Phylogenetic Analyses of Armillaria Reveal at Least 15 Phylogenetic Lineages in China, Seven of Which Are Associated with Cultivated Gastrodia elata
Identifieur interne : 000122 ( Pmc/Curation ); précédent : 000121; suivant : 000123Phylogenetic Analyses of Armillaria Reveal at Least 15 Phylogenetic Lineages in China, Seven of Which Are Associated with Cultivated Gastrodia elata
Auteurs : Ting Guo [République populaire de Chine] ; Han Chen Wang [République populaire de Chine] ; Wan Qiu Xue [République populaire de Chine] ; Jun Zhao [République populaire de Chine] ; Zhu L. Yang [République populaire de Chine]Source :
- PLoS ONE [ 1932-6203 ] ; 2016.
Abstract
Fungal species of
Url:
DOI: 10.1371/journal.pone.0154794
PubMed: 27138686
PubMed Central: 4854404
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Reveal at Least 15 Phylogenetic Lineages in China, Seven of Which Are Associated with Cultivated <italic>Gastrodia elata</italic>
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<affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>University of Chinese Academy of Sciences, No. 19A Yuquan Road, Beijing 100049, China</addr-line>
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<author><name sortKey="Wang, Han Chen" sort="Wang, Han Chen" uniqKey="Wang H" first="Han Chen" last="Wang">Han Chen Wang</name>
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<author><name sortKey="Xue, Wan Qiu" sort="Xue, Wan Qiu" uniqKey="Xue W" first="Wan Qiu" last="Xue">Wan Qiu Xue</name>
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<author><name sortKey="Zhao, Jun" sort="Zhao, Jun" uniqKey="Zhao J" first="Jun" last="Zhao">Jun Zhao</name>
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<author><name sortKey="Yang, Zhu L" sort="Yang, Zhu L" uniqKey="Yang Z" first="Zhu L." last="Yang">Zhu L. Yang</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Phylogenetic Analyses of <italic>Armillaria</italic>
Reveal at Least 15 Phylogenetic Lineages in China, Seven of Which Are Associated with Cultivated <italic>Gastrodia elata</italic>
</title>
<author><name sortKey="Guo, Ting" sort="Guo, Ting" uniqKey="Guo T" first="Ting" last="Guo">Ting Guo</name>
<affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming 650201, China</addr-line>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming 650201</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>University of Chinese Academy of Sciences, No. 19A Yuquan Road, Beijing 100049, China</addr-line>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>University of Chinese Academy of Sciences, No. 19A Yuquan Road, Beijing 100049</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wang, Han Chen" sort="Wang, Han Chen" uniqKey="Wang H" first="Han Chen" last="Wang">Han Chen Wang</name>
<affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>College of Life Sciences, Chongqing Normal University, Chongqing, 401331, China</addr-line>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Life Sciences, Chongqing Normal University, Chongqing, 401331</wicri:regionArea>
</affiliation>
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<author><name sortKey="Xue, Wan Qiu" sort="Xue, Wan Qiu" uniqKey="Xue W" first="Wan Qiu" last="Xue">Wan Qiu Xue</name>
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</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>College of Life Sciences, Chongqing Normal University, Chongqing, 401331</wicri:regionArea>
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<author><name sortKey="Zhao, Jun" sort="Zhao, Jun" uniqKey="Zhao J" first="Jun" last="Zhao">Jun Zhao</name>
<affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>General Station of Forest Pest Control, State Forestry Administration, Shenyang 110034, China</addr-line>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>General Station of Forest Pest Control, State Forestry Administration, Shenyang 110034</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Yang, Zhu L" sort="Yang, Zhu L" uniqKey="Yang Z" first="Zhu L." last="Yang">Zhu L. Yang</name>
<affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming 650201, China</addr-line>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming 650201</wicri:regionArea>
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<series><title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><p>Fungal species of <italic>Armillaria</italic>
, which can act as plant pathogens and/or symbionts of the Chinese traditional medicinal herb <italic>Gastrodia elata</italic>
(“Tianma”), are ecologically and economically important and have consequently attracted the attention of mycologists. However, their taxonomy has been highly dependent on morphological characterization and mating tests. In this study, we phylogenetically analyzed Chinese <italic>Armillaria</italic>
samples using the sequences of the internal transcribed spacer region, translation elongation factor-1 alpha gene and beta-tubulin gene. Our data revealed at least 15 phylogenetic lineages of <italic>Armillaria</italic>
from China, of which seven were newly discovered and two were recorded from China for the first time. Fourteen Chinese biological species of <italic>Armillaria</italic>
, which were previously defined based on mating tests, could be assigned to the 15 phylogenetic lineages identified herein. Seven of the 15 phylogenetic lineages were found to be disjunctively distributed in different continents of the Northern Hemisphere, while eight were revealed to be endemic to certain continents. In addition, we found that seven phylogenetic lineages of <italic>Armillaria</italic>
were used for the cultivation of Tianma, only two of which had been recorded to be associated with Tianma previously. We also illustrated that <italic>G</italic>
. <italic>elata</italic>
f. <italic>glauca</italic>
(“Brown Tianma”) and <italic>G</italic>
. <italic>elata</italic>
f. <italic>elata</italic>
(“Red Tianma”), two cultivars of Tianma grown in different regions of China, form symbiotic relationships with different phylogenetic lineages of <italic>Armillaria</italic>
. These findings should aid the development of Tianma cultivation in China.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27138686</article-id>
<article-id pub-id-type="pmc">4854404</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0154794</article-id>
<article-id pub-id-type="publisher-id">PONE-D-15-44992</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Computer and Information Sciences</subject>
<subj-group><subject>Data Management</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Molecular Biology</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Molecular Biology Assays and Analysis Techniques</subject>
<subj-group><subject>Phylogenetic Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Molecular Biology Assays and Analysis Techniques</subject>
<subj-group><subject>Phylogenetic Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Mycology</subject>
<subj-group><subject>Fungal Reproduction</subject>
<subj-group><subject>Fungal Spores</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject>
<subj-group><subject>Geographical Locations</subject>
<subj-group><subject>Asia</subject>
<subj-group><subject>China</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Molecular Biology</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Artificial Gene Amplification and Extension</subject>
<subj-group><subject>Polymerase Chain Reaction</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Artificial Gene Amplification and Extension</subject>
<subj-group><subject>Polymerase Chain Reaction</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Molecular biology</subject>
<subj-group><subject>Molecular biology techniques</subject>
<subj-group><subject>Sequencing techniques</subject>
<subj-group><subject>Sequence analysis</subject>
<subj-group><subject>DNA sequence analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and analysis methods</subject>
<subj-group><subject>Molecular biology techniques</subject>
<subj-group><subject>Sequencing techniques</subject>
<subj-group><subject>Sequence analysis</subject>
<subj-group><subject>DNA sequence analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Population Genetics</subject>
<subj-group><subject>Haplotypes</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Genetics</subject>
<subj-group><subject>Population Genetics</subject>
<subj-group><subject>Haplotypes</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Population Biology</subject>
<subj-group><subject>Population Genetics</subject>
<subj-group><subject>Haplotypes</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Molecular Biology</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Sequencing Techniques</subject>
<subj-group><subject>Sequence Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Sequencing Techniques</subject>
<subj-group><subject>Sequence Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Phylogenetic Analyses of <italic>Armillaria</italic>
Reveal at Least 15 Phylogenetic Lineages in China, Seven of Which Are Associated with Cultivated <italic>Gastrodia elata</italic>
</article-title>
<alt-title alt-title-type="running-head">Phylogeny of <italic>Armillaria</italic>
</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Guo</surname>
<given-names>Ting</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Han Chen</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Xue</surname>
<given-names>Wan Qiu</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhao</surname>
<given-names>Jun</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yang</surname>
<given-names>Zhu L.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Heilongtan, Kunming 650201, China</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>College of Life Sciences, Chongqing Normal University, Chongqing, 401331, China</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>University of Chinese Academy of Sciences, No. 19A Yuquan Road, Beijing 100049, China</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>General Station of Forest Pest Control, State Forestry Administration, Shenyang 110034, China</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Klopfenstein</surname>
<given-names>Ned B.</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>USDA Forest Service—RMRS, UNITED STATES</addr-line>
</aff>
<author-notes><fn fn-type="conflict" id="coi001"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: TG ZLY. Performed the experiments: TG WQX. Analyzed the data: TG ZLY HCW. Contributed reagents/materials/analysis tools: TG HCW JZ. Wrote the paper: TG ZLY HCW.</p>
</fn>
<corresp id="cor001">* E-mail: <email>fungi@mail.kib.ac.cn</email>
(ZLY); <email>higherfungi2005@aliyun.com</email>
(HCW)</corresp>
</author-notes>
<pub-date pub-type="epub"><day>3</day>
<month>5</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>11</volume>
<issue>5</issue>
<elocation-id>e0154794</elocation-id>
<history><date date-type="received"><day>13</day>
<month>10</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>19</day>
<month>4</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 Guo et al</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Guo et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="pone.0154794.pdf"></self-uri>
<abstract><p>Fungal species of <italic>Armillaria</italic>
, which can act as plant pathogens and/or symbionts of the Chinese traditional medicinal herb <italic>Gastrodia elata</italic>
(“Tianma”), are ecologically and economically important and have consequently attracted the attention of mycologists. However, their taxonomy has been highly dependent on morphological characterization and mating tests. In this study, we phylogenetically analyzed Chinese <italic>Armillaria</italic>
samples using the sequences of the internal transcribed spacer region, translation elongation factor-1 alpha gene and beta-tubulin gene. Our data revealed at least 15 phylogenetic lineages of <italic>Armillaria</italic>
from China, of which seven were newly discovered and two were recorded from China for the first time. Fourteen Chinese biological species of <italic>Armillaria</italic>
, which were previously defined based on mating tests, could be assigned to the 15 phylogenetic lineages identified herein. Seven of the 15 phylogenetic lineages were found to be disjunctively distributed in different continents of the Northern Hemisphere, while eight were revealed to be endemic to certain continents. In addition, we found that seven phylogenetic lineages of <italic>Armillaria</italic>
were used for the cultivation of Tianma, only two of which had been recorded to be associated with Tianma previously. We also illustrated that <italic>G</italic>
. <italic>elata</italic>
f. <italic>glauca</italic>
(“Brown Tianma”) and <italic>G</italic>
. <italic>elata</italic>
f. <italic>elata</italic>
(“Red Tianma”), two cultivars of Tianma grown in different regions of China, form symbiotic relationships with different phylogenetic lineages of <italic>Armillaria</italic>
. These findings should aid the development of Tianma cultivation in China.</p>
</abstract>
<funding-group><funding-statement>This study was financed by the National Natural Science Foundation of China (Nos. 30800006 and 31170024), the Chongqing Natural Science Foundation (No. CSTC, 2009BA5030), and the Key Laboratory for Plant Diversity and Biogeography of East Asia, KIB, Chinese Academy of Sciences (KLBB 201207). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><fig-count count="4"></fig-count>
<table-count count="2"></table-count>
<page-count count="21"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files. DNA accession numbers have been detailed in <xref ref-type="table" rid="pone.0154794.t001">Table 1</xref>
of the manuscript.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files. DNA accession numbers have been detailed in <xref ref-type="table" rid="pone.0154794.t001">Table 1</xref>
of the manuscript.</p>
</notes>
</front>
</pmc>
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