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Hygrophorus Annulatus, a New Edible Member of H. Olivaceoalbuscomplex from Southwestern China

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Hygrophorus Annulatus, a New Edible Member of H. Olivaceoalbuscomplex from Southwestern China Mycoscience VOL.62 (2021) 137-142 Short communication Hygrophorus annulatus, a new edible member of H. olivaceoalbus- complex from southwestern China Chao-Qun Wanga, Tai-Hui Lia,*, Xiang-Hua Wangb, Tie-Zheng Weic, Ming Zhanga, Xiao-Lan Hed a Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, State Key Laboratory of Applied Microbiology Southern China, Guang- dong Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, Guangdong, China b CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China c State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China d Soil and Fertilizer Institute, Sichuan Academy of Agricultural Sciences, Chengdu 610066, Sichuan, China ABSTRACT Members of Hygrophorus olivaceoalbus-complex or olive waxcaps have both ecological and economic significance. European and North American species diversity of this fungal group has been presented in recent molecular phylogenetic studies, but no Chinese materials were included. In this study, a phylogenetic overview of the H. olivaceoalbus-complex based on internal transcribed spacer (ITS) sequenc- es was made, and a local popular edible species from southwestern China was described as a new species H. annulatus. This new species is characterized by grayish brown, olive brown to dark brown pileus disc, inflexed to deflexed pileus margin, obvious and dark brown annulus, basidiospores measuring (8.0–)8.5–11.0(–12.0) × 5.0–7.5(–8.0) μm, and the distribution in subalpine forests dominated by Abies and/or Picea in southwestern China. Keywords: Basidiomycota, Hygrophoraceae, olive waxcaps, phylogeny, taxonomy Article history: Received 30 July 2020, Revised 13 January 2021, Accepted 14 January 2021, Available online 20 March 2021. Hygrophorus olivaceoalbus-complex is a striking group within olivaceoalbus”, but in phylogenetic trees, some of them appeared in the genus Hygrophorus (Hygrophoraceae, Agaricales) for having different lineages, implying that those samples of “H. olivaceoal- very slimy basidioma, gray-brown to gray-olive pileus, and two veils bus” represent a species complex, and this kind of morphological on the stipe. This group belongs to subg. Colorati (Bataille) E. plasticity is prevalent in this genus (Lodge et al., 2014; Razaq et al., Larss., sect. Olivaceoumbrini (Bataille) Konrad & Maubl., subsect. 2014; Moreau et al., 2018; Naseer et al., 2019). Although “H. oliva- Olivaceoumbrini (Bataille) Singer (Lodge et al., 2014). Morphologi- ceoalbus” was reported from China (Yuan & Sun, 2007; Chen & Li, cal and molecular analyses have shown that the complex includes 2013), no Asian ITS sequence of the H. olivaceoalbus-complex has three known European species [H. fuscoalbus (Lasch) Fr., H. kor- been deposited in public databases (GenBank [https://www.ncbi. honenii Harmaja, and H. olivaceoalbus (Fr.) Fr.] and an undescribed nlm.nih.gov/genbank/] and UNITE [https://unite.ut.ee/]; Ac- species from North America (Fries, 1838; Harmaja, 1985; Moreau cessed on 10 June 2020) or included in publications until now. et al., 2018). Among them, H. olivaceoalbus is the most common Previous studies indicated that the species diversity of the complex and well documented species in numerous European atlases, e.g. has been understudied. During a series of investigations on wax- Candusso (1997), Campo (2015), Læssøe and Petersen (2019), and caps in China, some H. olivaceoalbus-like mushrooms, with less in some North American ones as well (Hesler & Smith, 1963). Eco- slimy pilei, denser lamellae and well-developed annulus on the logically, the species of H. olivaceoalbus-complex are considered to stipe, were found in fields and local markets in southwestern Chi- form ectomycorrhizae on host plant roots; H. korhonenii and H. na. To determine the phylogenetic position of these Chinese collec- olivaceoalbus are usually associated with Picea abies (L.) Karst. tions and clarify the genetic diversity within the complex, we made (Harmaja, 1985; Læssøe & Petersen, 2019), whereas the host associ- a phylogenetic overview of H. olivaceoalbus-complex using all ation of H. fuscoalbus is not clear. available ITS sequences from Asia, Europe, and North America. Numerous internal transcribed spacer (ITS) sequences from The result show that the ITS sequence data from the Chinese sam- Europe and North America in public databases were labeled as “H. ples represent an independent and unique lineage within the H. olivaceoalbus-complex. This lineage is here documented and de- * Corresponding author. scribed as a new species. E-mail address: [email protected] (T.H. Li) Fresh specimens were photographed and recorded in the field This is an open-access paper distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivative 4.0 international license (CC BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/). doi: 10.47371/mycosci.2021.01.001 ― 137 ― C.-Q. Wang et al. / Mycoscience VOL.62 (2021) 137-142 and dried in a Dörrex dehydrator (Stockli, Switzerland) or other Taxonomy electric driers at 50 °C overnight. Macro-morphological characters were noted from the specimen records and photographs. Color Hygrophorus annulatus C.Q. Wang & T.H. Li, sp. nov. names and codes were given according to Kornerup and Wanscher Figs. 2, 3. (1978). Micro-morphological characters of the dry specimens were MycoBank no.: MB 836177. observed and measured using AX10 light microscopy and ZEN 2 lite software (Carl Zeiss Inc., Oberkochen, Germany). Dry tissues Diagnosis: Hygrophorus annulatus differs from the other species were rehydrated in water to observe colors and gelatinous zones of of H. olivaceoalbus-complex by the DNA sequences, obvious and pileipellis, and in 5% KOH then mounted with 1% Congo red to dark brown annulus, shorter basidiospores measuring (8.0–)8.5– measure basidiospores, basidia, pileipellis, stipitipellis, and hy- 11.0(–12.0) × 5.0–7.5(–8.0) μm, and the distribution in subalpine menophoral trama. For each individual, 20 basidiospores and 10 forests dominated by Abies forrestii Coltm.-Rog., A. georgei Orr, Pi- basidia were randomly selected and measured. Q value refers to the cea asperata Mast., P. likiangensis (Franch.) Pritz. in southwestern length/width ratio of basidiospores and basidia. Size and Q value China. dimensions of basidiospores and basidia are described with the Type: CHINA. Sichuan Province, Garze Tibetan Autonomous notation (a–)b–c(–d): the range ‘b–c’ represents 90% of the mea- Prefecture, Kangding City, Mugecuo, on the ground of a forest sured values, and ‘a’ and ‘d’ represent extreme values. Qm/Lm/Wm dominated by Picea asperata, 30°11′N, 101°54′E, elev. ca 3400 m, 4 refers to the average of Q values/length/width ± standard devia- Aug 2015, M. Zhang (GDGM45124, holotype). tion. Specimens are deposited in the Fungarium of Guangdong In- Gene sequence ex-holotype: MT758324 (ITS). stitute of Microbiology (GDGM), the Herbarium of Mycology, Aca- Etymology: annulatus means annulate, referring to the well-de- demia Sinica (HMAS), the Herbarium of Cryptogams at the veloped ring on the stipe. Kunming Institute of Botany, Chinese Academy of Sciences (KUN- Pileus (20–)40–70(–100) mm, hemispherical to convex when HKAS), and the Mycological Herbarium of Soil and Fertilizer Insti- young, becoming subumbilicate, plano-convex or applanate when tute, Sichuan Academy of Agricultural Sciences (SAAS). mature, grayish brown (6E3–4), olive brown (4F3–7) to dark brown Genomic DNA was extracted from the dry specimens using the (6F3–7) at disc, lighter towards the margin, light brown (6D4), HiPure Fungus DNA Mini Kit (Magen Biotech Co., Ltd., Guang- brownish gray (6C2) to gray (6B1, 6C1) from outer zone of disc to zhou, China) according to the manufacturer’s instructions. Se- pileus margin, sticky when wet; margin involute at the beginning quences of nuclear ribosomal ITS region were amplified by Poly- and then inflexed to deflexed, entire to irregularly fissured, even to merase Chain Reaction (PCR), using primers ITS1F and ITS4 wavy. Context up to 12 mm thick, white, soft. Lamellae narrowly (White et al., 1990; Gardes & Bruns, 1993). The PCR procedure for adnate with a decurrent tooth or subdecurrent, up to 5 mm broad, ITS was as follows: initial denaturation at 94 °C for 5 min, followed subdistant, white, sometimes with pinkish tint, waxy, with 1–3 by 35 cycles at 94 °C for 40 s, 52 °C for 40 s and 72 °C for 1 min, and lamellulae of different lengths between two complete lamellae; a final extension of 72 °C for 8 min. Amplified PCR products were edge even, concolorous. Stipe 60–150 × 5–20 mm, central, subcylin- cleaned and sequenced by Beijing Liuhe Co., Limited (Guangzhou, drical, nearly equal to slightly tapering upwards, solid, with a China) on an ABI 3730 DNA sequencer analyzer (Applied Biosys- brownish annulus or partial veil at upper part of stipe, white above tems, Foster City, CA, USA) with the same primers. Raw abi format the annulus, covered with grayish to dark brown (6F4–7) fibers sequences of both directions were assembled and unrecognized below, which usually form several vague to rather clear annular starting and ending base pairs were trimmed using SeqMan soft- stripes or bands, usually with white mycelium at base. Annulus ware version 7.1.0 (DNASTAR, Inc.). The consensus sequences superior, at an area of about 1 cm below the stipe apex when ma- have been deposited in GenBank (accession nos. MT758317– ture, as one or two layers of fibrous veil, connecting pileus margin MT758341). and stipe when young, leaving a strong dark brown (concolorous Phylogenetic analyses were conducted to elucidate the phyloge- with pileus disc) annulus and usually a weaker (concolorous to the netic position of the Chinese specimens and to examine the rela- pileus margin) ring on the stipe when mature, fibrous. Odor and tionships among the members of the H. olivaceoalbus-complex. taste mild. Edible. Fifty-eight downloaded and 25 newly generated ITS sequences of Basidiospores (8.0–)8.5–11.0(–12.0) × 5.0–7.5(–8.0) μm, Lm = the H.
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