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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Molecular and morphological analyses confirm <italic>Rhizopogon verii</italic> as a widely distributed ectomycorrhizal false truffle in Europe, and its presence in South America</title><author><name sortKey="Sulzbacher, Marcelo A" sort="Sulzbacher, Marcelo A" uniqKey="Sulzbacher M" first="Marcelo A." last="Sulzbacher">Marcelo A. Sulzbacher</name><affiliation><nlm:aff id="Aff1">Departamento de Micologia/CCB, Universidade Federal de Pernambuco, Av. Prof. Nelson Chaves, s/n, CEP: 50670-901 Recife, Pernambuco Brazil</nlm:aff></affiliation></author><author><name sortKey="Grebenc, Tine" sort="Grebenc, Tine" uniqKey="Grebenc T" first="Tine" last="Grebenc">Tine Grebenc</name><affiliation><nlm:aff id="Aff2">Slovenian Forestry Institute Večna pot 2, SI-1000 Ljubljana, Slovenia</nlm:aff></affiliation></author><author><name sortKey="Garcia, Miguel" sort="Garcia, Miguel" uniqKey="Garcia M" first="Miguel" last="García">Miguel García</name><affiliation><nlm:aff id="Aff3">Department of Biology, University of Toronto, 3359 Mississagua Road, Mississagua, ON L5L 1C6 Canada</nlm:aff></affiliation></author><author><name sortKey="Silva, Bianca D" sort="Silva, Bianca D" uniqKey="Silva B" first="Bianca D." last="Silva">Bianca D. Silva</name><affiliation><nlm:aff id="Aff4">Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Silveira, Andressa" sort="Silveira, Andressa" uniqKey="Silveira A" first="Andressa" last="Silveira">Andressa Silveira</name><affiliation><nlm:aff id="Aff5">Departamento de Solos, Universidade Federal de Santa Maria, CCR, Campus Universitário, 971050-900 Santa Maria, Rio Grande do Sul Brazil</nlm:aff></affiliation></author><author><name sortKey="Antoniolli, Zaida I" sort="Antoniolli, Zaida I" uniqKey="Antoniolli Z" first="Zaida I." last="Antoniolli">Zaida I. Antoniolli</name><affiliation><nlm:aff id="Aff5">Departamento de Solos, Universidade Federal de Santa Maria, CCR, Campus Universitário, 971050-900 Santa Maria, Rio Grande do Sul Brazil</nlm:aff></affiliation></author><author><name sortKey="Marinho, Paulo" sort="Marinho, Paulo" uniqKey="Marinho P" first="Paulo" last="Marinho">Paulo Marinho</name><affiliation><nlm:aff id="Aff6">Departamento de Biologia Celular e Genética, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Munzenberger, Babette" sort="Munzenberger, Babette" uniqKey="Munzenberger B" first="Babette" last="Münzenberger">Babette Münzenberger</name><affiliation><nlm:aff id="Aff7">Institute for Landscape Biogeochemistry, Leibniz Centre for Agricultural Landscape Research (ZALF), Eberswalder Straße 84, 15374 Müncheberg, Germany</nlm:aff></affiliation></author><author><name sortKey="Telleria, M Teresa" sort="Telleria, M Teresa" uniqKey="Telleria M" first="M. Teresa" last="Telleria">M. Teresa Telleria</name><affiliation><nlm:aff id="Aff8">Departamento de Micología, Real Jardín Botánico, RJB-CSIC, Plaza Murillo 2, Madrid, 28014 Spain</nlm:aff></affiliation></author><author><name sortKey="Baseia, Iuri G" sort="Baseia, Iuri G" uniqKey="Baseia I" first="Iuri G." last="Baseia">Iuri G. Baseia</name><affiliation><nlm:aff id="Aff4">Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Martin, Maria P" sort="Martin, Maria P" uniqKey="Martin M" first="María P." last="Martín">María P. Martín</name><affiliation><nlm:aff id="Aff8">Departamento de Micología, Real Jardín Botánico, RJB-CSIC, Plaza Murillo 2, Madrid, 28014 Spain</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26763005</idno><idno type="pmc">4909799</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4909799</idno><idno type="RBID">PMC:4909799</idno><idno type="doi">10.1007/s00572-015-0678-8</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000076</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000076</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Molecular and morphological analyses confirm <italic>Rhizopogon verii</italic> as a widely distributed ectomycorrhizal false truffle in Europe, and its presence in South America</title><author><name sortKey="Sulzbacher, Marcelo A" sort="Sulzbacher, Marcelo A" uniqKey="Sulzbacher M" first="Marcelo A." last="Sulzbacher">Marcelo A. Sulzbacher</name><affiliation><nlm:aff id="Aff1">Departamento de Micologia/CCB, Universidade Federal de Pernambuco, Av. Prof. Nelson Chaves, s/n, CEP: 50670-901 Recife, Pernambuco Brazil</nlm:aff></affiliation></author><author><name sortKey="Grebenc, Tine" sort="Grebenc, Tine" uniqKey="Grebenc T" first="Tine" last="Grebenc">Tine Grebenc</name><affiliation><nlm:aff id="Aff2">Slovenian Forestry Institute Večna pot 2, SI-1000 Ljubljana, Slovenia</nlm:aff></affiliation></author><author><name sortKey="Garcia, Miguel" sort="Garcia, Miguel" uniqKey="Garcia M" first="Miguel" last="García">Miguel García</name><affiliation><nlm:aff id="Aff3">Department of Biology, University of Toronto, 3359 Mississagua Road, Mississagua, ON L5L 1C6 Canada</nlm:aff></affiliation></author><author><name sortKey="Silva, Bianca D" sort="Silva, Bianca D" uniqKey="Silva B" first="Bianca D." last="Silva">Bianca D. Silva</name><affiliation><nlm:aff id="Aff4">Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Silveira, Andressa" sort="Silveira, Andressa" uniqKey="Silveira A" first="Andressa" last="Silveira">Andressa Silveira</name><affiliation><nlm:aff id="Aff5">Departamento de Solos, Universidade Federal de Santa Maria, CCR, Campus Universitário, 971050-900 Santa Maria, Rio Grande do Sul Brazil</nlm:aff></affiliation></author><author><name sortKey="Antoniolli, Zaida I" sort="Antoniolli, Zaida I" uniqKey="Antoniolli Z" first="Zaida I." last="Antoniolli">Zaida I. Antoniolli</name><affiliation><nlm:aff id="Aff5">Departamento de Solos, Universidade Federal de Santa Maria, CCR, Campus Universitário, 971050-900 Santa Maria, Rio Grande do Sul Brazil</nlm:aff></affiliation></author><author><name sortKey="Marinho, Paulo" sort="Marinho, Paulo" uniqKey="Marinho P" first="Paulo" last="Marinho">Paulo Marinho</name><affiliation><nlm:aff id="Aff6">Departamento de Biologia Celular e Genética, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Munzenberger, Babette" sort="Munzenberger, Babette" uniqKey="Munzenberger B" first="Babette" last="Münzenberger">Babette Münzenberger</name><affiliation><nlm:aff id="Aff7">Institute for Landscape Biogeochemistry, Leibniz Centre for Agricultural Landscape Research (ZALF), Eberswalder Straße 84, 15374 Müncheberg, Germany</nlm:aff></affiliation></author><author><name sortKey="Telleria, M Teresa" sort="Telleria, M Teresa" uniqKey="Telleria M" first="M. Teresa" last="Telleria">M. Teresa Telleria</name><affiliation><nlm:aff id="Aff8">Departamento de Micología, Real Jardín Botánico, RJB-CSIC, Plaza Murillo 2, Madrid, 28014 Spain</nlm:aff></affiliation></author><author><name sortKey="Baseia, Iuri G" sort="Baseia, Iuri G" uniqKey="Baseia I" first="Iuri G." last="Baseia">Iuri G. Baseia</name><affiliation><nlm:aff id="Aff4">Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</nlm:aff></affiliation></author><author><name sortKey="Martin, Maria P" sort="Martin, Maria P" uniqKey="Martin M" first="María P." last="Martín">María P. Martín</name><affiliation><nlm:aff id="Aff8">Departamento de Micología, Real Jardín Botánico, RJB-CSIC, Plaza Murillo 2, Madrid, 28014 Spain</nlm:aff></affiliation></author></analytic><series><title level="j">Mycorrhiza</title><idno type="ISSN">0940-6360</idno><idno type="eISSN">1432-1890</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The genus <italic>Rhizopogon</italic> includes species with hypogeous or subepigeus habit, forming ectomycorrhizae with naturally occurring or planted pines (Pinaceae). Species of the genus <italic>Rhizopogon</italic> can be distinguished easily from the other hypogeous basidiomycetes by their lacunose gleba without columella and their smooth elliptical spores; however, the limit between species is not always easy to establish. <italic>Rhizopogon luteolus</italic>, the type species of the genus, has been considered one of the species that are more abundant in Europe, as well as it has been cited in pine plantation of North and South America, different parts of Africa, Australia, and New Zealand. However, in this study, based on molecular analyses of the ITS nuclear ribosomal DNA (nrDNA) sequences (19 new sequences; 37 sequences from GenBank/UNITE, including those from type specimens), we prove that many GenBank sequences under <italic>R. luteolus</italic> were misidentified and correspond to <italic>Rhizopogon verii</italic>, a species described from Tunisia. Also, we confirm that basidiomes and ectomycorrhizae recently collected in Germany under <italic>Pinus sylvestris</italic>, as well as specimens from South of Brazil under <italic>Pinus taeda</italic> belong to <italic>R. verii</italic>. Thanks to the numerous ectomycorrhizal tips collected in Germany, a complete description of <italic>R. verii</italic>/<italic>P. sylvestris</italic> ectomycorrhiza is provided. Moreover, since in this paper the presence of <italic>R. verii</italic> in South America is here reported for the first time, a short description of basidiomes collected in Brazil, compared with collections located in different European herbaria, is included.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Agerer, R" uniqKey="Agerer R">R Agerer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Agerer, R" uniqKey="Agerer R">R Agerer</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Baseia, Ig" uniqKey="Baseia I">IG Baseia</name></author><author><name sortKey="Milanez, Ai" uniqKey="Milanez A">AI Milanez</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Beiler, Kj" uniqKey="Beiler K">KJ Beiler</name></author><author><name sortKey="Durall, Dm" uniqKey="Durall D">DM Durall</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Mycorrhiza</journal-id><journal-id journal-id-type="iso-abbrev">Mycorrhiza</journal-id><journal-title-group><journal-title>Mycorrhiza</journal-title></journal-title-group><issn pub-type="ppub">0940-6360</issn><issn pub-type="epub">1432-1890</issn><publisher><publisher-name>Springer Berlin Heidelberg</publisher-name><publisher-loc>Berlin/Heidelberg</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26763005</article-id><article-id pub-id-type="pmc">4909799</article-id><article-id pub-id-type="publisher-id">678</article-id><article-id pub-id-type="doi">10.1007/s00572-015-0678-8</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject></subj-group></article-categories><title-group><article-title>Molecular and morphological analyses confirm <italic>Rhizopogon verii</italic> as a widely distributed ectomycorrhizal false truffle in Europe, and its presence in South America</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Sulzbacher</surname><given-names>Marcelo A.</given-names></name><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Grebenc</surname><given-names>Tine</given-names></name><xref ref-type="aff" rid="Aff2"></xref></contrib><contrib contrib-type="author"><name><surname>García</surname><given-names>Miguel Á.</given-names></name><xref ref-type="aff" rid="Aff3"></xref></contrib><contrib contrib-type="author"><name><surname>Silva</surname><given-names>Bianca D.</given-names></name><xref ref-type="aff" rid="Aff4"></xref></contrib><contrib contrib-type="author"><name><surname>Silveira</surname><given-names>Andressa</given-names></name><xref ref-type="aff" rid="Aff5"></xref></contrib><contrib contrib-type="author"><name><surname>Antoniolli</surname><given-names>Zaida I.</given-names></name><xref ref-type="aff" rid="Aff5"></xref></contrib><contrib contrib-type="author"><name><surname>Marinho</surname><given-names>Paulo</given-names></name><xref ref-type="aff" rid="Aff6"></xref></contrib><contrib contrib-type="author"><name><surname>Münzenberger</surname><given-names>Babette</given-names></name><xref ref-type="aff" rid="Aff7"></xref></contrib><contrib contrib-type="author"><name><surname>Telleria</surname><given-names>M. Teresa</given-names></name><xref ref-type="aff" rid="Aff8"></xref></contrib><contrib contrib-type="author"><name><surname>Baseia</surname><given-names>Iuri G.</given-names></name><xref ref-type="aff" rid="Aff4"></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Martín</surname><given-names>María P.</given-names></name><address><phone>+34 91 420 30 17</phone><email>maripaz@rjb.csic.es</email></address><xref ref-type="aff" rid="Aff8"></xref></contrib><aff id="Aff1"><label></label>Departamento de Micologia/CCB, Universidade Federal de Pernambuco, Av. Prof. Nelson Chaves, s/n, CEP: 50670-901 Recife, Pernambuco Brazil</aff><aff id="Aff2"><label></label>Slovenian Forestry Institute Večna pot 2, SI-1000 Ljubljana, Slovenia</aff><aff id="Aff3"><label></label>Department of Biology, University of Toronto, 3359 Mississagua Road, Mississagua, ON L5L 1C6 Canada</aff><aff id="Aff4"><label></label>Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</aff><aff id="Aff5"><label></label>Departamento de Solos, Universidade Federal de Santa Maria, CCR, Campus Universitário, 971050-900 Santa Maria, Rio Grande do Sul Brazil</aff><aff id="Aff6"><label></label>Departamento de Biologia Celular e Genética, Universidade Federal do Rio Grande do Norte, Campus Universitário, Lagoa Nova, CEP: 59072-970 Natal, Rio Grande do Norte Brazil</aff><aff id="Aff7"><label></label>Institute for Landscape Biogeochemistry, Leibniz Centre for Agricultural Landscape Research (ZALF), Eberswalder Straße 84, 15374 Müncheberg, Germany</aff><aff id="Aff8"><label></label>Departamento de Micología, Real Jardín Botánico, RJB-CSIC, Plaza Murillo 2, Madrid, 28014 Spain</aff></contrib-group><pub-date pub-type="epub"><day>14</day><month>1</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>14</day><month>1</month><year>2016</year></pub-date><pub-date pub-type="ppub"><year>2016</year></pub-date><volume>26</volume><fpage>377</fpage><lpage>388</lpage><history><date date-type="received"><day>2</day><month>10</month><year>2015</year></date><date date-type="accepted"><day>28</day><month>12</month><year>2015</year></date></history><permissions><copyright-statement>© The Author(s) 2016</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.</license-p></license></permissions><abstract id="Abs1"><p>The genus <italic>Rhizopogon</italic> includes species with hypogeous or subepigeus habit, forming ectomycorrhizae with naturally occurring or planted pines (Pinaceae). Species of the genus <italic>Rhizopogon</italic> can be distinguished easily from the other hypogeous basidiomycetes by their lacunose gleba without columella and their smooth elliptical spores; however, the limit between species is not always easy to establish. <italic>Rhizopogon luteolus</italic>, the type species of the genus, has been considered one of the species that are more abundant in Europe, as well as it has been cited in pine plantation of North and South America, different parts of Africa, Australia, and New Zealand. However, in this study, based on molecular analyses of the ITS nuclear ribosomal DNA (nrDNA) sequences (19 new sequences; 37 sequences from GenBank/UNITE, including those from type specimens), we prove that many GenBank sequences under <italic>R. luteolus</italic> were misidentified and correspond to <italic>Rhizopogon verii</italic>, a species described from Tunisia. Also, we confirm that basidiomes and ectomycorrhizae recently collected in Germany under <italic>Pinus sylvestris</italic>, as well as specimens from South of Brazil under <italic>Pinus taeda</italic> belong to <italic>R. verii</italic>. Thanks to the numerous ectomycorrhizal tips collected in Germany, a complete description of <italic>R. verii</italic>/<italic>P. sylvestris</italic> ectomycorrhiza is provided. Moreover, since in this paper the presence of <italic>R. verii</italic> in South America is here reported for the first time, a short description of basidiomes collected in Brazil, compared with collections located in different European herbaria, is included.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Boletales</kwd><kwd>Ectomycorrhiza</kwd><kwd>Hypogeous fungi</kwd><kwd>Internal transcribed spacer</kwd><kwd>nrDNA</kwd><kwd><italic>Pinus sylvestris</italic></kwd><kwd><italic>Pinus taeda</italic></kwd><kwd>Phylogeny</kwd></kwd-group><funding-group><award-group><funding-source><institution>Coordination for the Improvement of Higher Education Personnel (CAPES – Brazil, scholarships granted to the senior author). </institution></funding-source></award-group><award-group><funding-source><institution>CNPq project PVE 407474/2013-7.</institution></funding-source></award-group><award-group><funding-source><institution>Brazil – Slovenia bilateral project </institution></funding-source><award-id>BI-BR/11-13-005(SRA) / 490648/2010-0 (CNPq)</award-id><principal-award-recipient><name><surname>Grebenc</surname><given-names>Tine</given-names></name></principal-award-recipient></award-group><award-group><funding-source><institution>Research Program in Forest Biology, Ecology and Technology </institution></funding-source><award-id>P4-0107</award-id><principal-award-recipient><name><surname>Grebenc</surname><given-names>Tine</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© Springer-Verlag Berlin Heidelberg 2016</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><p>The species of the genus <italic>Rhizopogon</italic> Fr. belong to the order Boletales and suborder Suillineae in the Agaricomycetidae (Binder and Hibbett <xref ref-type="bibr" rid="CR6">2006</xref>). The genus is represented with over 100 species distributed worldwide (Smith and Zeller <xref ref-type="bibr" rid="CR70">1966</xref>; Martín <xref ref-type="bibr" rid="CR39">1996</xref>; Martín and García <xref ref-type="bibr" rid="CR43">2009</xref>). All species produce hypogeous or semi-hypogeous basidiomes and form ectomycorrhizae (EcM) with members of the Pinaceae (<italic>Pinus</italic>, <italic>Pseudotsuga</italic>, and <italic>Tsuga</italic>). <italic>Rhizopogon</italic> species are easy to cultivate in pure culture (Molina and Trappe <xref ref-type="bibr" rid="CR49">1994</xref>; Brundrett et al. <xref ref-type="bibr" rid="CR8">1996</xref>); thus, some were frequently applied to study physiology, morphology, or ecology of its ectomycorrhizae in the agroforestry systems (Smith and Zeller <xref ref-type="bibr" rid="CR70">1966</xref>; Hung and Trappe <xref ref-type="bibr" rid="CR33">1983</xref>; Chu-Chou and Grace <xref ref-type="bibr" rid="CR13">1984</xref>; Miller <xref ref-type="bibr" rid="CR45">1986</xref>; Molina et al. <xref ref-type="bibr" rid="CR50">1997</xref>; Beiler et al. <xref ref-type="bibr" rid="CR5">2010</xref>).</p><p>Zeller and Dodge (<xref ref-type="bibr" rid="CR86">1918</xref>) were the first authors to present a worldwide monograph of <italic>Rhizopogon</italic>. Later, Smith and Zeller (<xref ref-type="bibr" rid="CR70">1966</xref>) produced the first modern account of the genus to North America including a total of 137 taxa, in which 128 were new for science. Since this paper, the Pacific Northwestern USA has been considered the greatest area of diversity of the genus (Hosford <xref ref-type="bibr" rid="CR30">1975</xref>; Molina et al. <xref ref-type="bibr" rid="CR50">1997</xref>; Grubisha et al. <xref ref-type="bibr" rid="CR24">2002</xref>), as well as other parts of the USA (Harrison and Smith <xref ref-type="bibr" rid="CR26">1968</xref>; Miller <xref ref-type="bibr" rid="CR45">1986</xref>). However, in posterior systematic studies undertaken in several part of the world, authors described new species in Mexico (Trappe and Guzmán <xref ref-type="bibr" rid="CR79">1971</xref>, Cázares et al. <xref ref-type="bibr" rid="CR12">1992</xref>), Tunisia (Pacioni <xref ref-type="bibr" rid="CR58">1984a</xref>), China (Liu <xref ref-type="bibr" rid="CR38">1985</xref>), Japan (Mujic et al. <xref ref-type="bibr" rid="CR52">2014</xref>), and different countries of Europe (Pacioni <xref ref-type="bibr" rid="CR59">1984b</xref>, Martín <xref ref-type="bibr" rid="CR39">1996</xref>, Martín and Calonge <xref ref-type="bibr" rid="CR41">2001</xref>); as well as new records, such as those of Mexico and Caribean countries (Hosford and Trappe <xref ref-type="bibr" rid="CR31">1980</xref>), Italy (Montecchi and Sarasini <xref ref-type="bibr" rid="CR51">2000</xref>), Japan (Hosford and Trappe <xref ref-type="bibr" rid="CR32">1988</xref>) and Spain (Martín and Calonge <xref ref-type="bibr" rid="CR42">2006</xref>), showing that the knowledge of the genus is not yet complete.</p><p>Nowadays, systematics and taxonomy of <italic>Rhizopogon</italic> have been under profound changes, mainly due to the use of molecular tools, specially using sequence-based analyses of the nuclear rDNA regions (nuc-ssu, nuc-lsu, ITS) and also mitochondrial genes (<italic>atp</italic>6, mt-lsu) (Grubisha <xref ref-type="bibr" rid="CR23">1998</xref>; Martín et al. <xref ref-type="bibr" rid="CR40">1998</xref>; Grubisha et al. <xref ref-type="bibr" rid="CR24">2002</xref>; Kretzer et al. <xref ref-type="bibr" rid="CR36">2003</xref>; Grubisha et al. <xref ref-type="bibr" rid="CR25">2005</xref>; Binder and Hibbett <xref ref-type="bibr" rid="CR6">2006</xref>; Martín and García <xref ref-type="bibr" rid="CR43">2009</xref>). According to Grubisha et al. (<xref ref-type="bibr" rid="CR24">2002</xref>), the species are distributed in five subgenera: <italic>Amylopogon</italic>, <italic>Rhizopogon</italic>, <italic>Roseoli</italic>, <italic>Versicolores</italic>, and <italic>Villosuli</italic>. The species of the subgenus <italic>Rhizopogon</italic> have shown a combination of features, such as a simple peridium completely covered by rhizomorphs. <italic>Rhizopogon luteolus</italic> is the type species of the subgenus and it has been considered widely distributed in the Northern hemisphere.</p><p><italic>Rhizopogon verii</italic> Pacioni (Pacioni <xref ref-type="bibr" rid="CR58">1984a</xref>) was described from Tunisia under <italic>Pinus pinaster</italic>. However, studies related to the systematic and distributions of <italic>R. verii</italic> are limited to only few collections from Italy, Spain, and Tunisia (Martín <xref ref-type="bibr" rid="CR39">1996</xref>). From other continents, <italic>R. verii</italic> has not been cited yet. Recent collections on an abandoned coal mine area near Crinitz (Brandenburg, Germany) on <italic>Pinus sylvestris</italic> could fit with <italic>R. verii</italic>, as well as the specimens collected during a survey of hypogeous fungi in State of Rio Grande do Sul (Brazil) growing under <italic>Pinus taeda</italic>.</p><p>Thus, with the opportunity to study new fresh specimens, the main objective of this paper was to clearly identify the specimens from Germany and Brazil using molecular analyses of ITS nrDNA sequences. This has allowed us also to confirm the presence of <italic>R. verii</italic> in these countries, as well as the EcM of <italic>R. verii</italic> on <italic>P. sylvestris</italic>. A detailed description is provided, both to the basidiomes and the EcM formed by <italic>R. verii</italic>/<italic>P. sylvestris</italic>. Moreover, information to <italic>R. verii</italic> worldwide distribution in different native and pine plantation areas is provided.</p></sec><sec id="Sec2" sec-type="materials|methods"><title>Materials and methods</title><p>Specimens from Brazil were collected during mycological trips in the State of Rio Grande do Sul, close to the “Estação Ecológica do TAIM” in a sandy dune near to mature trees of <italic>P. taeda</italic>. In Germany, fresh basidiomes and soil cores to collect ectomycorrhizal tips were taken from the abandoned coal mine area along the side road toward Schlabendorfer See near the village Crinitz; the area is represented by a ca. 30-year-old <italic>P. sylvestris</italic> plantation established on silicate sandy neosol with shallow organic layer and poor understory vegetation. Data of new specimens and ectomycorrhiza collected for this paper are included in Table <xref rid="Tab1" ref-type="table">1</xref>.<table-wrap id="Tab1"><label>Table 1</label><caption><p>Samples of <italic>Rhizopogon verii</italic> included in morphological and molecular analyses</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Herbarium number or EcM code</th><th>Origin</th><th>Coordinates</th><th>Collection date</th><th>Host</th><th>Isolation source</th><th>Accession number</th></tr></thead><tbody><tr><td rowspan="2">UFRN-fungos 2371</td><td rowspan="2">BR: Rio Grande do Sul, TAIM area</td><td>52° 31′ 43.4″ N</td><td rowspan="2">5 Jan 2012</td><td rowspan="2"><italic>Pinus taeda</italic></td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>32° 32′ 05″ E</td></tr><tr><td rowspan="2">UFRN-fungos 2372 (duplo URM 88223)</td><td rowspan="2">BR: Rio Grande do Sul, TAIM area</td><td>52° 31′ 4.4″ N</td><td rowspan="2">9 Jan 2013</td><td rowspan="2"><italic>Pinus taeda</italic></td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875275</td></tr><tr><td>32° 32′ 05″ E</td></tr><tr><td rowspan="2">LJF 4035</td><td rowspan="2">DE: Casel, Kozen</td><td>51° 67′ 88.27″ N</td><td rowspan="2">26 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875272</td></tr><tr><td>14° 15′ 65.71″ E</td></tr><tr><td rowspan="2">LJF 4003, LJF 4015, LJF 4022, LJF 4038, LJF 4039</td><td rowspan="2">DE: Crinitz, village of Bergen</td><td>51° 46′ 5.30″ N</td><td rowspan="2">19 Oct 2013</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation and natural regeneration</td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875267 (LJF 4022)</td></tr><tr><td>13° 44′ 46.22″ E</td></tr><tr><td rowspan="2">LJF 4031</td><td rowspan="2">DE: Crinitz, NW from the village of Bergen</td><td>51° 76′ 68.35″ N</td><td rowspan="2">22 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> young plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>13° 74′ 46.97″ E</td></tr><tr><td rowspan="2">LJF 4029</td><td rowspan="2">DE: Crinitz, NW from the village of Bergen</td><td>51° 76′ 71.30″ N</td><td rowspan="2">22 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> young plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875271</td></tr><tr><td>13° 74′ 49.02″ E</td></tr><tr><td rowspan="2">LJF 4027</td><td rowspan="2">DE: Crinitz, NW from the village of Bergen</td><td>51° 76′ 66.19″ N</td><td rowspan="2">22 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> young plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>13° 74′ 45.91″ E</td></tr><tr><td rowspan="2">LJF 4030, LJF 4058</td><td rowspan="2">DE: Gorden-Staupitz, Senftenberg strasse</td><td>51° 52′ 84.04″ N</td><td rowspan="2">24 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875273, LN875274</td></tr><tr><td>13° 65′ 54.99″ E</td></tr><tr><td rowspan="2">LJF4019, LJF 4036</td><td rowspan="2">DE: Göritz, Drebkau</td><td>51° 66′ 40.91″ N</td><td rowspan="2">26 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation and <italic>Alnus glutinosa</italic></td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>14° 10′ 77.43″ E</td></tr><tr><td rowspan="2">LJF 4016, LJF 4055 (A), LJF 4055 (B), LJF 4055 (C)</td><td rowspan="2">DE: Hennersdorf</td><td>51° 38′ 7.43″ N</td><td rowspan="2">21 Oct 2013</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation with individual <italic>Betula pendula</italic>, <italic>Robinia pseudoacacia</italic>, <italic>Quercus robur</italic>, and <italic>Q. rubra</italic></td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875268, LN875264, LN875265, LN875266</td></tr><tr><td>13° 37′ 31.10″ E</td></tr><tr><td rowspan="2">LJF 4025, LJF 4032, LJF 4037, LJF 4041</td><td rowspan="2">DE: Hennersdorf</td><td>51° 63′ 54.69″ N</td><td rowspan="2">23 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> plantation with <italic>Robinia pseudoacacia</italic></td><td rowspan="2">Basidiomes</td><td rowspan="2">LN875269 (LJF 4025), LN875270 (LJF 4032)</td></tr><tr><td>13° 62′ 43.10″ E</td></tr><tr><td>LJU-SFI-PSyl-2-2-1, LJU-SFI-PSyl-2-2-2, LJU-SFI-PSyl-2-2-3, LJU-SFI-PSyl-2-3-1, LJU-SFI-PSyl-2-3-3</td><td>DE: Hennersdorf</td><td>n.d.</td><td>n.d.</td><td><italic>Pinus sylvestris</italic> plantation</td><td>Root tips</td><td>LN875259, LN875260, LN875261, LN875262, LN875263</td></tr><tr><td rowspan="2">LJF 4014</td><td rowspan="2">DE: Leippe</td><td>51° 25′ 24.36″ N</td><td rowspan="2">24 Oct 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> young plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>14° 2′ 52.61″ E</td></tr><tr><td rowspan="2">LJF 4026, LJF 4042</td><td rowspan="2">DE: Lugkteich (lake), Lower Lusatian Ridge Nature Park</td><td>51° 72′ 38.07″ N</td><td rowspan="2">27 Sep 2014</td><td rowspan="2"><italic>Pinus sylvestris</italic> young plantation</td><td rowspan="2">Basidiomes</td><td rowspan="2">n.d.</td></tr><tr><td>13° 58′ 85.12″ E</td></tr></tbody></table><table-wrap-foot><p><italic>BR</italic> Brazil, <italic>DE</italic> Germany, <italic>n.d</italic>. no data</p></table-wrap-foot></table-wrap></p><sec id="Sec3"><title>Morphological analyses</title><p>Fresh basidiomata were collected and analyzed macro- and microscopically following previously described methods (Miller and Miller <xref ref-type="bibr" rid="CR46">1988</xref>; Martín <xref ref-type="bibr" rid="CR39">1996</xref>), and compared with <italic>R. verii</italic> collections located at AQUI herbarium, including the type, as well as collections in BCN herbarium. Color codes followed Munsell Soil Color Charts (<xref ref-type="bibr" rid="CR53">2009</xref>). Presentation of basidiospore data follows the methodology proposed by Tulloss et al. (<xref ref-type="bibr" rid="CR80">1992</xref>), slightly modified by Wartchow (<xref ref-type="bibr" rid="CR83">2012</xref>) and Wartchow et al. (<xref ref-type="bibr" rid="CR84">2012</xref>). Abbreviations include <italic>L</italic>(<italic>W</italic>) = average basidiospore length (width), <italic>Q</italic> = the length to width ratio range as determined from all measured basidiospores, and <italic>Q</italic><sub>m</sub> = the <italic>Q</italic> value averaged from all basidiospores measured. Herbarium abbreviations follow those of the online version of Thiers [continuously updated]. Specimens are deposited in UFRN, URM and LJF herbaria.</p><p>Soil was gently washed from ectomycorrhizae (EcM) under binocular using forceps and brush, and subsequently EcM were stored in 2 % glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.2) at room temperature. For semi-thin sections of mycorrhizae, six washes (10 min each) in 0.1 M sodium cacodylate buffer were performed. Samples were postfixed in 1 % osmium tetroxide in the same buffer for 1 h in the dark under room temperature. After six washes with distilled water, samples were dehydrated in acetone (25, 50, 70, and 95 %, for 15 min each) and three times in 100 % acetone for 1 h. The mycorrhizal tips were embedded in Spurr’s plastic (Spurr <xref ref-type="bibr" rid="CR74">1969</xref>) and sectioned with a diamond knife on an Ultracut Reichert Ultramicrotome (W. Reichert-LABTAC, Wolfratshausen, Germany). The sections (0.5 μm thin) were stained with crystal violet. Twenty mycorrhizal tips were investigated by the use of a light microscope (Axioscop 50, Zeiss, Oberkochen, Germany).</p><p>Macroscopic, anatomorphic, and biochemical characteristics were assessed as described in Agerer (<xref ref-type="bibr" rid="CR1">1991</xref>), following also the computer character checklist from Agerer (<xref ref-type="bibr" rid="CR3">1987–2012</xref>). A stereomicroscope (Zeiss SteREO Lumar.V12) with ×6.4–×80 magnification (Zeiss, Jena, Germany) and a microscope (Zeiss AXIO Imager.Z2) equipped for VIS, DIC, dark field, and fluorescent microscopy with magnification ×12.5–×1000 (Zeiss, Jena, Germany) were used to assess characters and make photos.</p></sec><sec id="Sec4"><title>DNA extraction, amplification, and sequencing</title><p>Total genomic DNA was extracted from the gleba of air-dried basidiomes or from stored ectomycorrhizal root tips (5–10 tips from the same cluster per extraction) by using a Plant DNeasy Mini Kit (Qiagen, Hilden, Germany). Extracted DNA was resuspended in pre-warmed, sterile Milli-Q water to the approximate final concentration of 100 ng μl<sup>−1</sup> and kept at −80 °C. Primer pair ITS1F (Gardes & Bruns <xref ref-type="bibr" rid="CR19">1993</xref>) and ITS4 (White et al. <xref ref-type="bibr" rid="CR85">1990</xref>) was used for PCR amplification of the complete nuclear ITS region. Amplification reactions were performed in a PE 9700 DNA thermocycler, with an annealing temperature of 55 °C. Negative controls, lacking fungal DNA, were run for each experiment to check for any contamination. Amplified DNA was separated and analyzed as described in Grebenc et al. (<xref ref-type="bibr" rid="CR22">2009</xref>).</p><p>Amplified DNA fragments were first separated and purified from the agarose gel using the Wizard SV Gel and PCR Clean-Up System (Promega Corporation, Madison, WI, USA) and sent to Macrogen Korea (Seoul, Korea) for sequencing. Sequencher 5.1 (Gene Codes Corporations, Ann Arbor, MI, USA) was used to identify the consensus sequence from the two strands of each isolate.</p></sec><sec id="Sec5"><title>Molecular analyses</title><p>Preliminary identification of the new sequences obtained were done through UNITE database (<ext-link ext-link-type="uri" xlink:href="http://unite.ut.ee/">http://unite.ut.ee</ext-link>) species hypothesis (SH) search (Kõljalg et al. <xref ref-type="bibr" rid="CR35">2013</xref>). The PlutoF multiple sequence alignments obtained in UNITE were merged and manually adjusted using Se-Al v.2.0a11 (Rambaut <xref ref-type="bibr" rid="CR66">2002</xref>). The sequence AF062933 of <italic>Rhizopogon succosus</italic> A.H. Sm. was chosen as outgroup, since it is one of the few sequences available of subgen. <italic>Roseoli</italic> Fr. with voucher collection, excluding the sequences of <italic>R. luteolus</italic> and <italic>R. verii</italic>.</p><p>Analyses were conducted using parsimony and Bayesian inference. In the parsimony analyses, nucleotide characters were treated as unordered and all changes were equally weighted; gaps were treated as missing data. Searches for most parsimonious (MP) trees were performed using a two-stage strategy with PAUP* v.4.0b10 (Swofford <xref ref-type="bibr" rid="CR71">2002</xref>). First, the analyses involved 10,000 replicates with stepwise random taxon addition, tree bisection-reconnection (TBR) branch swapping saving no more than 10 trees per replicate, and MULTREES option off. The second round of analyses was performed on all trees in memory with the same settings except the MULTREES option on. Both stages were conducted to completion or until one million trees were found. Relative support for clades was inferred by nonparametric bootstrapping (Felsenstein <xref ref-type="bibr" rid="CR17">1985</xref>) as implemented in PAUP* using 500 pseudoreplicates, each with 20 random sequence addition cycles, TBR branch swapping, and MULTREES option off (DeBry and Olmstead <xref ref-type="bibr" rid="CR16">2000</xref>). To the Bayesian analyses, the program MrModeltest v.2.3 (Nylander <xref ref-type="bibr" rid="CR55">2004</xref>) was used to determine the model of sequence evolution that fits best the dataset. The Hasegawa-Kishino-Yano (Hasegawa et al. <xref ref-type="bibr" rid="CR27">1985</xref>) of DNA substitution, with rate variation among nucleotides following a discrete gamma distribution (HKY + G), was selected as the best-fit by both the hierarchical likelihood ratio test (hLRT) and Akaike information criterion (AIC). Bayesian phylogenetic inferences were performed using MrBayes v.3.2.2 (Ronquist et al. <xref ref-type="bibr" rid="CR69">2012</xref>) run on the CIPRES Science Gateway (Miller et al. <xref ref-type="bibr" rid="CR47">2010</xref>). Two runs starting from random trees were carried out using the HKY + G substitution model. All model parameters were treated as unknown variables with uniform prior probabilities and were estimated as part of the analysis together with tree topologies. Metropolis-coupled Markov chain Monte Carlo algorithm was used with eight simultaneous chains for each run, set at two million generations, and sampled every 1000 generations. Of the 40,002 trees obtained, the first 25 % were discarded as burn-in; the 50 % majority-rule consensus tree and the Bayesian posterior probabilities (PP) were obtained in MrBayes from the remaining 30,002 trees.</p></sec></sec><sec id="Sec6"><title>Results</title><sec id="Sec7"><title>Molecular analyses</title><p>The matrix contained the 19 sequences obtained in this study (Table <xref rid="Tab1" ref-type="table">1</xref>) and sequences of the species hypothesis groups SH5_008910 and SH5_008911 obtained through UNITE search (Table <xref rid="Tab2" ref-type="table">2</xref>: SH5_008910, clade A and C; SH5_008911, clade B). After manual adjustment, the matrix had 749 characters, 95 of them variable and 23 parsimony-informative that produced >1,000,000 MP trees, 107 steps in length. There was a consistency index of 0.953 and a retention index of 0.941. The harmonic mean of the estimated marginal likelihoods from the Bayesian analysis was −ln = 1727.88. The MP and Bayesian analyses produced trees of identical topology (Fig. <xref rid="Fig1" ref-type="fig">1</xref>), representing the Bayesian Majority Rule Consensus tree with the PP and Bootstrap values on the branches.<table-wrap id="Tab2"><label>Table 2</label><caption><p>Metadata from NCBI and UNITE sequences included in the molecular analyses</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Clades/Taxon names</th><th>Acc. Number NCBI or UNITE</th><th>Sequence name in databases</th><th>Isolation source</th><th>Origin</th><th>Host</th><th>Publication were the sequences Unpublished</th></tr></thead><tbody><tr><td rowspan="3">Clade A <italic>Rhizopogon</italic> sp.</td><td>AB211261</td><td>Uncultured ECM fungus</td><td>Root tip</td><td>Japan</td><td><italic>Pinus densiflora</italic></td><td>Lian et al (<xref ref-type="bibr" rid="CR37">2006</xref>)</td></tr><tr><td>AB253521</td><td>Uncultured <italic>Rhizopogon</italic></td><td>Root tip</td><td>Japan:Tottori, Tottori sand dune</td><td><italic>Pinus thunbergii</italic></td><td>Taniguchi et al (<xref ref-type="bibr" rid="CR76">2007</xref>)</td></tr><tr><td>AB587765</td><td>Uncultured ECM fungus</td><td>Root tip</td><td>South Korea: Kangwon-do</td><td><italic>Pinus thunbergii</italic></td><td>Obase et al (<xref ref-type="bibr" rid="CR56">2011</xref>)</td></tr><tr><td rowspan="3">Clade B <italic>Rhizopogon luteolus</italic> Fr. & Nordhom</td><td>AF062936, neotype</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>Sweden: Uppsala</td><td><italic>Pinus</italic> sp.</td><td>Grubisha et al (<xref ref-type="bibr" rid="CR24">2002</xref>)</td></tr><tr><td>UDB008728</td><td>ECM <italic>Suillus</italic>-<italic>Rhizopogon</italic> clade</td><td>Root tip</td><td>Estonia: Kuusnõmme</td><td><italic>Pinus sylvestris</italic></td><td>Unpublished</td></tr><tr><td>UDB015830</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>Estonia: Audaku, Saare</td><td>Mixed forest</td><td>Unpublished</td></tr><tr><td rowspan="20">Clade C <italic>Rhizopogon verii</italic> G. Pacioni</td><td>AM085521</td><td><italic>R. verii</italic> (under <italic>R. corsicus</italic> in herbarium label)</td><td>Basidiome</td><td>Belgium: Limburg</td><td>Probably planted pines from Corsica</td><td>Unpublished</td></tr><tr><td>AM085531, Holotype</td><td><italic>R. verii</italic></td><td>Basidiome</td><td>Tunisia: Tabarka</td><td><italic>Pinus pinaster</italic></td><td>Martín and García (<xref ref-type="bibr" rid="CR46">2009</xref>)</td></tr><tr><td>DQ068966</td><td>Uncultured ECM <italic>Rhizopogon</italic></td><td>Root tip</td><td>Lithuania</td><td><italic>Pinus sylvestris</italic></td><td>Menkis et al (<xref ref-type="bibr" rid="CR44">2005</xref>)</td></tr><tr><td>EU379676</td><td><italic>R. luteolus</italic></td><td>Root tip</td><td>Poland</td><td><italic>Pinus sylvestris</italic></td><td>Hilszczanska et al (<xref ref-type="bibr" rid="CR28">2008</xref>)</td></tr><tr><td>EU423919</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>Spain</td><td><italic>Pinus pinea</italic></td><td>Hortal et al (<xref ref-type="bibr" rid="CR29">2008</xref>)</td></tr><tr><td>EU784397</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>UK: Surrey</td><td>–<sup>a</sup></td><td>Brock et al (<xref ref-type="bibr" rid="CR7">2009</xref>)</td></tr><tr><td>EU784398</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>UK: South Hampshire</td><td>–<sup>a</sup></td><td>Brock et al (<xref ref-type="bibr" rid="CR7">2009</xref>)</td></tr><tr><td>FJ013053</td><td>Uncultured ECM (<italic>Rhizopogon</italic>)</td><td>Root tip</td><td>Spain</td><td><italic>Pinus pinaster</italic></td><td>Rincón & Pueyo (<xref ref-type="bibr" rid="CR67">2010</xref>)</td></tr><tr><td>FJ816742, FJ816745</td><td>Uncultured <italic>Rhizopogon</italic></td><td>Root tip</td><td>Spain</td><td><italic>Pinus pinaster</italic></td><td>Pestana & Santolamazza (<xref ref-type="bibr" rid="CR61">2011</xref>)</td></tr><tr><td>FJ876174</td><td><italic>Rhizopogon</italic> sp.</td><td>Root tip</td><td>UK: England, Stoborough Heath National Nature Reserve</td><td><italic>Pinus</italic> sp.</td><td>Collier & Bidartondo (<xref ref-type="bibr" rid="CR14">2009</xref>)</td></tr><tr><td>FN679020</td><td>Uncultured <italic>Rhizopogon</italic></td><td>Root tip</td><td>Czech Republic: Bohemian Switzerland National Park</td><td><italic>Pinus sylvestris</italic></td><td>Kohout et al (<xref ref-type="bibr" rid="CR34">2011</xref>)</td></tr><tr><td>FN679021</td><td>Uncultured <italic>Rhizopogon</italic></td><td>Root tip</td><td>Czech Republic: Bohemian Switzerland National Park</td><td><italic>Pinus strobus</italic></td><td>Kohout et al (<xref ref-type="bibr" rid="CR34">2011</xref>)</td></tr><tr><td>GQ205357</td><td>Uncultured fungus</td><td>Root tip</td><td>Portugal</td><td><italic>Pinus pinaster</italic></td><td>Buscardo et al (<xref ref-type="bibr" rid="CR9">2010</xref>)</td></tr><tr><td>GQ267481</td><td><italic>R. luteolus</italic></td><td>Basidiome</td><td>New Zealand</td><td><italic>Pinus radiata</italic></td><td>Walbert et al (<xref ref-type="bibr" rid="CR82">2010</xref>)</td></tr><tr><td>HM545731</td><td>Uncultured fungus</td><td>Root tip</td><td>Italy</td><td><italic>Pinus pinaster</italic></td><td>Buscardo et al (<xref ref-type="bibr" rid="CR10">2011</xref>)</td></tr><tr><td>HQ259630-HQ259639</td><td>Uncultured ECM fungus</td><td>Root tip</td><td>Germany: Saxony-Anhalt, Duebener Heide, Roesa</td><td><italic>Pinus sylvestris</italic></td><td>Schulz et al (<xref ref-type="bibr" rid="CR73">2012</xref>)</td></tr><tr><td>HQ625448</td><td>Uncultured fungus</td><td>Root tip</td><td>Portugal</td><td><italic>Pinus pinaster</italic></td><td>Buscardo et al (<xref ref-type="bibr" rid="CR11">2012</xref>)</td></tr><tr><td>JQ888192</td><td rowspan="2"><italic>R. luteolus</italic></td><td rowspan="2">Basidiome</td><td rowspan="2">UK: Scotland, Culbin forest</td><td rowspan="2"><italic>Pinus sylvestris</italic> and <italic>P. nigra</italic> plantation</td><td rowspan="2">Pickles et al (<xref ref-type="bibr" rid="CR62">2012</xref>)</td></tr><tr><td>UDB001618</td></tr><tr><td>JQ975973</td><td>Uncultured fungus</td><td>Root tip</td><td>Spain</td><td><italic>Pinus pinaster</italic></td><td>Rincón et al. (<xref ref-type="bibr" rid="CR68">2014</xref>)</td></tr><tr><td>Outgroup</td><td>AF062933</td><td><italic>Rhizopogon succosus</italic></td><td>Basidiome</td><td>USA: West Virginia</td><td><italic>Pinus</italic> sp.</td><td>Grubisha et al (<xref ref-type="bibr" rid="CR24">2002</xref>)</td></tr></tbody></table><table-wrap-foot><p><sup>a</sup>Unknown possible host</p></table-wrap-foot></table-wrap><fig id="Fig1"><label>Fig. 1</label><caption><p>The 50 % majority-rule consensus tree of ITS nrDNA sequences of <italic>Rhizopogon luteolus</italic> and <italic>R. verii</italic> using Bayesian approach. A sequence of <italic>R. succosus</italic> was indicated as outgroup. Sequences from <italic>Rhizopogon luteolus</italic> and <italic>R. verii</italic> specimen types are marked in <italic>bold</italic>, as well as the accession numbers of the new sequences obtained in this study from Brazil and Germany. <italic>Numbers at the nodes</italic> indicate the percentage of boostrap values obtained from parsimony analysis with PAUP, and the posterior probabilities from the Bayesian analysis</p></caption><graphic xlink:href="572_2015_678_Fig1_HTML" id="MO1"></graphic></fig></p><p>Including <italic>R. succosus</italic> as outgroup, sequences are distributed in three highly supported clades. The clade A (bs = 92 %, pp = 1.0) grouped three sequences from Japan and South Korea, collected under <italic>Pinus densiflora</italic> and <italic>Pinus thunbergii</italic> from unidentified collections (both basidiomata and ECM). The clade B (bs = 93 %, pp = 1.0) included three sequences, two from Estonia and the sequence from the neotype of <italic>R. luteolus</italic> from Uppsala (Sweden) [designated in Martín (<xref ref-type="bibr" rid="CR39">1996</xref>)], all under <italic>Pinus</italic> species; this <italic>R. luteolus</italic> clade is the sister group of the clade C (bs = 84 %, pp = 1.0) that grouped 47 sequences, including the sequence of the type of <italic>R. verii</italic>, a species described from Tunisia under <italic>P. pinaster</italic>, eight sequences identified as <italic>R. luteolus</italic> collected under different <italic>Pinus</italic> species (mainly <italic>P. pinaster</italic> and <italic>P. sylvestris</italic>), from Europe and New Zealand, and many sequences from uncultured ectomycorrhizal fungi. All new sequences obtained from Germany and Brazil were grouped in clade C, confirming that they belong to the species <italic>R. verii</italic>.</p></sec><sec id="Sec8"><title><italic>Rhizopogon verii</italic> morphological descriptions</title><p><italic>Basidiomes</italic> (7–) 18–23 mm width, (11–) 20–27 mm high, depressed subglobose to irregular, others are compressed, covered by red to reddish yellow rhizomorphs (HUE10R 5/8), 0.1–05-mm diam., appressed to the peridium (Fig. <xref rid="Fig2" ref-type="fig">2a, c</xref>). Peridium <0.5 mm thick, pink (HUE7.5YR 8/4) to reddish yellow (HUE 7.5YR 7/6) in maturity, glabrous. Gleba loculate, rounded locules up to 0.5-μm diam., none gelatinized, olive brown (HUE 2.5Y 4/4) to dark-reddish-brown (HUE 2.5YR 3/4) at maturity, columella absent (Fig. <xref rid="Fig2" ref-type="fig">2a, b</xref>). <italic>Microscopic characters</italic>: Peridium 358–384 μm thick, composed of prostate to interwoven hyphae (<italic>luteolus</italic>-type); external layer formed by abundant yellowish brown to brown hyphae, walls thin to thickened, encrusted with irregular granules and crystals, some amorphous, brown pigmented bodies also present, 1.5–7-μm diam; internal layer composed by hyaline, smooth, and thick-walled hyphae, compactly interwoven, filamentous to inflated hyphae broader than the external layer, 3–12-μm diam. (Fig. <xref rid="Fig3" ref-type="fig">3b</xref>). Trama 11–25 μm thick, formed by interwoven hyphae, often in part gelatinized, hyaline, smooth and thin-walled, simple septate hyphae, 1–5-μm diam. Clamp connections absent in all septa. Subhymenium ramose, hyaline, 3–5-μm diam. Brachybasidioles clavate to cylindrical (12–) 14–20 × 3–5 μm. Basidia are lageniform, with a thick-walled (<1.5-μm diam.), ventricose base (9–20-μm length × 3.5–8 μm width), and a thin-walled beak (5.5–14.5 μm length × 2–4 μm width), developing from 6 to 8 hyaline sterigmata (Fig. <xref rid="Fig3" ref-type="fig">3a</xref>). Basidiospores 5–8 × 2–3 μm (<italic>L</italic> = 6.6 μm, <italic>W</italic> = 2.3 μm, <italic>Q</italic> = 2–3.5 (– 4.5), <italic>Q</italic><sub>m</sub> = 2.94), narrowly ellipsoid, elongate to slightly cylindrical, with a not much truncate apex, smooth and thin to thickened wall, hyaline to pale greenish in KOH 5 %, generally mono- or bi-guttulate (Fig. <xref rid="Fig3" ref-type="fig">3c</xref>). <italic>Chemical reactions</italic>: Peridium with KOH 5 % revives orange pigments, even in dried specimens.<fig id="Fig2"><label>Fig. 2</label><caption><p><italic>Rhizopogon verii</italic> (UFRN-fungos 2372). <bold>a</bold> Basidiomes. <bold>b</bold> Longitudinal section of basidioma showing the gleba. <bold>c</bold> Surface of peridium showing the reddish rhizomorphs. <italic>Scale bars</italic> represent 20 mm (<bold>a</bold>) and 10 mm (<bold>b</bold>–<bold>c</bold>)</p></caption><graphic xlink:href="572_2015_678_Fig2_HTML" id="MO2"></graphic></fig><fig id="Fig3"><label>Fig. 3</label><caption><p><italic>Rhizopogon verii</italic> (UFRN-fungos 2372). <bold>a</bold> Basidia. <bold>b</bold> Peridium showing differentiation of the outer and inner peridial layers. <bold>c</bold> Basidiospores. <italic>Scale bars</italic> represent 10 μm</p></caption><graphic xlink:href="572_2015_678_Fig3_HTML" id="MO3"></graphic></fig></p><p><italic>Ectomycorrhiza</italic> (Fig. <xref rid="Fig4" ref-type="fig">4a</xref>) dichotomous ramified with 1–4 orders; ectomycorrhizal systems dense and abundant; distinct mantle surface and cortical cells not visible; mantle not transparent, mycorrhiza surface reticulate, taste mild, surface hydrophobic; system 1–10 mm long, unramified ends <2 mm long, diameter of unramified ends 0.20–0.40 μm; mycorrhizal ends straight, not inflated. Ectomycorrhiza ochre to yellowish, in parts shiny, older parts ochre to yellowish covered with soil particles; the very tips ochre to yellowish, no soil particles attached; older parts light brown, shiny, not carbonizing, no dots on mantle. <italic>Laticifers</italic> absent. <italic>Rhizomorphs</italic>—present, infrequent, origin proximal with a distinct connection to mantle; infrequently ramified, at restricted point; concolors to mantle (ochre, yellowish brown); margin smooth, in cross-section roundish, 5–60 μm in diameter, emanating hyphae present but infrequent; sclerotia on rhizomorphs not observed. <italic>Anatomy of outer mantle layers</italic> (Fig. <xref rid="Fig5" ref-type="fig">5a</xref>): plectenchymatous, hyphae rather irregularly arranged, no special pattern discernible (type B); hyphae with septae, forked, some hyphal junctions inflated at distal end; cells 10–50 (80)-μm long, 2–7 μm in diameter; hyphal net present, loose, some terminal hyphae forming cystidia; cells not filled with oily droplets, drops of exuded pigment, brownish content or needle-like content, blue granules, crystals, or cells of mounds absent; cell not colored, cell walls thin (<2 μm), cells 3–7 μm in diameter; clamps absent, septa as thick as walls, surface of cells smooth; matrix not gelatinous. <italic>Anatomy of middle mantle layers</italic> (Fig. <xref rid="Fig5" ref-type="fig">5b</xref>) plectenchymatous, hyphae arranged in broad streaks of parallel hyphae, matrix present and gelatinous; cells (5) 8–30 (80) μm long, 2–5 (7) μm in diameter; cells not filled with oily droplets brownish content or needle-like content, blue granules, crystals, or cells of mounds absent; cell not colored. <italic>Anatomy of inner mantle layers</italic> (Fig. <xref rid="Fig5" ref-type="fig">5c</xref>): pseudoparenchymatous, hyphae arranged with no pattern, matrix present and gelatinous; clamps not observed; cells not filled with oily droplets, brownish content or needle-like content and blue granules not observed. <italic>Anatomy of outer mantle layer of ectomycorrhizal tip</italic> (Fig. <xref rid="Fig5" ref-type="fig">5e, f</xref>): organized like other parts of mantle. <italic>Anatomy of cystidia</italic> (Fig. <xref rid="Fig6" ref-type="fig">6a</xref>): cystidia present, infrequent, only one type of cystidia present in the form of a normal hypha but twisted (type L); cells with septa, septa simple, no clamp connection observed, thin walled, cell walls not colored; cells not filled, no apical knob present, not branched; cells 10–50 (–65) μm long, diameter of proximal ends 3–6 μm; and distal ends 2–5 μm; surface smooth or infrequently covered with soil particles. <italic>Anatomy of emanating hyphae</italic> (Fig. <xref rid="Fig5" ref-type="fig">5d</xref>): hyphae observed as hyphal net over ectomycorrhiza forming short non-branched or branched terminal hyphae but not forming cystidia; cell walls thin, not colored, or infrequently covered with soil particles; clamp connections not present; anastomoses present, infrequent, opened with a long or rarely short bridge, anastomose bridge as thick as hyphae, cell walls of anastomoses as thick as hyphae. <italic>Anatomy of rhizomorphs</italic> (Fig. <xref rid="Fig6" ref-type="fig">6b</xref>): differentiated with thick central hyphae and complete septa (type E); nodia present, conical young side branches lacking, gelatinous matrix lacking, trumpet-like ambulate hyphae present; cystidia, laticifers, surface cell staining with sulfo-vanilline and hyphae filled with brownish substance or crystal-like reflecting content, blue granules all absent; central vessel-like hyphae present, without or with one side branch at septum, diameter 6–8 (–10) μm, thickened part distal, cell wall thin and color of cell walls lacking; non-vessel-like central hyphae 2–5 (–6) μm in diameter, central hyphae with septa, no clamp connections observed, septa of the same thickness as walls, color of cells lacking; peripheral hyphae 2–5 (–7) μm in diameter, cell walls <1 μm thick, surface smooth, droplets of secreted pigment, color of cells, balls of intertwined ramified thin hyphae or crystals all lacking. <italic>Chlamydospores</italic> not observed. <italic>Sclerotia</italic> not observed. <italic>Anatomy of longitudinal section</italic> (Fig. <xref rid="Fig4" ref-type="fig">4b</xref>): mantle 50–100 μm thick, different layers in mantle discernable, outer mantle layer plectenchymatous, inner mantle layer pseudoparenchymatous. <italic>Hartig net</italic> palmetto type with a single hyphal row (Fig. <xref rid="Fig4" ref-type="fig">4b</xref>), no haustoria observed. <italic>Autofluorescence</italic>: of the whole mycorrhiza not observed for rhodamine, green fluorescent, and DAPI filters. <italic>Chemical reactions</italic>: sulfo-vanilline—no reaction; lactic acid—no reaction, cotton blue lactic acid—blue spots in mantle cells.<fig id="Fig4"><label>Fig. 4</label><caption><p>Ectomycorrhiza <italic>Rhizopogon verii</italic>-<italic>Pinus sylvestris</italic>. <bold>a</bold> Habitus. <bold>b</bold> Longitudinal semi-thin section of the ectomycorrhiza <italic>Rhizopogon verii</italic>-<italic>Pinus sylvestris. CC</italic> central cylinder, <italic>HM</italic> hyphal mantle, <italic>HN</italic> Hartig net. <italic>Scale bars</italic> represent 2 mm (<bold>a</bold>) and 50 μm (<bold>b</bold>)</p></caption><graphic xlink:href="572_2015_678_Fig4_HTML" id="MO4"></graphic></fig><fig id="Fig5"><label>Fig. 5</label><caption><p>Anatomy of <italic>Rhizopogon verii</italic> ectomycorrhiza. <bold>a</bold> The outer mantle layers with septated, occasionally branched, and at distal ends inflated hyphae. <bold>b</bold> The middle mantle layers with hyphae arranged in broad streaks of parallel hyphae and gelatinous matrix present. <bold>c</bold> The pseudoparenchymatous inner mantle layers, hyphae arranged with no pattern and gelatinous matrix present. <bold>d</bold> Hyphal net over ectomycorrhiza. <bold>e</bold> Outer mantle layers. <bold>f</bold> Inner mantle layers of the very tip of ectomycorrhiza. <italic>Scale bars</italic> represent 10 μm (<bold>a</bold>, <bold>b</bold>, <bold>e</bold>, <bold>f</bold>) and 50 μm (<bold>c</bold>, <bold>d</bold>)</p></caption><graphic xlink:href="572_2015_678_Fig5_HTML" id="MO5"></graphic></fig><fig id="Fig6"><label>Fig. 6</label><caption><p>Anatomy of <italic>Rhizopogon verii</italic> ectomycorrhiza emanating elements. <bold>a</bold> Cystidia in the form of a normal hypha but twisted (type L). <bold>b</bold> Rhizomorphs differentiated with thick central hyphae and complete septa (type E). <italic>Scale bars</italic> represent 20 μm (<bold>a</bold>) and 10 μm (<bold>b</bold>)</p></caption><graphic xlink:href="572_2015_678_Fig6_HTML" id="MO6"></graphic></fig></p><p>Distribution: Belgium, Brazil, Czech Republic, Germany, Lithuania, New Zealand, Spain, Tunisia, and the UK.</p><p>Specimens examined: The data of the specimens examined are included in Table <xref rid="Tab1" ref-type="table">1</xref>. Brazilian collections are located at the herbarium of the Universidade Federal do Rio Grande do Norte of (UFRN) and Universidade Federal de Pernambuco (URM), and the German specimens at the Mycotheca and Herbarium of Slovenian Forestry University (LJF).</p></sec></sec><sec id="Sec9"><title>Discussion</title><p><italic>Rhizopogon verii</italic> was originally described from Tunisia (Pacioni <xref ref-type="bibr" rid="CR58">1984a</xref>), under <italic>P. pinaster</italic>. Since Pacioni’s discovery, little was published related to these species; however, in the past few years, new samples were collected in Spain (Martín <xref ref-type="bibr" rid="CR39">1996</xref>). With the data obtained in our study, a general distribution of <italic>R. verii</italic> is shown, both in natural and planted pine forests, and it is expected that this species can be found in other countries where pine plantations were established using European seedling material.</p><p>Based on morphological data, Martín (<xref ref-type="bibr" rid="CR39">1996</xref>) considered that in Europe, the wider distributed <italic>Rhizopogon</italic> species with <italic>luteolus</italic>-type peridium was <italic>R. luteolus</italic>. However, the present study combining basidiomata and EcM anatomy, together with molecular analyses, shows that the species <italic>R. verii</italic> is well defined and commonly present in Europe. Distribution of <italic>R. verii</italic> on other continents is fairly unknown, but the ecology of known sites indicates several similarities. Mineral and sandy soil requirements (Table <xref rid="Tab1" ref-type="table">1</xref>) with Pinaceae for <italic>Rhizopogon</italic> were recorded for Europe and Africa (Raidl and Agerer <xref ref-type="bibr" rid="CR64">1998</xref>). Similarly the Brazilian specimens were gathered on sandy soil in natural sand dune plots, at the base of a <italic>P. taeda</italic> site in the Campos Sulinos (or Pampa) biome, especially covered by open grassy formations used as natural pastures (Overbeck et al. <xref ref-type="bibr" rid="CR57">2007</xref>; Fiaschi and Pirani <xref ref-type="bibr" rid="CR18">2009</xref>). In a floristic study for Brazil, Porto and Dillenburg (<xref ref-type="bibr" rid="CR63">1986</xref>) reported that the indigenous vegetation is composed by members of Bignoniaceae, Cactaceae, Euphorbiaceae, Fabaceae (subfam. Caesalpinoideae and Faboideae), Myrtaceae, Nyctaginaceae, Rubiaceae, and Sapotaceae, but the presence of exotic tree species, such as <italic>Pinus</italic> or <italic>Eucalyptus</italic>, was required. <italic>Rhizopogon</italic> data from the tropical and subtropical region are rarely available, limiting the knowledge about the identification and phylogenetic placement of those fungi. In Brazil, the genus was introduced through seedlings of exotic <italic>Pinus</italic> spp. (Sulzbacher et al. <xref ref-type="bibr" rid="CR75">2013</xref>) in the southern and southeast region (Giachini et al. <xref ref-type="bibr" rid="CR20">2000</xref>; Baseia and Milanez <xref ref-type="bibr" rid="CR4">2002</xref>; Giachini et al. <xref ref-type="bibr" rid="CR21">2004</xref>; Sobestiansky <xref ref-type="bibr" rid="CR72">2005</xref>; Cortez et al. <xref ref-type="bibr" rid="CR15">2011</xref>). Neves and Capelari (<xref ref-type="bibr" rid="CR54">2007</xref>) reported seven species of this genus in a Brazilian checklist (<italic>R. fuscorubens</italic> Smith, <italic>R. luteolus</italic> Fr. & Nordholm, <italic>R. nigrescens</italic> Coker & Couch, <italic>R. roseolus</italic> Corda sensu Smith, <italic>R. rubescens</italic> (Tul.) Tulasne, <italic>R. vulgaris</italic> (Vitt.) Lange, and <italic>R. zelleri</italic> Smith).</p><p>The studied <italic>R. verii</italic> Brazilian basidiomata covered different developmental stages (Fig. <xref rid="Fig2" ref-type="fig">2a–c</xref>), thus providing more information related to the basidiome morphology. The Brazilian collection exhibits basidiomata very similar to that illustrated by Pacioni (<xref ref-type="bibr" rid="CR60">1988</xref>): subglobose to irregular basidiomata, covered by reddish yellow rhizomorphs and with an olive brown gleba. <italic>Rhizopogon verii</italic> shared several features with the widespread <italic>R. luteolus</italic> (Martín <xref ref-type="bibr" rid="CR39">1996</xref>), for example, the basidiome shapes, rhizomorphs covering the whole peridium surface, also the shape and size of basidiospores and the <italic>luteolus</italic>-type peridium. However, <italic>R. luteolus</italic> has a clavate to cylindrical basidia, with thin wall, and <italic>R. verii</italic> has mostly lageniform basidia, with a thick-walled ventricose base up to 1.5 μm diam. as described in Martín (<xref ref-type="bibr" rid="CR39">1996</xref>). This morphological distinction between <italic>R. luteolus</italic> and <italic>R. verii</italic> is well supported by phylogenetic species delimitation using nrDNA ITS spacer molecular characterization which separated these two morphological groups in two distinct terminal clades (Fig. <xref rid="Fig1" ref-type="fig">1</xref>).</p><p>The comprehensive description of <italic>R. verii</italic> ectomycorrhiza on <italic>P. sylvestris</italic> is provided for the first time. In comparison to other described ectomycorrhizae from the genus <italic>Rhizopogon</italic> (<ext-link ext-link-type="uri" xlink:href="http://www.deemy.de/">www.deemy.de</ext-link>; Mohan et al. <xref ref-type="bibr" rid="CR48">1993</xref>), ectomycorrhiza of <italic>R. verii</italic> can be easily distinguished at least by the plectenchymatous mantle type B bearing some inflated cells at proximal end next to septae, the presence of rhizomorphs type E, cystidia type L, and loose hyphal net covering ectomycorrhiza. On the other hand, <italic>R. luteolus</italic> ectomycorrhiza showed type E of outer mantle layers, no emanating hyphae of cystidia and type F rhizomorphs (Uhl <xref ref-type="bibr" rid="CR81">1988</xref>). A more distant related <italic>R. roseolus</italic> ectomycorrhiza showed outer mantle type C and distinct reddish to whitish color of vital ECM tips (Raidl and Agerer <xref ref-type="bibr" rid="CR64">1998</xref>) and <italic>Rhizopogon melanogastroides</italic> with the same mantle type but ectomycorrhiza color similar yellowish to <italic>R. verii</italic> (Raidl et al. <xref ref-type="bibr" rid="CR65">1998</xref>). Morphological ECM characters of <italic>R. verii</italic> fit well to some previous observations by Agerer (<xref ref-type="bibr" rid="CR2">2006</xref>) who noted that <italic>Rhizopogon</italic> has one of the most advanced rhizomorph-type structure (the boletoid rhizomorphs).</p><p>The combination of molecular analysis and morphological analyses of sporocarps and ectomycorrhiza supports the separation of <italic>R. verii</italic> from other <italic>Rhizopogon</italic> species. We also confirmed that <italic>R. verii</italic> has global distribution, most likely to originate from Europe but being introduced to all continents, with most recent discovery in South America, namely from pine plantation in Brazil and any further exploitations of the species globally would contribute valuable information to its distribution and ecology. As mentioned, in Tedersoo et al. (<xref ref-type="bibr" rid="CR77">2010</xref>) and Tedersoo and Smith (<xref ref-type="bibr" rid="CR78">2013</xref>), some lineages, such as the genus <italic>Rhizopogon</italic>, are restricted to this host family, hence explaining their geographical distribution.</p></sec></body><back><ack><p>The study was financed by the Coordination for the Improvement of Higher Education Personnel (CAPES—Brazil, scholarships granted to the senior author). The work was co-financed by the Brazil–Slovenia bilateral project (BI-BR/11-13-005(SRA)/490648/2010-0 (CNPq)), by EUFORINNO 7th FP EV Infrastructure Program (RegPot No. 315982), and the Research Program in Forest Biology, Ecology and Technology (P4-0107) of the Slovenian Research Agency. Part of the molecular analyses have been done in the framework of the CNPq project PVE 407474/2013-7. 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