Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus.
Identifieur interne : 002374 ( Main/Corpus ); précédent : 002373; suivant : 002375Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus.
Auteurs : Scott A. Harding ; Liang-Jiao Xue ; Lei Du ; Batbayar Nyamdari ; Richard L. Lindroth ; Robert Sykes ; Mark F. Davis ; Chung-Jui TsaiSource :
- Tree physiology [ 1758-4469 ] ; 2014.
English descriptors
- KwdEn :
- Carbon (metabolism), Carbon Sequestration (MeSH), Chimera (MeSH), Gene Expression Regulation, Plant (MeSH), Genotype (MeSH), Glucosides (metabolism), Glycosides (metabolism), Metabolome (MeSH), Nitrogen (metabolism), Oligonucleotide Array Sequence Analysis (MeSH), Phenethylamines (metabolism), Phenols (metabolism), Plant Leaves (chemistry), Plant Leaves (growth & development), Plant Leaves (immunology), Plant Leaves (metabolism), Polymerization (MeSH), Populus (chemistry), Populus (growth & development), Populus (immunology), Populus (metabolism), Proanthocyanidins (metabolism), Propanols (metabolism).
- MESH :
- chemical , metabolism : Carbon, Glucosides, Glycosides, Nitrogen, Phenethylamines, Phenols, Proanthocyanidins, Propanols.
- chemistry : Plant Leaves, Populus.
- growth & development : Plant Leaves, Populus.
- immunology : Plant Leaves, Populus.
- metabolism : Plant Leaves, Populus.
- Carbon Sequestration, Chimera, Gene Expression Regulation, Plant, Genotype, Metabolome, Oligonucleotide Array Sequence Analysis, Polymerization.
Abstract
The partitioning of carbon for growth, storage and constitutive chemical defenses is widely framed in terms of a hypothetical sink-source differential that varies with nutrient supply. According to this framework, phenolics accrual is passive and occurs in source leaves when normal sink growth is not sustainable due to a nutrient limitation. In assessing this framework, we present gene and metabolite evidence that condensed tannin (CT) accrual is strongest in sink leaves and sequesters carbon in a way that impinges upon foliar sink strength and upon phenolic glycoside (PG) accrual in Populus. The work was based on two Populus fremontii × angustifolia backcross lines with contrasting rates of CT accrual and growth, and equally large foliar PG reserves. However, foliar PG accrual was developmentally delayed in the high-CT, slow-growth line (SG), and nitrogen-limitation led to increased foliar PG accrual only in the low-CT, fast-growth line (FG). Metabolite profiling of developing leaves indicated comparatively carbon-limited amino acid metabolism, depletion of several Krebs cycle intermediates and reduced organ sink strength in SG. Gene profiling indicated that CT synthesis decreased as leaves expanded and PGs increased. A most striking finding was that the nitrogenous monoamine phenylethylamine accumulated only in leaves of SG plants. The potential negative impact of CT hyper-accumulation on foliar sink strength, as well as a mechanism for phenylethylamine involvement in CT polymerization in Populus are discussed. Starch accrual in source leaves and CT accrual in sink leaves of SG may both contribute to the maintenance of a slow-growth phenotype suited to survival in nutrient-poor habitats.
DOI: 10.1093/treephys/tpt097
PubMed: 24336515
Links to Exploration step
pubmed:24336515Le document en format XML
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Harding</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA sharding@uga.edu cjtsai@uga.edu.</nlm:affiliation></affiliation></author><author><name sortKey="Xue, Liang Jiao" sort="Xue, Liang Jiao" uniqKey="Xue L" first="Liang-Jiao" last="Xue">Liang-Jiao Xue</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Du, Lei" sort="Du, Lei" uniqKey="Du L" first="Lei" last="Du">Lei Du</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA Present address: Unit of Computational Medicine, Department of Medicine, Karolinska Institute, Stockholm 17176, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Nyamdari, Batbayar" sort="Nyamdari, Batbayar" uniqKey="Nyamdari B" first="Batbayar" last="Nyamdari">Batbayar Nyamdari</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Lindroth, Richard L" sort="Lindroth, Richard L" uniqKey="Lindroth R" first="Richard L" last="Lindroth">Richard L. 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Harding</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA sharding@uga.edu cjtsai@uga.edu.</nlm:affiliation></affiliation></author><author><name sortKey="Xue, Liang Jiao" sort="Xue, Liang Jiao" uniqKey="Xue L" first="Liang-Jiao" last="Xue">Liang-Jiao Xue</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Du, Lei" sort="Du, Lei" uniqKey="Du L" first="Lei" last="Du">Lei Du</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA Present address: Unit of Computational Medicine, Department of Medicine, Karolinska Institute, Stockholm 17176, Sweden.</nlm:affiliation></affiliation></author><author><name sortKey="Nyamdari, Batbayar" sort="Nyamdari, Batbayar" uniqKey="Nyamdari B" first="Batbayar" last="Nyamdari">Batbayar Nyamdari</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Lindroth, Richard L" sort="Lindroth, Richard L" uniqKey="Lindroth R" first="Richard L" last="Lindroth">Richard L. Lindroth</name><affiliation><nlm:affiliation>Department of Entomology, University of Wisconsin, Madison, WI 53706, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Sykes, Robert" sort="Sykes, Robert" uniqKey="Sykes R" first="Robert" last="Sykes">Robert Sykes</name><affiliation><nlm:affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Davis, Mark F" sort="Davis, Mark F" uniqKey="Davis M" first="Mark F" last="Davis">Mark F. Davis</name><affiliation><nlm:affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Tsai, Chung Jui" sort="Tsai, Chung Jui" uniqKey="Tsai C" first="Chung-Jui" last="Tsai">Chung-Jui Tsai</name><affiliation><nlm:affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA sharding@uga.edu cjtsai@uga.edu.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Tree physiology</title><idno type="eISSN">1758-4469</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Carbon (metabolism)</term><term>Carbon Sequestration (MeSH)</term><term>Chimera (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Genotype (MeSH)</term><term>Glucosides (metabolism)</term><term>Glycosides (metabolism)</term><term>Metabolome (MeSH)</term><term>Nitrogen (metabolism)</term><term>Oligonucleotide Array Sequence Analysis (MeSH)</term><term>Phenethylamines (metabolism)</term><term>Phenols (metabolism)</term><term>Plant Leaves (chemistry)</term><term>Plant Leaves (growth & development)</term><term>Plant Leaves (immunology)</term><term>Plant Leaves (metabolism)</term><term>Polymerization (MeSH)</term><term>Populus (chemistry)</term><term>Populus (growth & development)</term><term>Populus (immunology)</term><term>Populus (metabolism)</term><term>Proanthocyanidins (metabolism)</term><term>Propanols (metabolism)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Carbon</term><term>Glucosides</term><term>Glycosides</term><term>Nitrogen</term><term>Phenethylamines</term><term>Phenols</term><term>Proanthocyanidins</term><term>Propanols</term></keywords><keywords scheme="MESH" qualifier="chemistry" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Plant Leaves</term><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Carbon Sequestration</term><term>Chimera</term><term>Gene Expression Regulation, Plant</term><term>Genotype</term><term>Metabolome</term><term>Oligonucleotide Array Sequence Analysis</term><term>Polymerization</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The partitioning of carbon for growth, storage and constitutive chemical defenses is widely framed in terms of a hypothetical sink-source differential that varies with nutrient supply. According to this framework, phenolics accrual is passive and occurs in source leaves when normal sink growth is not sustainable due to a nutrient limitation. In assessing this framework, we present gene and metabolite evidence that condensed tannin (CT) accrual is strongest in sink leaves and sequesters carbon in a way that impinges upon foliar sink strength and upon phenolic glycoside (PG) accrual in Populus. The work was based on two Populus fremontii × angustifolia backcross lines with contrasting rates of CT accrual and growth, and equally large foliar PG reserves. However, foliar PG accrual was developmentally delayed in the high-CT, slow-growth line (SG), and nitrogen-limitation led to increased foliar PG accrual only in the low-CT, fast-growth line (FG). Metabolite profiling of developing leaves indicated comparatively carbon-limited amino acid metabolism, depletion of several Krebs cycle intermediates and reduced organ sink strength in SG. Gene profiling indicated that CT synthesis decreased as leaves expanded and PGs increased. A most striking finding was that the nitrogenous monoamine phenylethylamine accumulated only in leaves of SG plants. The potential negative impact of CT hyper-accumulation on foliar sink strength, as well as a mechanism for phenylethylamine involvement in CT polymerization in Populus are discussed. Starch accrual in source leaves and CT accrual in sink leaves of SG may both contribute to the maintenance of a slow-growth phenotype suited to survival in nutrient-poor habitats. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24336515</PMID><DateCompleted><Year>2015</Year><Month>08</Month><Day>24</Day></DateCompleted><DateRevised><Year>2017</Year><Month>11</Month><Day>16</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1758-4469</ISSN><JournalIssue CitedMedium="Internet"><Volume>34</Volume><Issue>11</Issue><PubDate><Year>2014</Year><Month>Nov</Month></PubDate></JournalIssue><Title>Tree physiology</Title><ISOAbbreviation>Tree Physiol</ISOAbbreviation></Journal><ArticleTitle>Condensed tannin biosynthesis and polymerization synergistically condition carbon use, defense, sink strength and growth in Populus.</ArticleTitle><Pagination><MedlinePgn>1240-51</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/treephys/tpt097</ELocationID><Abstract><AbstractText>The partitioning of carbon for growth, storage and constitutive chemical defenses is widely framed in terms of a hypothetical sink-source differential that varies with nutrient supply. According to this framework, phenolics accrual is passive and occurs in source leaves when normal sink growth is not sustainable due to a nutrient limitation. In assessing this framework, we present gene and metabolite evidence that condensed tannin (CT) accrual is strongest in sink leaves and sequesters carbon in a way that impinges upon foliar sink strength and upon phenolic glycoside (PG) accrual in Populus. The work was based on two Populus fremontii × angustifolia backcross lines with contrasting rates of CT accrual and growth, and equally large foliar PG reserves. However, foliar PG accrual was developmentally delayed in the high-CT, slow-growth line (SG), and nitrogen-limitation led to increased foliar PG accrual only in the low-CT, fast-growth line (FG). Metabolite profiling of developing leaves indicated comparatively carbon-limited amino acid metabolism, depletion of several Krebs cycle intermediates and reduced organ sink strength in SG. Gene profiling indicated that CT synthesis decreased as leaves expanded and PGs increased. A most striking finding was that the nitrogenous monoamine phenylethylamine accumulated only in leaves of SG plants. The potential negative impact of CT hyper-accumulation on foliar sink strength, as well as a mechanism for phenylethylamine involvement in CT polymerization in Populus are discussed. Starch accrual in source leaves and CT accrual in sink leaves of SG may both contribute to the maintenance of a slow-growth phenotype suited to survival in nutrient-poor habitats. </AbstractText><CopyrightInformation>© The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Harding</LastName><ForeName>Scott A</ForeName><Initials>SA</Initials><AffiliationInfo><Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA sharding@uga.edu cjtsai@uga.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xue</LastName><ForeName>Liang-Jiao</ForeName><Initials>LJ</Initials><AffiliationInfo><Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Lei</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA Present address: Unit of Computational Medicine, Department of Medicine, Karolinska Institute, Stockholm 17176, Sweden.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nyamdari</LastName><ForeName>Batbayar</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lindroth</LastName><ForeName>Richard L</ForeName><Initials>RL</Initials><AffiliationInfo><Affiliation>Department of Entomology, University of Wisconsin, Madison, WI 53706, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sykes</LastName><ForeName>Robert</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Davis</LastName><ForeName>Mark F</ForeName><Initials>MF</Initials><AffiliationInfo><Affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tsai</LastName><ForeName>Chung-Jui</ForeName><Initials>CJ</Initials><AffiliationInfo><Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA sharding@uga.edu cjtsai@uga.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2013</Year><Month>12</Month><Day>10</Day></ArticleDate></Article><MedlineJournalInfo><Country>Canada</Country><MedlineTA>Tree Physiol</MedlineTA><NlmUniqueID>100955338</NlmUniqueID><ISSNLinking>0829-318X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005960">Glucosides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D006027">Glycosides</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010627">Phenethylamines</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010636">Phenols</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D044945">Proanthocyanidins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D020005">Propanols</NameOfSubstance></Chemical><Chemical><RegistryNumber>0F897O3O4M</RegistryNumber><NameOfSubstance UI="C439395">1-phenylpropanol</NameOfSubstance></Chemical><Chemical><RegistryNumber>7440-44-0</RegistryNumber><NameOfSubstance UI="D002244">Carbon</NameOfSubstance></Chemical><Chemical><RegistryNumber>N762921K75</RegistryNumber><NameOfSubstance UI="D009584">Nitrogen</NameOfSubstance></Chemical><Chemical><RegistryNumber>YI29948E0Q</RegistryNumber><NameOfSubstance UI="C113068">salicortin</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D002244" MajorTopicYN="N">Carbon</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D057965" MajorTopicYN="N">Carbon Sequestration</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002678" MajorTopicYN="N">Chimera</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005838" MajorTopicYN="N">Genotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005960" MajorTopicYN="N">Glucosides</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006027" MajorTopicYN="N">Glycosides</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055442" MajorTopicYN="N">Metabolome</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009584" 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MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D058105" MajorTopicYN="N">Polymerization</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D044945" MajorTopicYN="N">Proanthocyanidins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020005" MajorTopicYN="N">Propanols</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">MYB</Keyword><Keyword MajorTopicYN="N">flavonoid</Keyword><Keyword MajorTopicYN="N">glycolysis</Keyword><Keyword MajorTopicYN="N">phenylethylamine</Keyword><Keyword MajorTopicYN="N">phenylpropanoid</Keyword><Keyword MajorTopicYN="N">salicortin</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2013</Year><Month>12</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2013</Year><Month>12</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2015</Year><Month>8</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">24336515</ArticleId><ArticleId IdType="pii">tpt097</ArticleId><ArticleId IdType="doi">10.1093/treephys/tpt097</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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