53-67. https://doi.org/10.3897/mycokeys.40.26918
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A large species diversity has recently been discovered in the genus Agaricus. Six subgenera and 23 sections are now recognised. In this study, three specimens collected from Thailand, formed a monophyletic clade in subgenus Pseudochitonia, based on analyses of ITS sequence data. Further analyses, based on multi-gene sequence data (ITS, LSU, tef1-α), using BEAST, revealed that this clade originated 26.7 Ma. According to their distinct morphological characteristics, phylogenetic position and relatively old divergence time, a new section Cymbiformes is proposed and this section is represented by a new species A. angusticystidiatus. This new section is characterised by the strong iodoform odour of basidiomes and cymbiform basidiospores. Descriptions, colour photographs and illustrations are presented.
New taxa, Agaricaceae , Phylogeny, Taxonomy
Agaricus L. 1753 (Agaricaceae, Agaricales) is a well-known genus. Many species in this genus are commercially cultivated and served as food. One of the popular edible mushrooms is A. bisporus (J.E. Lange) Imbach, which is the most extensively cultivated mushroom in the world, accounting for 38% of world production (ISMS Edible mushrooms 2017, http://www.isms.biz/edible-mushrooms/). Another popular edible mushroom, A. subrufescens Peck, is also a medicinal mushroom and contains abundant bioactive compounds, for example, some compounds extracted from the basidiomes can be used as antioxidant (
The taxonomic, systematic and species delimitation of Agaricus inferred by morphology are variable (Cappelli 1984,
In this study three interesting specimens found near Chiang Mai, Thailand were analysed morphologically and molecularly. We provide a full description and analyses are presented to support the distinction of this material as a new species and section in subgenus Pseudochitonia.
Photographs were taken immediately in situ, in the field in Thailand. Basidiomes were wrapped in aluminium foil or kept in plastic boxes separately. Macro morphological characteristics were recorded when specimens were fresh. Every specimen was completely dried in an electrical food drier at 60 °C, then kept in a plastic ziplock bag and deposited in Herbarium Mycologicum Academiae Sinicae (HMAS), Mae Fah Luang University Herbarium (
At the Institute of Microbiology Chinese Academy of Science, genomic DNA was extracted from dry specimens by using an E.Z.N.A. Forensic DNA Extraction Kit (D3591-01, Omega Bio-Tek) following the manufacturer’s protocol. PCR amplification was performed following
A total of 119 specimens representing 87 species were incorporated in phylogenetic analyses. Three new sequences representing A. angusticystidiatus were generated from this study. They are one ITS sequence from specimen BC088 and two LSU sequences from ZRL2085 and ZRL2043 separately. Details of all sequences are listed in Table
Taxa information used in the phylogenetic analyses, new taxa are in bold, “T” refers to type.
Species Name | Collection Number | LSU | ITS | tef1-α | Origin |
---|---|---|---|---|---|
Agaricus abruptibulbus | ZRL2012005 | KT951460 | KT951356 | KT951626 | Yunnan, China |
A. albosquamosus T | LD2012192 | KT951520 | KT951394 | KT951636 | Thailand |
A. amoenus T | ZRL2010072 | KT951524 | KT951348 | KT951638 | Yunnan, China |
A. angusticystidiatus | BC088 | – | MG888054 | – | Thailand |
A. angusticystidiatus | ZRL2085 | MG835413 | KT951434 | – | Thailand |
A. angusticystidiatus T | ZRL2043 | MG835412 | JF691553 | – | Thailand |
A. atrodiscus | LD2012185 | KT951473 | KT284912 | KT951653 | Thailand |
A. benesii | LAPAG283 | – | JF797179 | – | Burgos, Spain |
A. bernardiformis | CA433 | KT951467 | KT951321 | KT951577 | – |
A. biannulatus | LAPAG611 | – | JF896229 | – | Sardinia, Italy |
A. biberi | LAPAG687 | KR006614 | KM657919 | KR006642 | Hungary |
A. bingensis | ADK1992 | – | KJ540954 | – | Atakora, Benin |
A. bisporiticus | LD2012111 | KT951507 | KJ575611 | KT951650 | Thailand |
A. bisporiticus | MCR25 | – | KJ575608 | – | Pakistan |
A. bisporus | LAPAG446 | KR006611 | KM657920 | KR006640 | Burgos, Spain |
A. bitorquis | CA427 | KT951491 | KT951320 | KT951646 | |
A. bitorquis | WZR2012827 | KT951492 | KM657916 | KT951647 | Xingjiang, China |
A. bohusii | LAPAG562 | KR006613 | KM657928 | KR006641 | Madrid, Spain |
A. boisseletii | CA123 | – | DQ182531 | – | – |
A. brunneopictus | ADK2564 | – | JF514518 | – | Plateau Atlantique, Bénin |
A. brunneopileatus T | ZRL2012115 | KT951489 | KT951404 | KT951587 | Yunnan, China |
A. brunneosquamulosus | LD2012105 | – | KJ540968 | – | Thailand |
A. brunneosquamulosus | ZRL4017 | – | JF691549 | – | Thailand |
A. caballeroi | AH44503 | – | KJ575605 | – | Spain |
A. campestris | LAPAG370 | KR006607 | KM657927 | KR006636 | Madrid, Spain |
A. campestroides | LAPAF2 | – | JF727842 | – | Plateaux, Togo |
A. candidolutescens T | LD2012129 | KT951525 | KT951335 | KT951616 | Thailand |
A. cf. bernardi | CA383 | KT951469 | KT951319 | KT951576 | |
A. cf. goossensiae | ADK2171 | – | JF514517 | – | Borgou, Benin |
A. chiangmaiensis | NTS113 | – | JF514531 | – | Thailand |
A. comtulus | LAPAG724 | KT951448 | KT951332 | KT951593 | Burgos, Spain |
A. crassisquamosus T | ZRL2012607 | KT951510 | KT951376 | KT951645 | Tibet, China |
A. cupressicola | LAPAG889 | KT951465 | KT951334 | KT951649 | Roma, Italy |
A. desjardinii | WZR2012907 | KT951474 | KM657901 | KT951644 | Xinjiang, China |
A. dilutibrunneus T | ZRL2012010 | KT951512 | KT951358 | KT951569 | Yunnan, China |
A. dolichopus | ZRL2012715 | KT951502 | KT951382 | KT951573 | Tibet, China |
A. dolichopus | ZRL2014120 | – | KT951433 | – | – |
A. duplocingulatus | ZRL3064 | – | KJ540966 | – | Thailand |
A. erectosquamosus T | LD2012165 | KT951509 | KT951338 | KT951565 | Thailand |
A. erythrosarx | MURU6080 | – | JF495068 | – | – |
A. freirei | CA186 | – | DQ185553 | – | – |
A. fuscofibrillosus | WC913 | – | AY484684 | – | – |
A. fuscopunctatus | LD2012115 | – | KJ575612 | – | Thailand |
A. fuscovelatus | RWK2100 | – | KJ577973 | – | – |
A. gennadii | CA339 | – | KT951318 | KT951575 | – |
A. grandiomyces T | ZRL2012611 | KR006624 | KM657879 | KR006652 | Tibet, China |
A. gratolens | ZRL3093 | KT951488 | JF691548 | – | Thailand |
A. haematinus | ZRL2109 | – | KT951435 | – | Thailand |
A. haematinus | ZRL2136 | – | JF691552 | – | Thailand |
A. hondensis | RWK1938 | – | DQ182513 | – | USA |
A. huijsmanii | LAPAG639 | KT951444 | KF447889 | KT951571 | Navarra, Spain |
A. kunmingensis | ZRL2012015 | KT951506 | KT951361 | KT951642 | Yunnan, China |
A. kunmingensis | ZRL2012007 | – | KT951427 | – | Yunnan, China |
A. lamellidistans T | ZRL3099 | – | JF691556 | – | Thailand |
A. laskibarii | LAPAG115 | – | AY943975 | – | Landes, France |
A. leucocarpus T | LD2012159 | KX083981 | KU975101 | KX198048 | Thailand |
A. leucolepidotus T | LD201214 | KT951519 | KT951336 | KT951635 | Thailand |
A. linzhiensis T | ZRL2012618 | KT951503 | KT951378 | KT951582 | Tibet, China |
A. litoralis | LAPAG420 | KT951483 | KT951327 | KT951572 | Burgos, Spain |
A. litoraloides | ZRL2011249 | KT951523 | KT951353 | KT951580 | Yunnan, China |
A. magnivelaris | F2389 | – | JF727851 | – | – |
A. martinicensis | F2815 | KX084032 | JF727855 | KX198038 | MartiniqueFrance |
A. megacystidiatus | LD2012179 | – | KF305946 | – | Thailand |
A. microvolvatulus | LD201271 | KT951508 | KJ575614 | KT951651 | Thailand |
A. murinocephalus | ZRL3044 | – | JF691555 | – | Thailand |
A. nevoi | LAPAG257 | KR006606 | KM657922 | KR006635 | Burgos, Spain |
A. nevoi | LAPAG535 | – | KT951330 | KT951574 | Teruel, Spain |
A. nigrobrunnescens | DEH632 | – | JX308267 | – | Hawaii, USA |
A. nigrogracilis T | ZRL2012014 | KR006621 | KM657882 | KR006647 | Yunnan, China |
A. niveogranulatus | LD201124 | – | KJ540959 | – | Thailand |
A. padanus | WZR2012903 | KR006616 | KM657903 | KR006644 | Xingjiang, China |
A. pallidobrunneus T | ZRL2012358 | KT951471 | KT951370 | KT951566 | Yunnan, China |
A. parvitigrinus | CA158 | – | AY899267 | – | – |
A. pattersoniae | RWK1415 | – | AY943974 | – | – |
A. phaeolepidotus | CA217 | – | DQ185552 | – | – |
A. pilosporus | LAPAG227 | – | KT951425 | – | Burgos, Spain |
A. pseudolangei | ZRL3012 | – | JF691551 | – | Thailand |
A. rufoaurantiacus | LAPAM15 | KX671708 | KT951313 | KT951641 | Dominican Republic |
A. silvaticus | ALG07 213 | KT951307 | KT951567 | Algonquin, ON, Canada | |
A. sinodeliciosus | WZR2012822 | KT951518 | KM657907 | KT951648 | Xingjiang, China |
A. sordidocarpus | LD201237 | – | KJ540946 | – | Thailand |
A. subrufescens | ZRL2012722 | KT951451 | KT951383 | KT951632 | Yunnan, China |
A. subsaharianus | ADK4732 | – | JF440300 | – | Ouagadougou, Burkina Faso |
A. sylvaticus | LAPAG382 | KR006608 | KM657929 | KR006637 | Burgos, Spain |
A. sylvaticus | ZRL2012013 | KT951500 | KT951360 | KT951570 | Thailand |
A. sylvaticus | ZRL2012568 | KT951501 | KT951371 | KT951568 | Tibet, China |
A. tibetensis | ZRL2012585 | KR006633 | KM657895 | KR006658 | Tibet, China |
A. tollocanensis | CA235 | – | AY703913 | – | – |
A. toluenolens | CA911 | – | KJ540947 | – | – |
A. trisulphuratus complex | LAPAF7 | KR006605 | KM657924 | KR006634 | Plateaux, Togo |
A. trisulphuratus complex | Swk079 | KT951472 | KT951343 | KT951561 | Lanjak-Entimau, Malaysia |
A. trisulphuratus complex | ZRL2014023 | – | KT951428 | – | China |
A. trisulphuratus complex | ZRL2014024 | – | KT951429 | – | China |
A. trisulphuratus complex | ZRL2014030 | – | KT951432 | – | China |
A. trisulphuratus complex | ZRL2132 | – | JF691558 | – | Thailand |
A. tytthocarpus | ZRLWXH3077 | KR006618 | KM657889 | KR006645 | Fujian, China |
A. variabilicolor | ZRL4002 | – | KT951438 | – | Thailand |
A. variabilicolor | ZRL4007 | – | KT951439 | – | Thailand |
A. variabilicolor | ZRL4012 | – | KT951440 | – | Thailand |
A. variicystis | LD201228 | – | KT951426 | – | Thailand |
A. variicystis T | LD201234 | KT951517 | KT951339 | KT951562 | Thailand |
A. xanthodermulus | CA160 | – | AY899273 | – | – |
A. xanthodermus | CA15 | – | AY899271 | – | – |
A. xanthodermus | LAPAG387 | KR006609 | KM657923 | KR006638 | Soria, Spain |
A. xanthosarcus | Goossens5415 | – | JF514523 | – | – |
A. sp. | CA486 | – | JF797189 | – | – |
A. sp. | CA820 | – | JF727861 | – | – |
A. sp. | LD2012162 | KT951493 | KT951337 | KT951563 | Thailand |
A. sp. | NT020 | – | JF797197 | – | Thailand |
A. sp. | Swk014 | KT951482 | KT951342 | KT951654 | Lanjak-Entimau, Malaysia |
A. sp. | ZRL133 | KT951505 | KT951344 | KT951656 | Thailand |
A. sp. | ZRL2010010 | KT951511 | KT951347 | KT951639 | Thailand |
A. sp. | ZRL2010099 | KT951479 | KT951349 | KT951564 | Yunnan, China |
A. sp. | ZRL2012267 | KT951504 | KT951368 | KT951655 | Yunnan, China |
A. sp. | ZRL2012629 | KR006627 | KM657890 | KR006656 | Tibet, China |
A. sp. | ZRLWXH3078 | KT951464 | KT951464 | KT951643 | Fujian, China |
A. sp. | ZRLWXH3161 | KT951526 | KT951391 | KT951615 | Guangdong, China |
A. sp. | ZRLWXH3140 | – | KT951441 | – | Guangdong, China |
Heinemannomyces sp. | ZRL185 | KT951527 | KT951346 | KT951657 | Thailand |
The Bayesian tree from ITS sequences is shown in Figure
Phylogenetic tree of Agaricus subgenus Pseudochitonia generated from Bayesian analysis of ITS sequences, rooted with A. campestris. Bayesian posterior probability (PP) values ≥ 0.9 or Bootstrap support (BS) values ≥ 50% are indicated at the internodes (PP/BS). The branches in bold mean the related PP > 0.95, “T” refers to sequences from type specimen.
The multi-gene MCC tree is shown in Figure
Maximium Clade Credibility tree of genus Agaricus based on ITS, LSU and tef1-α gene sequences with the outgroup Heinemannomyces sp. Posterior probability values equal or above 0.9 are annotated at the internodes. The 95% highest posterior density of divergence time estimation are marked by horizontal bars.
Agaricus angusticystidiatus M.Q. He, Desjardin., K.D. Hyde & R.L. Zhao
In reference to the cymbiform basidiospores.
KOH reaction negative, Schäffer’s reaction negative on dry specimens. No discolouration on touching, but discolouration reddish-brown on cutting. Annulus membranous. Smell strong iodoform. Basidiospores cymbiform and cheilocystidia narrow with variable shapes.
refers to the narrow clavate cheilocystidia.
Thailand, Chiang Mai Province, Mae Taeng, Baan Mae Sae village, on Hwy 1095 near 50 km marker, 19°14.599'N, 98°39.456'E, alt. 960 m. In rain forest dominated by Castanopsis armata, Castanopsis sp., Pinus sp., Lithocarpus sp., 26 June 2005, collected by Jennifer Kerekes. Holotype: ZRL2043 (HMAS279593); Isotype: BBH19428 and SFSUZRL2043,
Pileus 40–80 mm diam., plano-convex, applanate, broadly umbonate; surface concentric squamulose with small skull-cup at disc, appressed, slightly fissured, light brown (6D8), brown (7E3), greyish-brown (5D5), dark brown (6D6) against the grey (8E3) background. Context 4–5 mm thick at disc, fragile, white to grey (8E3) in age. Lamellae free, crowded, lamellulae with 3–4 lengths, 3–4 mm broad, normal to slightly ventricose, brown (7E5) to dark brown (7F7-8), edge colour similar to the gill itself. Stipe 55–100 × 5–8 (base 8–15) mm, cylindrical bulbous, with rhizomorphs in most cases, hollow, surface glabrous to silky, white to dark brown (6D6). Annulus pendent or percurrent; single; upper side membranous, white; lower side surface powdery, light yellow (4B2) grain-like dots in circulate; superior, persistent, edge entire, up to 5 mm broad. Smell of iodoform. No colour change on touching; light dull red, greyish brown (7D4) on cutting.
KOH reaction: negative. Schäffer’s reaction: negative on dry specimens.
Basidiospores 5–6.5 × 3–4 (–4.5) µm [X = 5.6 ± 0.5 × 3.8 ± 0.4, Q = 1.1–2.2, Qm = 1.52 ± 0.7, n = 20], cymbiform, some endosporium, no germ pore, brown. Basidia 10–15 × 5.5–7 µm, clavate, hyaline, smooth, 4-spored. Pleurocystidia absent. Cheilocystidia 20–30 (–45) × 5–8 µm, occasionally one septum, narrowly clavate to clavate, some with elongated top, rarely subcapitate, hyaline, smooth. Pileipellis cutis consisting of 3–5 µm diam. hyphae, hyaline, smooth, non-constricted at septa. Annulus hyphae same as pileipellis.
Gregarious on soil in rain forest which is mainly dominated by Castanopsis armata, Castanopsis sp., Pinus sp., Lithocarpus sp.
Thailand, Chiang Mai Province (type distribution).
Thailand, Chiang Mai Province, Mae Taeng, Ban Mae Sae Village, on Hwy 1095 near 50 km marker, 19°14.599'N, 98°39.456'E, elev. ca. 960 m, 3 July 2004, collected by Thitiya Boonpratuang, ZRL2085 (HMAS279594, BBH19468 and SFSUZRL2085); Thailand, Chiang Mai Province, Mae Taeng, Mushrooms research center, 30 July 2014, collected by Boontiya Chuankid, BC088 (
This new species is morphologically distinguished from other Agaricus species by its strong iodoform smell, context reddish-brown discolouration on cutting, cymbiform basidiospores and narrow cheilocystidia with variable shapes. Phylogenetic analyses confirmed it is a member of the subgenus Pseudochitonia with an isolated phylogenetic position in Agaricus. This new species is similar to A. iodolens Heinem. & Gooss.-Font. of section Xanthodermatei, because both have relatively slender basidiomes and odour of iodine (
Based on phylogenetic and morphological studies, we propose A. angusticystidiatus as a new species in subgenus Pseudochitonia. Furthermore, the dating analysis, based on multi-gene sequences, indicated that A. angusticystidiatus diverged at 26.7 Ma which is slightly older than other sections in Agaricus (18–26 Ma, in
As mentioned before, this proposed new section Cymbiformes has a closely phylogenetic relationship with sections Trisulphurati and Crassispori. In morphology, all of them differed with other sections of Agaricus by the combination of negative Schäffer’s reaction, chemical odours such as phenol, ink or carbolic acid and basidiospores endosporium and often cymbiform. However, section Trisulphurati has woolly squamules on the surfaces of the pileus and stipe and the other two sections only have appressed squamules at the centre of the pileus. Furthermore, this new section Cymbiformes could be separated from section Crassispori by its negative KOH reaction and developed annulus (the latter is positive KOH reaction and with fragile annulus) (
So far, section Cymbiformes is only known from a tropical area. The cymbiform basidiospores are rare in Agaricus species. Presently there are three Agaricus species from tropical areas which have this kind of basidiospores. They are A. angusticystidiatus of section Cymbiformes and A. lamellidistans and A. variicystis of section Crassispori (
This project was conducted under the financial support of the National Key R&D Program of China (Project No. 2018YFD0400200), the National Natural Science Foundation of China (Project ID:31470152 and 31360014) and Beijing Innovative Consortium of Agriculture Research System (Project ID: BAIC05-2018).