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Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen.

Identifieur interne : 001D09 ( Main/Exploration ); précédent : 001D08; suivant : 001D10

Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen.

Auteurs : Braham Dhillon [Canada] ; Nicolas Feau [Canada] ; Andrea L. Aerts [États-Unis] ; Stéphanie Beauseigle [Canada] ; Louis Bernier [Canada] ; Alex Copeland [États-Unis] ; Adam Foster [Canada] ; Navdeep Gill [Canada] ; Bernard Henrissat [Arabie saoudite] ; Padmini Herath [Canada] ; Kurt M. Labutti [États-Unis] ; Anthony Levasseur [France] ; Erika A. Lindquist [États-Unis] ; Eline Majoor [Pays-Bas] ; Robin A. Ohm [États-Unis] ; Jasmyn L. Pangilinan [États-Unis] ; Amadeus Pribowo [Canada] ; John N. Saddler [Canada] ; Monique L. Sakalidis [Canada] ; Ronald P. De Vries [Pays-Bas] ; Igor V. Grigoriev [États-Unis] ; Stephen B. Goodwin [États-Unis] ; Philippe Tanguay [Canada] ; Richard C. Hamelin [Canada]

Source :

RBID : pubmed:25733908

Descripteurs français

English descriptors

Abstract

Some of the most damaging tree pathogens can attack woody stems, causing lesions (cankers) that may be lethal. To identify the genomic determinants of wood colonization leading to canker formation, we sequenced the genomes of the poplar canker pathogen, Mycosphaerella populorum, and the closely related poplar leaf pathogen, M. populicola. A secondary metabolite cluster unique to M. populorum is fully activated following induction by poplar wood and leaves. In addition, genes encoding hemicellulose-degrading enzymes, peptidases, and metabolite transporters were more abundant and were up-regulated in M. populorum growing on poplar wood-chip medium compared with M. populicola. The secondary gene cluster and several of the carbohydrate degradation genes have the signature of horizontal transfer from ascomycete fungi associated with wood decay and from prokaryotes. Acquisition and maintenance of the gene battery necessary for growth in woody tissues and gene dosage resulting in gene expression reconfiguration appear to be responsible for the adaptation of M. populorum to infect, colonize, and cause mortality on poplar woody stems.

DOI: 10.1073/pnas.1424293112
PubMed: 25733908
PubMed Central: PMC4371944


Affiliations:


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Le document en format XML

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<region type="state">Californie</region>
</placeName>
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<region type="state">Californie</region>
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<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Fungal Physiology, Centraalbureau voor Schimmelcultures-Royal Netherlands Academy of Arts and Sciences Fungal Biodiversity Centre (CBS-KNAW), 3584 CT, Utrecht, The Netherlands; Fungal Molecular Physiology, Utrecht University, 3584 CT, Utrecht</wicri:regionArea>
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<name sortKey="Ohm, Robin A" sort="Ohm, Robin A" uniqKey="Ohm R" first="Robin A" last="Ohm">Robin A. Ohm</name>
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<nlm:affiliation>US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>US Department of Energy Joint Genome Institute, Walnut Creek</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Pangilinan, Jasmyn L" sort="Pangilinan, Jasmyn L" uniqKey="Pangilinan J" first="Jasmyn L" last="Pangilinan">Jasmyn L. Pangilinan</name>
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<nlm:affiliation>US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>US Department of Energy Joint Genome Institute, Walnut Creek</wicri:cityArea>
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</author>
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<name sortKey="Pribowo, Amadeus" sort="Pribowo, Amadeus" uniqKey="Pribowo A" first="Amadeus" last="Pribowo">Amadeus Pribowo</name>
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<nlm:affiliation>Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; and.</nlm:affiliation>
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<wicri:regionArea>Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC</wicri:regionArea>
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<settlement type="city">Vancouver</settlement>
<region type="state">Colombie-Britannique </region>
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<name sortKey="Saddler, John N" sort="Saddler, John N" uniqKey="Saddler J" first="John N" last="Saddler">John N. Saddler</name>
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<nlm:affiliation>Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; and.</nlm:affiliation>
<country>Canada</country>
<wicri:regionArea>Forest Products Biotechnology and Bioenergy, The University of British Columbia, Vancouver, BC</wicri:regionArea>
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<settlement type="city">Vancouver</settlement>
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<author>
<name sortKey="Sakalidis, Monique L" sort="Sakalidis, Monique L" uniqKey="Sakalidis M" first="Monique L" last="Sakalidis">Monique L. Sakalidis</name>
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<nlm:affiliation>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;</nlm:affiliation>
<country>Canada</country>
<wicri:regionArea>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC</wicri:regionArea>
<orgName type="university">Université de la Colombie-Britannique</orgName>
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<settlement type="city">Vancouver</settlement>
<region type="state">Colombie-Britannique </region>
</placeName>
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<author>
<name sortKey="De Vries, Ronald P" sort="De Vries, Ronald P" uniqKey="De Vries R" first="Ronald P" last="De Vries">Ronald P. De Vries</name>
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<nlm:affiliation>Fungal Physiology, Centraalbureau voor Schimmelcultures-Royal Netherlands Academy of Arts and Sciences Fungal Biodiversity Centre (CBS-KNAW), 3584 CT, Utrecht, The Netherlands; Fungal Molecular Physiology, Utrecht University, 3584 CT, Utrecht, The Netherlands;</nlm:affiliation>
<country xml:lang="fr">Pays-Bas</country>
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<settlement type="city">Utrecht</settlement>
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<orgName type="university">Université d'Utrecht</orgName>
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<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
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<nlm:affiliation>US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>US Department of Energy Joint Genome Institute, Walnut Creek</wicri:cityArea>
</affiliation>
</author>
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<name sortKey="Goodwin, Stephen B" sort="Goodwin, Stephen B" uniqKey="Goodwin S" first="Stephen B" last="Goodwin">Stephen B. Goodwin</name>
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<nlm:affiliation>US Department of Agriculture-Agricultural Research Service Crop Production and Pest Control Research Unit, Purdue University, West Lafayette, IN 47907-2054.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Indiana</region>
</placeName>
<wicri:cityArea>US Department of Agriculture-Agricultural Research Service Crop Production and Pest Control Research Unit, Purdue University, West Lafayette</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Tanguay, Philippe" sort="Tanguay, Philippe" uniqKey="Tanguay P" first="Philippe" last="Tanguay">Philippe Tanguay</name>
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<nlm:affiliation>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, QC, Canada G1V 4C7;</nlm:affiliation>
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<orgName type="university">Université de la Colombie-Britannique</orgName>
<placeName>
<settlement type="city">Vancouver</settlement>
<region type="state">Colombie-Britannique </region>
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<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
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<term>Adaptation, Physiological (genetics)</term>
<term>Ascomycota (genetics)</term>
<term>Ascomycota (growth & development)</term>
<term>Ascomycota (pathogenicity)</term>
<term>Base Sequence (MeSH)</term>
<term>Colony Count, Microbial (MeSH)</term>
<term>Gene Dosage (MeSH)</term>
<term>Gene Expression Regulation, Fungal (MeSH)</term>
<term>Gene Transfer, Horizontal (MeSH)</term>
<term>Genetic Speciation (MeSH)</term>
<term>Genome, Fungal (genetics)</term>
<term>Host-Pathogen Interactions (genetics)</term>
<term>Indole Alkaloids (metabolism)</term>
<term>Molecular Sequence Data (MeSH)</term>
<term>Nitrogen (metabolism)</term>
<term>Phylogeny (MeSH)</term>
<term>Populus (microbiology)</term>
<term>Proteolysis (MeSH)</term>
<term>Synteny (genetics)</term>
<term>Time Factors (MeSH)</term>
<term>Trees (microbiology)</term>
<term>Wood (microbiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Adaptation physiologique (génétique)</term>
<term>Alcaloïdes indoliques (métabolisme)</term>
<term>Arbres (microbiologie)</term>
<term>Ascomycota (croissance et développement)</term>
<term>Ascomycota (génétique)</term>
<term>Ascomycota (pathogénicité)</term>
<term>Azote (métabolisme)</term>
<term>Bois (microbiologie)</term>
<term>Données de séquences moléculaires (MeSH)</term>
<term>Dosage génique (MeSH)</term>
<term>Facteurs temps (MeSH)</term>
<term>Génome fongique (génétique)</term>
<term>Interactions hôte-pathogène (génétique)</term>
<term>Numération de colonies microbiennes (MeSH)</term>
<term>Phylogenèse (MeSH)</term>
<term>Populus (microbiologie)</term>
<term>Protéolyse (MeSH)</term>
<term>Régulation de l'expression des gènes fongiques (MeSH)</term>
<term>Spéciation génétique (MeSH)</term>
<term>Synténie (génétique)</term>
<term>Séquence nucléotidique (MeSH)</term>
<term>Transfert horizontal de gène (MeSH)</term>
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<term>Nitrogen</term>
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</keywords>
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<term>Adaptation, Physiological</term>
<term>Ascomycota</term>
<term>Genome, Fungal</term>
<term>Host-Pathogen Interactions</term>
<term>Synteny</term>
</keywords>
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<term>Ascomycota</term>
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<term>Adaptation physiologique</term>
<term>Ascomycota</term>
<term>Génome fongique</term>
<term>Interactions hôte-pathogène</term>
<term>Synténie</term>
</keywords>
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<term>Arbres</term>
<term>Bois</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Populus</term>
<term>Trees</term>
<term>Wood</term>
</keywords>
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<term>Alcaloïdes indoliques</term>
<term>Azote</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Ascomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Ascomycota</term>
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<keywords scheme="MESH" xml:lang="en">
<term>Base Sequence</term>
<term>Colony Count, Microbial</term>
<term>Gene Dosage</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Gene Transfer, Horizontal</term>
<term>Genetic Speciation</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Proteolysis</term>
<term>Time Factors</term>
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<term>Données de séquences moléculaires</term>
<term>Dosage génique</term>
<term>Facteurs temps</term>
<term>Numération de colonies microbiennes</term>
<term>Phylogenèse</term>
<term>Protéolyse</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Spéciation génétique</term>
<term>Séquence nucléotidique</term>
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<div type="abstract" xml:lang="en">Some of the most damaging tree pathogens can attack woody stems, causing lesions (cankers) that may be lethal. To identify the genomic determinants of wood colonization leading to canker formation, we sequenced the genomes of the poplar canker pathogen, Mycosphaerella populorum, and the closely related poplar leaf pathogen, M. populicola. A secondary metabolite cluster unique to M. populorum is fully activated following induction by poplar wood and leaves. In addition, genes encoding hemicellulose-degrading enzymes, peptidases, and metabolite transporters were more abundant and were up-regulated in M. populorum growing on poplar wood-chip medium compared with M. populicola. The secondary gene cluster and several of the carbohydrate degradation genes have the signature of horizontal transfer from ascomycete fungi associated with wood decay and from prokaryotes. Acquisition and maintenance of the gene battery necessary for growth in woody tissues and gene dosage resulting in gene expression reconfiguration appear to be responsible for the adaptation of M. populorum to infect, colonize, and cause mortality on poplar woody stems. </div>
</front>
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<PMID Version="1">25733908</PMID>
<DateCompleted>
<Year>2015</Year>
<Month>06</Month>
<Day>04</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
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<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>112</Volume>
<Issue>11</Issue>
<PubDate>
<Year>2015</Year>
<Month>Mar</Month>
<Day>17</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen.</ArticleTitle>
<Pagination>
<MedlinePgn>3451-6</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1424293112</ELocationID>
<Abstract>
<AbstractText>Some of the most damaging tree pathogens can attack woody stems, causing lesions (cankers) that may be lethal. To identify the genomic determinants of wood colonization leading to canker formation, we sequenced the genomes of the poplar canker pathogen, Mycosphaerella populorum, and the closely related poplar leaf pathogen, M. populicola. A secondary metabolite cluster unique to M. populorum is fully activated following induction by poplar wood and leaves. In addition, genes encoding hemicellulose-degrading enzymes, peptidases, and metabolite transporters were more abundant and were up-regulated in M. populorum growing on poplar wood-chip medium compared with M. populicola. The secondary gene cluster and several of the carbohydrate degradation genes have the signature of horizontal transfer from ascomycete fungi associated with wood decay and from prokaryotes. Acquisition and maintenance of the gene battery necessary for growth in woody tissues and gene dosage resulting in gene expression reconfiguration appear to be responsible for the adaptation of M. populorum to infect, colonize, and cause mortality on poplar woody stems. </AbstractText>
</Abstract>
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<LastName>Dhillon</LastName>
<ForeName>Braham</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Feau</LastName>
<ForeName>Nicolas</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4; feaunico@mail.ubc.ca Richard.Hamelin@RNCan-NRCan.gc.ca.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Aerts</LastName>
<ForeName>Andrea L</ForeName>
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<Affiliation>US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Beauseigle</LastName>
<ForeName>Stéphanie</ForeName>
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<Affiliation>Department of Forest and Conservation Sciences, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Bernier</LastName>
<ForeName>Louis</ForeName>
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<Affiliation>Centre d'Étude de la Forêt, Université Laval, Québec, QC, Canada G1V 0A6;</Affiliation>
</AffiliationInfo>
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<LastName>Copeland</LastName>
<ForeName>Alex</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598;</Affiliation>
</AffiliationInfo>
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</AffiliationInfo>
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<LastName>Gill</LastName>
<ForeName>Navdeep</ForeName>
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<Affiliation>Department of Botany, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4;</Affiliation>
</AffiliationInfo>
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<LastName>Henrissat</LastName>
<ForeName>Bernard</ForeName>
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<Affiliation>UMR 7257 Centre National de la Recherche Scientifique, Aix-Marseille University, 13288 Marseille, France; Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia;</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Herath</LastName>
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</AffiliationInfo>
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<LastName>LaButti</LastName>
<ForeName>Kurt M</ForeName>
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<LastName>Lindquist</LastName>
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<LastName>Majoor</LastName>
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