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Evidence for Inbreeding and Genetic Differentiation Among Geographic Populations of the Saprophytic Mushroom Trogia Venenata from Southwestern China

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Evidence for Inbreeding and Genetic Differentiation Among Geographic Populations of the Saprophytic Mushroom Trogia Venenata from Southwestern China RESEARCH ARTICLE Evidence for Inbreeding and Genetic Differentiation among Geographic Populations of the Saprophytic Mushroom Trogia venenata from Southwestern China Fei Mi1,2☯, Ying Zhang1☯, Dan Yang1, Xiaozhao Tang1, Pengfei Wang1, Xiaoxia He1, Yunrun Zhang1, Jianyong Dong1, Yang Cao3, Chunli Liu4, Ke-Qin Zhang1, Jianping Xu1,5* 1 Laboratory for Conservation and Utilization of Bio-Resources, and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming, Yunnan, PR China, 2 Institute of Communicable Disease Control and Prevention, Guizhou Provincial Centre for Disease Control and Prevention, Guiyang, Guizhou, PR China, 3 Yunnan Institute for Tropical Crop Research, Jinghong, Yunnan, PR China, 4 Kunming Edible Fungi Institute of All China Federation of Supply and Marketing Cooperatives, Kunming, Yunnan, PR China, 5 Department of Biology, McMaster University, Hamilton, Ontario, Canada ☯ These authors contributed equally to this work. * [email protected] OPEN ACCESS Citation: Mi F, Zhang Y, Yang D, Tang X, Wang P, He X, et al. (2016) Evidence for Inbreeding and Genetic Abstract Differentiation among Geographic Populations of the Saprophytic Mushroom Trogia venenata from During the past 40 years, more than 400 Sudden Unexplained Deaths (SUDs) have Southwestern China. PLoS ONE 11(2): e0149507. occurred in Yunnan, southwestern China. Epidemiological and toxicological analyses sug- doi:10.1371/journal.pone.0149507 gested that a newly discovered mushroom called Trogia venenata was the leading culprit for Editor: Erika Kothe, Friedrich Schiller University, SUDs. At present, relatively little is known about the genetics and natural history of this GERMANY mushroom. In this study, we analyzed the sequence variation at four DNA fragments Received: July 29, 2015 among 232 fruiting bodies of T. venenata collected from seven locations. Our ITS sequence Accepted: February 2, 2016 analyses confirmed that all the isolates belonged to the same species. The widespread presence of sequence heterozygosity within many strains at each of three protein-coding Published: February 18, 2016 genes suggested that the fruiting bodies were diploid, dikaryotic or heterokaryotic. Within Copyright: © 2016 Mi et al. This is an open access individual geographic populations, we found significant deviations of genotype frequencies article distributed under the terms of the Creative Commons Attribution License, which permits from Hardy-Weinberg expectations, with the overall observed heterozygosity lower than unrestricted use, distribution, and reproduction in any that expected under random mating, consistent with prevalent inbreeding within local popu- medium, provided the original author and source are lations. The geographic populations were overall genetically differentiated. Interestingly, credited. while a positive correlation was found between population genetic distance and geographic Data Availability Statement: All relevant data are distance, there was little correlation between genetic distance and barium concentration dif- within the paper and its Supporting Information files. ference for the geographic populations. Our results suggest frequent inbreeding, geo- Funding: This study was jointly supported by grants graphic structuring, and limited gene flow among geographic populations of T. venenata from the Yunnan Provincial Department of Science from southwestern China. and Technology (2010CI106), National Natural Science Foundation Program of the People’s Republic of China (31100018 and 31470147), and Education Department of Yunnan Province (2014Z005). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. PLOS ONE | DOI:10.1371/journal.pone.0149507 February 18, 2016 1/21 Inbreeding and Genetic Differentiation of T. venenata Competing Interests: The authors have declared Introduction that no competing interests exist. Since 1978, more than 400 apparently healthy persons have died suddenly without any obvious Abbreviations: JZSH, Jizushan, a village in causes in Yunnan, southwestern China [1, 2]. Those Sudden Unexplained Deaths (SUDs) often Bingchuan county; LXJ and MG respectively, Lixiji and Moguang, two villages in Heqing county; XY, occurred during the rainy season, from June to August, in remote areas surrounded by moun- represents Xiangyun county; SY, represents Shiyang, tains at altitudes between 1800 and 2400 m [3]. This serious medical mystery attracted broad a village in Dayao; JTand QS, represent Jietou and concerns from national and local governments. Various hypothetical causes have been pro- Qushi respectively, two villages in Tengchong county; posed, including Keshan (a viral disease), heavy metal poisoning, drinking water contaminated LWM, little white mushroom, a common local name with toxins or pathogens, and mushroom poisoning [1]. In China, about 3,800 species of for Trogia venenata. mushrooms have been catalogued and 421 of which are considered poisonous and unfit for human consumption [4]. However, edible and poisonous mushrooms are often difficult to dis- tinguish and incidents of mushroom poisoning are reported every year in southern China [5]. Due to the temporal clustering of SUDs around the July-August rainy season that favors mush- room fruiting and the observation that some of the households with incidents of SUDs had eaten a mushroom called the “Little White Mushroom (LWM)”, this mushroom soon became the leading culprit for SUDs. Subsequent studies identified two unusual and toxic amino acids in the fruiting bodies of LWM [6]. Indeed, recent public health campaigns warning people against consuming this and other potentially poisonous mushrooms have led to a significant reduction of SUDs in Yunnan, consistent with a potentially important role for this mushroom in SUDs. Very little, however, is known about the genetics and general biology of this mushroom. Morphologically, the fruiting body of LWM is white when fresh and looks like a ginkgo leaf. Its fruiting body is usually about 5cm long and 3cm wide, typically found as clusters on rotten wood. Fruiting bodies of LWM are fragile and easy to break. Based on its morphological fea- tures and sequences at the internal transcribed spacer (ITS) regions of the nuclear ribosomal RNA gene, Yang et al. [7] classified this mushroom as a new species of the basidiomycete genus Trogia and named the LWM Trogia venenata. At present, this species is only found in the mountains in central and western parts of Yunnan Province. Previous studies have shown that saprophytic fungi are generally opportunistic in their eco- logical distributions and are found wherever substrates (e.g. dead organic matter such as rotten wood) and growth conditions permit [8]. Indeed, frequent gene flows have been found among populations of saprophytic mushrooms (e.g. Agaricus species, Lepiota cristata, etc) [9]. Such gene flow could be accomplished through either basidiospore dispersals and/or anthropogenic activities [9]. Here, we hypothesize that populations of the saprophytic T. venenata from Yun- nan will also show frequent gene flow and limited geographic differentiation. Multilocus sequence typing (MLST) [10] and multiple gene genealogy analysis (MGGA) [11] have become popular methods for studying population biology and molecular ecology. Such studies have helped resolve a diversity of biological issues such as the modes of reproduc- tion, cryptic speciation, gene flows, phylogeography, horizontal gene transfer, as well as eco- logical adaptation in a diversity of microorganisms [12, 13]. For example, genealogical analyses of DNA sequences at five mitochondrial loci and their comparisons with four nuclear loci iden- tified evidence of horizontal gene transfer and recombination in the mitochondrial genomes of the saprophytic and opportunistic human pathogenic yeast Cryptococcus gattii [14]. In addi- tion, there was abundant evidence for gene flow among geographic regions and the largely con- gruent phylogenetic pattern between the mitochondrial and nuclear genes suggest historical divergence and cryptic speciation within C. gattii [15, 16]. In the saprophytic mushroom L. cristata, MGGA identified long distance dispersal and recombination [9]. In this study, we collected 232 fruiting body samples of T. venenata from seven sites in Yun- nan province representing the broad geographic distribution range of SUDs. ITS sequences PLOS ONE | DOI:10.1371/journal.pone.0149507 February 18, 2016 2/21 Inbreeding and Genetic Differentiation of T. venenata were first obtained from representative samples at each of the seven sites to confirm species identity. These samples were then analyzed for sequence variation at the following three pro- tein-coding genes: the second largest subunit of RNA polymerase II gene (rpb2), the translation elongation factor 1-α gene (tef1-α), and the β tubulin gene (β-tub). The sequences were ana- lyzed to identify the patterns of genetic variation within and among populations. In addition, we also analyzed the putative relationships between genetic differentiation and the concentra- tion of the heavy metal barium related to the seven sampled sites in T. venenata. A high con- centration of barium in this mushroom was originally suspected as a major contributor to SUDs [1]. However, a later analysis refuted the hypothesis that this mushroom preferentially accumulated barium in its fruiting bodies and concluded that barium in T. venenata was unlikely a contributor to SUDs [17]. Despite
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