Unequal Recombination and Evolution of the Mating-Type (MAT) Loci in the Pathogenic Fungus Grosmannia clavigera and Relatives
Identifieur interne : 000179 ( Pmc/Curation ); précédent : 000178; suivant : 000180Unequal Recombination and Evolution of the Mating-Type (MAT) Loci in the Pathogenic Fungus Grosmannia clavigera and Relatives
Auteurs : Clement K.-M. Tsui [Canada] ; Scott Diguistini [Canada] ; Ye Wang [Canada] ; Nicolas Feau [Canada] ; Braham Dhillon [Canada] ; Jörg Bohlmann [Canada] ; Richard C. Hamelin [Canada]Source :
- G3: Genes|Genomes|Genetics [ 2160-1836 ] ; 2013.
Abstract
Sexual reproduction in fungi is regulated by the mating-type (
Url:
DOI: 10.1534/g3.112.004986
PubMed: 23450093
PubMed Central: 3583454
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) Loci in the Pathogenic Fungus <italic>Grosmannia clavigera</italic>
and Relatives</title>
<author><name sortKey="Tsui, Clement K M" sort="Tsui, Clement K M" uniqKey="Tsui C" first="Clement K.-M." last="Tsui">Clement K.-M. Tsui</name>
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<author><name sortKey="Feau, Nicolas" sort="Feau, Nicolas" uniqKey="Feau N" first="Nicolas" last="Feau">Nicolas Feau</name>
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<affiliation wicri:level="1"><nlm:aff id="aff3">Michael Smith Laboratory, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
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</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Natural Resources Canada, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7</nlm:aff>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Unequal Recombination and Evolution of the Mating-Type (<italic>MAT</italic>
) Loci in the Pathogenic Fungus <italic>Grosmannia clavigera</italic>
and Relatives</title>
<author><name sortKey="Tsui, Clement K M" sort="Tsui, Clement K M" uniqKey="Tsui C" first="Clement K.-M." last="Tsui">Clement K.-M. Tsui</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Diguistini, Scott" sort="Diguistini, Scott" uniqKey="Diguistini S" first="Scott" last="Diguistini">Scott Diguistini</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Department of Wood Science, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Wood Science, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wang, Ye" sort="Wang, Ye" uniqKey="Wang Y" first="Ye" last="Wang">Ye Wang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Department of Wood Science, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Wood Science, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Feau, Nicolas" sort="Feau, Nicolas" uniqKey="Feau N" first="Nicolas" last="Feau">Nicolas Feau</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Dhillon, Braham" sort="Dhillon, Braham" uniqKey="Dhillon B" first="Braham" last="Dhillon">Braham Dhillon</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Bohlmann, Jorg" sort="Bohlmann, Jorg" uniqKey="Bohlmann J" first="Jörg" last="Bohlmann">Jörg Bohlmann</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff3">Michael Smith Laboratory, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Michael Smith Laboratory, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Hamelin, Richard C" sort="Hamelin, Richard C" uniqKey="Hamelin R" first="Richard C." last="Hamelin">Richard C. Hamelin</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff4">Natural Resources Canada, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7</nlm:aff>
<country>Canada</country>
<wicri:regionArea>Natural Resources Canada, Laurentian Forestry Centre, Québec, QC</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">G3: Genes|Genomes|Genetics</title>
<idno type="eISSN">2160-1836</idno>
<imprint><date when="2013">2013</date>
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<front><div type="abstract" xml:lang="en"><p>Sexual reproduction in fungi is regulated by the mating-type (<italic>MAT</italic>
) locus where recombination is suppressed. We investigated the evolution of <italic>MAT</italic>
loci in eight fungal species belonging to <italic>Grosmannia</italic>
and <italic>Ophiostoma</italic>
(Sordariomycetes, Ascomycota) that include conifer pathogens and beetle symbionts. The <italic>MAT1-2</italic>
idiomorph/allele was identified from the assembled and annotated <italic>Grosmannia clavigera</italic>
genome, and the <italic>MAT</italic>
locus is flanked by genes coding for cytoskeleton protein (<italic>SLA</italic>
) and DNA lyase. The synteny of these genes is conserved and consistent with other members in Ascomycota. Using sequences from <italic>SLA</italic>
and flanking regions, we characterized the <italic>MAT1-1</italic>
idiomorph from other isolates of <italic>G. clavigera</italic>
and performed dotplot analysis between the two idiomorphs. Unexpectedly, the <italic>MAT1-2</italic>
idiomorph contains a truncated <italic>MAT1-1-1</italic>
gene upstream of the <italic>MAT1-2-1</italic>
gene that bears the high-mobility-group domain. The nucleotide and amino acid sequence of the truncated <italic>MAT1-1-1</italic>
gene is similar to its homologous copy in the <italic>MAT1-1</italic>
idiomorph in the opposite mating-type isolate, except that positive selection is acting on the truncated gene and the alpha(α)-box that encodes the transcription factor has been deleted. The <italic>MAT</italic>
idiomorphs sharing identical gene organization were present in seven additional species in the Ophiostomatales, suggesting that the presence of truncated <italic>MAT1-1-1</italic>
gene is a general pattern in this order. We propose that an ancient unequal recombination event resulted in the ancestral <italic>MAT1-1-1</italic>
gene integrated into the <italic>MAT1-2</italic>
idiomorph and surviving as the truncated <italic>MAT1-1-1</italic>
genes. The α-box domain of <italic>MAT1-1-1</italic>
gene, located at the same <italic>MAT</italic>
locus adjacent to the <italic>MAT1-2-1</italic>
gene, could have been removed by deletion after recombination due to mating signal interference. Our data confirmed a 1:1 MAT/sex ratio in two pathogen populations, and showed that all members of the Ophiostomatales studied here including those that were previously deemed asexual have the potential to reproduce sexually. This ability can potentially increase genetic variability and can enhance fitness in new, ecological niches.</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">G3 (Bethesda)</journal-id>
<journal-id journal-id-type="iso-abbrev">Genetics</journal-id>
<journal-id journal-id-type="hwp">G3: Genes, Genomes, Genetics</journal-id>
<journal-id journal-id-type="pmc">G3: Genes, Genomes, Genetics</journal-id>
<journal-id journal-id-type="publisher-id">G3: Genes, Genomes, Genetics</journal-id>
<journal-title-group><journal-title>G3: Genes|Genomes|Genetics</journal-title>
</journal-title-group>
<issn pub-type="epub">2160-1836</issn>
<publisher><publisher-name>Genetics Society of America</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23450093</article-id>
<article-id pub-id-type="pmc">3583454</article-id>
<article-id pub-id-type="publisher-id">GGG_004986</article-id>
<article-id pub-id-type="doi">10.1534/g3.112.004986</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Investigations</subject>
</subj-group>
</article-categories>
<title-group><article-title>Unequal Recombination and Evolution of the Mating-Type (<italic>MAT</italic>
) Loci in the Pathogenic Fungus <italic>Grosmannia clavigera</italic>
and Relatives</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Tsui</surname>
<given-names>Clement K.-M.</given-names>
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<xref ref-type="aff" rid="aff1">*</xref>
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</contrib>
<contrib contrib-type="author"><name><surname>DiGuistini</surname>
<given-names>Scott</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Ye</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Feau</surname>
<given-names>Nicolas</given-names>
</name>
<xref ref-type="aff" rid="aff1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dhillon</surname>
<given-names>Braham</given-names>
</name>
<xref ref-type="aff" rid="aff1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bohlmann</surname>
<given-names>Jörg</given-names>
</name>
<xref ref-type="aff" rid="aff1">*</xref>
<xref ref-type="aff" rid="aff3"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hamelin</surname>
<given-names>Richard C.</given-names>
</name>
<xref ref-type="aff" rid="aff1">*</xref>
<xref ref-type="aff" rid="aff4"><sup>§</sup>
</xref>
</contrib>
<aff id="aff1"><label>*</label>
Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</aff>
<aff id="aff2"><label>†</label>
Department of Wood Science, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</aff>
<aff id="aff3"><label>‡</label>
Michael Smith Laboratory, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4</aff>
<aff id="aff4"><label>§</label>
Natural Resources Canada, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7</aff>
</contrib-group>
<author-notes><fn><p>Supporting information is available online at <ext-link ext-link-type="uri" xlink:href="http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.112.004986/-/DC1">http://www.g3journal.org/lookup/suppl/doi:10.1534/g3.112.004986/-/DC1</ext-link>
</p>
</fn>
<fn><p>Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. JX402930−JX402996.</p>
</fn>
<corresp id="cor1"><label>1</label>
Corresponding author: 2424 Main Mall, Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4. E-mail: <email>clementsui@gmail.com</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>1</day>
<month>3</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection"><month>3</month>
<year>2013</year>
</pub-date>
<volume>3</volume>
<issue>3</issue>
<fpage>465</fpage>
<lpage>480</lpage>
<history><date date-type="received"><day>14</day>
<month>11</month>
<year>2012</year>
</date>
<date date-type="accepted"><day>02</day>
<month>1</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013 Tsui <italic>et al.</italic>
</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="465.pdf"></self-uri>
<abstract><p>Sexual reproduction in fungi is regulated by the mating-type (<italic>MAT</italic>
) locus where recombination is suppressed. We investigated the evolution of <italic>MAT</italic>
loci in eight fungal species belonging to <italic>Grosmannia</italic>
and <italic>Ophiostoma</italic>
(Sordariomycetes, Ascomycota) that include conifer pathogens and beetle symbionts. The <italic>MAT1-2</italic>
idiomorph/allele was identified from the assembled and annotated <italic>Grosmannia clavigera</italic>
genome, and the <italic>MAT</italic>
locus is flanked by genes coding for cytoskeleton protein (<italic>SLA</italic>
) and DNA lyase. The synteny of these genes is conserved and consistent with other members in Ascomycota. Using sequences from <italic>SLA</italic>
and flanking regions, we characterized the <italic>MAT1-1</italic>
idiomorph from other isolates of <italic>G. clavigera</italic>
and performed dotplot analysis between the two idiomorphs. Unexpectedly, the <italic>MAT1-2</italic>
idiomorph contains a truncated <italic>MAT1-1-1</italic>
gene upstream of the <italic>MAT1-2-1</italic>
gene that bears the high-mobility-group domain. The nucleotide and amino acid sequence of the truncated <italic>MAT1-1-1</italic>
gene is similar to its homologous copy in the <italic>MAT1-1</italic>
idiomorph in the opposite mating-type isolate, except that positive selection is acting on the truncated gene and the alpha(α)-box that encodes the transcription factor has been deleted. The <italic>MAT</italic>
idiomorphs sharing identical gene organization were present in seven additional species in the Ophiostomatales, suggesting that the presence of truncated <italic>MAT1-1-1</italic>
gene is a general pattern in this order. We propose that an ancient unequal recombination event resulted in the ancestral <italic>MAT1-1-1</italic>
gene integrated into the <italic>MAT1-2</italic>
idiomorph and surviving as the truncated <italic>MAT1-1-1</italic>
genes. The α-box domain of <italic>MAT1-1-1</italic>
gene, located at the same <italic>MAT</italic>
locus adjacent to the <italic>MAT1-2-1</italic>
gene, could have been removed by deletion after recombination due to mating signal interference. Our data confirmed a 1:1 MAT/sex ratio in two pathogen populations, and showed that all members of the Ophiostomatales studied here including those that were previously deemed asexual have the potential to reproduce sexually. This ability can potentially increase genetic variability and can enhance fitness in new, ecological niches.</p>
</abstract>
<kwd-group><kwd>heterothallism</kwd>
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<kwd>selfing</kwd>
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