The nitrilase PtNIT1 catabolizes herbivore-induced nitriles in Populus trichocarpa.
Identifieur interne : 000C34 ( Main/Exploration ); précédent : 000C33; suivant : 000C35The nitrilase PtNIT1 catabolizes herbivore-induced nitriles in Populus trichocarpa.
Auteurs : Jan Günther [Allemagne] ; Sandra Irmisch [Allemagne, Canada] ; Nathalie D. Lackus [Allemagne] ; Michael Reichelt [Allemagne] ; Jonathan Gershenzon [Allemagne] ; Tobias G. Köllner [Allemagne]Source :
- BMC plant biology [ 1471-2229 ] ; 2018.
Descripteurs français
- KwdFr :
- MESH :
- analogues et dérivés : Alanine.
- enzymologie : Feuilles de plante, Populus.
- génétique : Aminohydrolases, Feuilles de plante, Populus.
- métabolisme : Alanine, Aminohydrolases, Nitriles.
- Herbivorie.
English descriptors
- KwdEn :
- MESH :
- chemical , analogs & derivatives : Alanine.
- chemical , genetics : Aminohydrolases.
- chemical , metabolism : Alanine, Aminohydrolases, Nitriles.
- enzymology : Plant Leaves, Populus.
- genetics : Plant Leaves, Populus.
- Herbivory.
Abstract
BACKGROUND
Nitrilases are nitrile-converting enzymes commonly found within the plant kingdom that play diverse roles in nitrile detoxification, nitrogen recycling, and phytohormone biosynthesis. Although nitrilases are present in all higher plants, little is known about their function in trees. Upon herbivory, poplars produce considerable amounts of toxic nitriles such as benzyl cyanide, 2-methylbutyronitrile, and 3-methylbutyronitrile. In addition, as byproduct of the ethylene biosynthetic pathway upregulated in many plant species after herbivory, toxic β-cyanoalanine may accumulate in damaged poplar leaves. In this work, we studied the nitrilase gene family in Populus trichocarpa and investigated the potential role of the nitrilase PtNIT1 in the catabolism of herbivore-induced nitriles.
RESULTS
A BLAST analysis revealed three putative nitrilase genes (PtNIT1, PtNIT2, PtNIT3) in the genome of P. trichocarpa. While PtNIT1 was expressed in poplar leaves and showed increased transcript accumulation after leaf herbivory, PtNIT2 and PtNIT3 appeared not to be expressed in undamaged or herbivore-damaged leaves. Recombinant PtNIT1 produced in Escherichia coli accepted biogenic nitriles such as β-cyanoalanine, benzyl cyanide, and indole-3-acetonitrile as substrates in vitro and converted them into the corresponding acids. In addition to this nitrilase activity, PtNIT1 showed nitrile hydratase activity towards β-cyanoalanine, resulting in the formation of the amino acid asparagine. The kinetic parameters of PtNIT1 suggest that the enzyme utilizes β-cyanoalanine and benzyl cyanide as substrates in vivo. Indeed, β-cyanoalanine and benzyl cyanide were found to accumulate in herbivore-damaged poplar leaves. The upregulation of ethylene biosynthesis genes after leaf herbivory indicates that herbivore-induced β-cyanoalanine accumulation is likely caused by ethylene formation.
CONCLUSIONS
Our data suggest a role for PtNIT1 in the catabolism of herbivore-induced β-cyanoalanine and benzyl cyanide in poplar leaves.
DOI: 10.1186/s12870-018-1478-z
PubMed: 30348089
PubMed Central: PMC6196558
Affiliations:
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Köllner</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany. koellner@ice.mpg.de.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2018">2018</date><idno type="RBID">pubmed:30348089</idno><idno type="pmid">30348089</idno><idno type="doi">10.1186/s12870-018-1478-z</idno><idno type="pmc">PMC6196558</idno><idno type="wicri:Area/Main/Corpus">000C06</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000C06</idno><idno type="wicri:Area/Main/Curation">000C06</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000C06</idno><idno type="wicri:Area/Main/Exploration">000C06</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The nitrilase PtNIT1 catabolizes herbivore-induced nitriles in Populus trichocarpa.</title><author><name sortKey="Gunther, Jan" sort="Gunther, Jan" uniqKey="Gunther J" first="Jan" last="Günther">Jan Günther</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Irmisch, Sandra" sort="Irmisch, Sandra" uniqKey="Irmisch S" first="Sandra" last="Irmisch">Sandra Irmisch</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Present Address: Michael Smith Laboratories, University of British Columbia, Vancouver, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Present Address: Michael Smith Laboratories, University of British Columbia, Vancouver</wicri:regionArea><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique</region></placeName><orgName type="university">Université de la Colombie-Britannique</orgName></affiliation></author><author><name sortKey="Lackus, Nathalie D" sort="Lackus, Nathalie D" uniqKey="Lackus N" first="Nathalie D" last="Lackus">Nathalie D. Lackus</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Reichelt, Michael" sort="Reichelt, Michael" uniqKey="Reichelt M" first="Michael" last="Reichelt">Michael Reichelt</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Kollner, Tobias G" sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G" last="Köllner">Tobias G. Köllner</name><affiliation wicri:level="1"><nlm:affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany. koellner@ice.mpg.de.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author></analytic><series><title level="j">BMC plant biology</title><idno type="eISSN">1471-2229</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Alanine (analogs & derivatives)</term><term>Alanine (metabolism)</term><term>Aminohydrolases (genetics)</term><term>Aminohydrolases (metabolism)</term><term>Herbivory (MeSH)</term><term>Nitriles (metabolism)</term><term>Plant Leaves (enzymology)</term><term>Plant Leaves (genetics)</term><term>Populus (enzymology)</term><term>Populus (genetics)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Alanine (analogues et dérivés)</term><term>Alanine (métabolisme)</term><term>Aminohydrolases (génétique)</term><term>Aminohydrolases (métabolisme)</term><term>Feuilles de plante (enzymologie)</term><term>Feuilles de plante (génétique)</term><term>Herbivorie (MeSH)</term><term>Nitriles (métabolisme)</term><term>Populus (enzymologie)</term><term>Populus (génétique)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="analogs & derivatives" xml:lang="en"><term>Alanine</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Aminohydrolases</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Alanine</term><term>Aminohydrolases</term><term>Nitriles</term></keywords><keywords scheme="MESH" qualifier="analogues et dérivés" xml:lang="fr"><term>Alanine</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Feuilles de plante</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Aminohydrolases</term><term>Feuilles de plante</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Alanine</term><term>Aminohydrolases</term><term>Nitriles</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Herbivory</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Herbivorie</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND</b></p><p>Nitrilases are nitrile-converting enzymes commonly found within the plant kingdom that play diverse roles in nitrile detoxification, nitrogen recycling, and phytohormone biosynthesis. Although nitrilases are present in all higher plants, little is known about their function in trees. Upon herbivory, poplars produce considerable amounts of toxic nitriles such as benzyl cyanide, 2-methylbutyronitrile, and 3-methylbutyronitrile. In addition, as byproduct of the ethylene biosynthetic pathway upregulated in many plant species after herbivory, toxic β-cyanoalanine may accumulate in damaged poplar leaves. In this work, we studied the nitrilase gene family in Populus trichocarpa and investigated the potential role of the nitrilase PtNIT1 in the catabolism of herbivore-induced nitriles.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>A BLAST analysis revealed three putative nitrilase genes (PtNIT1, PtNIT2, PtNIT3) in the genome of P. trichocarpa. While PtNIT1 was expressed in poplar leaves and showed increased transcript accumulation after leaf herbivory, PtNIT2 and PtNIT3 appeared not to be expressed in undamaged or herbivore-damaged leaves. Recombinant PtNIT1 produced in Escherichia coli accepted biogenic nitriles such as β-cyanoalanine, benzyl cyanide, and indole-3-acetonitrile as substrates in vitro and converted them into the corresponding acids. In addition to this nitrilase activity, PtNIT1 showed nitrile hydratase activity towards β-cyanoalanine, resulting in the formation of the amino acid asparagine. The kinetic parameters of PtNIT1 suggest that the enzyme utilizes β-cyanoalanine and benzyl cyanide as substrates in vivo. Indeed, β-cyanoalanine and benzyl cyanide were found to accumulate in herbivore-damaged poplar leaves. The upregulation of ethylene biosynthesis genes after leaf herbivory indicates that herbivore-induced β-cyanoalanine accumulation is likely caused by ethylene formation.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Our data suggest a role for PtNIT1 in the catabolism of herbivore-induced β-cyanoalanine and benzyl cyanide in poplar leaves.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30348089</PMID><DateCompleted><Year>2018</Year><Month>11</Month><Day>19</Day></DateCompleted><DateRevised><Year>2018</Year><Month>11</Month><Day>19</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2229</ISSN><JournalIssue CitedMedium="Internet"><Volume>18</Volume><Issue>1</Issue><PubDate><Year>2018</Year><Month>Oct</Month><Day>22</Day></PubDate></JournalIssue><Title>BMC plant biology</Title><ISOAbbreviation>BMC Plant Biol</ISOAbbreviation></Journal><ArticleTitle>The nitrilase PtNIT1 catabolizes herbivore-induced nitriles in Populus trichocarpa.</ArticleTitle><Pagination><MedlinePgn>251</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12870-018-1478-z</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Nitrilases are nitrile-converting enzymes commonly found within the plant kingdom that play diverse roles in nitrile detoxification, nitrogen recycling, and phytohormone biosynthesis. Although nitrilases are present in all higher plants, little is known about their function in trees. Upon herbivory, poplars produce considerable amounts of toxic nitriles such as benzyl cyanide, 2-methylbutyronitrile, and 3-methylbutyronitrile. In addition, as byproduct of the ethylene biosynthetic pathway upregulated in many plant species after herbivory, toxic β-cyanoalanine may accumulate in damaged poplar leaves. In this work, we studied the nitrilase gene family in Populus trichocarpa and investigated the potential role of the nitrilase PtNIT1 in the catabolism of herbivore-induced nitriles.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">A BLAST analysis revealed three putative nitrilase genes (PtNIT1, PtNIT2, PtNIT3) in the genome of P. trichocarpa. While PtNIT1 was expressed in poplar leaves and showed increased transcript accumulation after leaf herbivory, PtNIT2 and PtNIT3 appeared not to be expressed in undamaged or herbivore-damaged leaves. Recombinant PtNIT1 produced in Escherichia coli accepted biogenic nitriles such as β-cyanoalanine, benzyl cyanide, and indole-3-acetonitrile as substrates in vitro and converted them into the corresponding acids. In addition to this nitrilase activity, PtNIT1 showed nitrile hydratase activity towards β-cyanoalanine, resulting in the formation of the amino acid asparagine. The kinetic parameters of PtNIT1 suggest that the enzyme utilizes β-cyanoalanine and benzyl cyanide as substrates in vivo. Indeed, β-cyanoalanine and benzyl cyanide were found to accumulate in herbivore-damaged poplar leaves. The upregulation of ethylene biosynthesis genes after leaf herbivory indicates that herbivore-induced β-cyanoalanine accumulation is likely caused by ethylene formation.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Our data suggest a role for PtNIT1 in the catabolism of herbivore-induced β-cyanoalanine and benzyl cyanide in poplar leaves.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Günther</LastName><ForeName>Jan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Irmisch</LastName><ForeName>Sandra</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Present Address: Michael Smith Laboratories, University of British Columbia, Vancouver, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lackus</LastName><ForeName>Nathalie D</ForeName><Initials>ND</Initials><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Reichelt</LastName><ForeName>Michael</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gershenzon</LastName><ForeName>Jonathan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Köllner</LastName><ForeName>Tobias G</ForeName><Initials>TG</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-7037-904X</Identifier><AffiliationInfo><Affiliation>Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745, Jena, Germany. koellner@ice.mpg.de.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>10</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Plant Biol</MedlineTA><NlmUniqueID>100967807</NlmUniqueID><ISSNLinking>1471-2229</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D009570">Nitriles</NameOfSubstance></Chemical><Chemical><RegistryNumber>923-01-3</RegistryNumber><NameOfSubstance UI="C004631">3-cyanoalanine</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.5.4.-</RegistryNumber><NameOfSubstance UI="D000619">Aminohydrolases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.5.5.1</RegistryNumber><NameOfSubstance UI="C021867">nitrilase</NameOfSubstance></Chemical><Chemical><RegistryNumber>OF5P57N2ZX</RegistryNumber><NameOfSubstance UI="D000409">Alanine</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000409" MajorTopicYN="N">Alanine</DescriptorName><QualifierName UI="Q000031" MajorTopicYN="N">analogs & derivatives</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000619" MajorTopicYN="N">Aminohydrolases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D060434" MajorTopicYN="N">Herbivory</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009570" MajorTopicYN="N">Nitriles</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Benzyl cyanide</Keyword><Keyword MajorTopicYN="N">NIT1</Keyword><Keyword MajorTopicYN="N">Nitrilase</Keyword><Keyword MajorTopicYN="N">Plant defense</Keyword><Keyword MajorTopicYN="N">Populus trichocarpa</Keyword><Keyword MajorTopicYN="N">β-Cyanoalanine</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>01</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>10</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>10</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>11</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30348089</ArticleId><ArticleId IdType="doi">10.1186/s12870-018-1478-z</ArticleId><ArticleId IdType="pii">10.1186/s12870-018-1478-z</ArticleId><ArticleId 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sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G" last="Köllner">Tobias G. Köllner</name><name sortKey="Lackus, Nathalie D" sort="Lackus, Nathalie D" uniqKey="Lackus N" first="Nathalie D" last="Lackus">Nathalie D. Lackus</name><name sortKey="Reichelt, Michael" sort="Reichelt, Michael" uniqKey="Reichelt M" first="Michael" last="Reichelt">Michael Reichelt</name></country><country name="Canada"><region name="Colombie-Britannique"><name sortKey="Irmisch, Sandra" sort="Irmisch, Sandra" uniqKey="Irmisch S" first="Sandra" last="Irmisch">Sandra Irmisch</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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