Overexpression of PtHMGR enhances drought and salt tolerance of poplar.
Identifieur interne : 000236 ( Main/Exploration ); précédent : 000235; suivant : 000237Overexpression of PtHMGR enhances drought and salt tolerance of poplar.
Auteurs : Hui Wei [République populaire de Chine] ; Ali Movahedi [République populaire de Chine] ; Chen Xu [République populaire de Chine] ; Weibo Sun [République populaire de Chine] ; Lingling Li [République populaire de Chine] ; Pu Wang [République populaire de Chine] ; Dawei Li [République populaire de Chine] ; Qiang Zhuge [République populaire de Chine]Source :
- Annals of botany [ 1095-8290 ] ; 2020.
Descripteurs français
- KwdFr :
- MESH :
English descriptors
- KwdEn :
- MESH :
- chemical : Plant Proteins.
- genetics : Populus.
- Droughts, Gene Expression Regulation, Plant, Plants, Genetically Modified, Salt Tolerance, Stress, Physiological.
Abstract
BACKGROUND AND AIMS
Soil salinization and aridification are swiftly engulfing the limited land resources on which humans depend, restricting agricultural production. Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) is important in the biosynthesis of terpenoids, which are involved in plant growth, development and responses to environmental stresses. This study aimed to provide guidance for producing salt- and drought-resistant poplar.
METHODS
A protein expression system was used to obtain PtHMGR protein, and high-performance liquid chromatography was used to detect the activity of PtHMGR protein in vitro. In addition, a simplified version of the leaf infection method was used for transformation of 'Nanlin895' poplar (Populus×euramericana). qRT-PCR was used to identify expression levels of genes.
KEY RESULTS
PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate. Overexpression of PtHMGR in Populus × euramericana 'Nanlin895' improved drought and salinity tolerance. In the presence of NaCl and PEG6000, the rates of rooting and survival of PtHMGR-overexpressing poplars were higher than those of wild-type poplars. The transgenic lines also exhibited higher proline content and peroxidase and superoxide dismutase activities, and a lower malondialdehyde level under osmotic stress. In addition, the expression of genes related to reactive oxygen species (ROS) scavenging and formation was altered by osmotic stress. Moreover, the effect of osmotic stress on transcript levels of stress-related genes differed between the transgenic and wild-type poplars.
CONCLUSION
PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate in vitro. Overexpression of PtHMGR promoted root development, increased the expression of ROS scavenging-related genes, decreased the expression of ROS formation-related genes, and increased the activity of antioxidant enzymes in transgenic poplars, enhancing their tolerance of osmotic stress. In addition, overexpression of PtHMGR increased expression of the stress-related genes KIN1, COR15 and AAO3 and decreased that of ABI, MYB, MYC2 and RD22, enhancing the stress resistance of poplar.
DOI: 10.1093/aob/mcz158
PubMed: 31574532
PubMed Central: PMC7182595
Affiliations:
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Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Pu" sort="Wang, Pu" uniqKey="Wang P" first="Pu" last="Wang">Pu Wang</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Li, Dawei" sort="Li, Dawei" uniqKey="Li D" first="Dawei" last="Li">Dawei Li</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhuge, Qiang" sort="Zhuge, Qiang" uniqKey="Zhuge Q" first="Qiang" last="Zhuge">Qiang Zhuge</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno 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Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Movahedi, Ali" sort="Movahedi, Ali" uniqKey="Movahedi A" first="Ali" last="Movahedi">Ali Movahedi</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Xu, Chen" sort="Xu, Chen" uniqKey="Xu C" first="Chen" last="Xu">Chen Xu</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Jiangsu Provincial Key Construction Laboratory of Special Biomass Resource Utilization, Nanjing Xiaozhuang University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Jiangsu Provincial Key Construction Laboratory of Special Biomass Resource Utilization, Nanjing Xiaozhuang University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Sun, Weibo" sort="Sun, Weibo" uniqKey="Sun W" first="Weibo" last="Sun">Weibo Sun</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Li, Lingling" sort="Li, Lingling" uniqKey="Li L" first="Lingling" last="Li">Lingling Li</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Pu" sort="Wang, Pu" uniqKey="Wang P" first="Pu" last="Wang">Pu Wang</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Li, Dawei" sort="Li, Dawei" uniqKey="Li D" first="Dawei" last="Li">Dawei Li</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author><author><name sortKey="Zhuge, Qiang" sort="Zhuge, Qiang" uniqKey="Zhuge Q" first="Qiang" last="Zhuge">Qiang Zhuge</name><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author></analytic><series><title level="j">Annals of botany</title><idno type="eISSN">1095-8290</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Droughts (MeSH)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Plant Proteins (MeSH)</term><term>Plants, Genetically Modified (MeSH)</term><term>Populus (genetics)</term><term>Salt Tolerance (MeSH)</term><term>Stress, Physiological (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Populus (génétique)</term><term>Protéines végétales (MeSH)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Stress physiologique (MeSH)</term><term>Sécheresses (MeSH)</term><term>Tolérance au sel (MeSH)</term><term>Végétaux génétiquement modifiés (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" xml:lang="en"><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Populus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Droughts</term><term>Gene Expression Regulation, Plant</term><term>Plants, Genetically Modified</term><term>Salt Tolerance</term><term>Stress, Physiological</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Protéines végétales</term><term>Régulation de l'expression des gènes végétaux</term><term>Stress physiologique</term><term>Sécheresses</term><term>Tolérance au sel</term><term>Végétaux génétiquement modifiés</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>BACKGROUND AND AIMS</b></p><p>Soil salinization and aridification are swiftly engulfing the limited land resources on which humans depend, restricting agricultural production. Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) is important in the biosynthesis of terpenoids, which are involved in plant growth, development and responses to environmental stresses. This study aimed to provide guidance for producing salt- and drought-resistant poplar.</p></div><div type="abstract" xml:lang="en"><p><b>METHODS</b></p><p>A protein expression system was used to obtain PtHMGR protein, and high-performance liquid chromatography was used to detect the activity of PtHMGR protein in vitro. In addition, a simplified version of the leaf infection method was used for transformation of 'Nanlin895' poplar (Populus×euramericana). qRT-PCR was used to identify expression levels of genes.</p></div><div type="abstract" xml:lang="en"><p><b>KEY RESULTS</b></p><p>PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate. Overexpression of PtHMGR in Populus × euramericana 'Nanlin895' improved drought and salinity tolerance. In the presence of NaCl and PEG6000, the rates of rooting and survival of PtHMGR-overexpressing poplars were higher than those of wild-type poplars. The transgenic lines also exhibited higher proline content and peroxidase and superoxide dismutase activities, and a lower malondialdehyde level under osmotic stress. In addition, the expression of genes related to reactive oxygen species (ROS) scavenging and formation was altered by osmotic stress. Moreover, the effect of osmotic stress on transcript levels of stress-related genes differed between the transgenic and wild-type poplars.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSION</b></p><p>PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate in vitro. Overexpression of PtHMGR promoted root development, increased the expression of ROS scavenging-related genes, decreased the expression of ROS formation-related genes, and increased the activity of antioxidant enzymes in transgenic poplars, enhancing their tolerance of osmotic stress. In addition, overexpression of PtHMGR increased expression of the stress-related genes KIN1, COR15 and AAO3 and decreased that of ABI, MYB, MYC2 and RD22, enhancing the stress resistance of poplar.</p></div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Automated" Owner="NLM"><PMID Version="1">31574532</PMID><DateCompleted><Year>2020</Year><Month>07</Month><Day>13</Day></DateCompleted><DateRevised><Year>2020</Year><Month>07</Month><Day>13</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1095-8290</ISSN><JournalIssue CitedMedium="Internet"><Volume>125</Volume><Issue>5</Issue><PubDate><Year>2020</Year><Month>04</Month><Day>25</Day></PubDate></JournalIssue><Title>Annals of botany</Title><ISOAbbreviation>Ann Bot</ISOAbbreviation></Journal><ArticleTitle>Overexpression of PtHMGR enhances drought and salt tolerance of poplar.</ArticleTitle><Pagination><MedlinePgn>785-803</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/aob/mcz158</ELocationID><Abstract><AbstractText Label="BACKGROUND AND AIMS">Soil salinization and aridification are swiftly engulfing the limited land resources on which humans depend, restricting agricultural production. Hydroxy-3-methylglutaryl coenzyme A reductase (HMGR) is important in the biosynthesis of terpenoids, which are involved in plant growth, development and responses to environmental stresses. This study aimed to provide guidance for producing salt- and drought-resistant poplar.</AbstractText><AbstractText Label="METHODS">A protein expression system was used to obtain PtHMGR protein, and high-performance liquid chromatography was used to detect the activity of PtHMGR protein in vitro. In addition, a simplified version of the leaf infection method was used for transformation of 'Nanlin895' poplar (Populus×euramericana). qRT-PCR was used to identify expression levels of genes.</AbstractText><AbstractText Label="KEY RESULTS">PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate. Overexpression of PtHMGR in Populus × euramericana 'Nanlin895' improved drought and salinity tolerance. In the presence of NaCl and PEG6000, the rates of rooting and survival of PtHMGR-overexpressing poplars were higher than those of wild-type poplars. The transgenic lines also exhibited higher proline content and peroxidase and superoxide dismutase activities, and a lower malondialdehyde level under osmotic stress. In addition, the expression of genes related to reactive oxygen species (ROS) scavenging and formation was altered by osmotic stress. Moreover, the effect of osmotic stress on transcript levels of stress-related genes differed between the transgenic and wild-type poplars.</AbstractText><AbstractText Label="CONCLUSION">PtHMGR catalysed a reaction involving HMG-CoA and NADPH to form mevalonate in vitro. Overexpression of PtHMGR promoted root development, increased the expression of ROS scavenging-related genes, decreased the expression of ROS formation-related genes, and increased the activity of antioxidant enzymes in transgenic poplars, enhancing their tolerance of osmotic stress. In addition, overexpression of PtHMGR increased expression of the stress-related genes KIN1, COR15 and AAO3 and decreased that of ABI, MYB, MYC2 and RD22, enhancing the stress resistance of poplar.</AbstractText><CopyrightInformation>© The Author(s) 2019. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Hui</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Movahedi</LastName><ForeName>Ali</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Chen</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Jiangsu Provincial Key Construction Laboratory of Special Biomass Resource Utilization, Nanjing Xiaozhuang University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Weibo</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Lingling</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Pu</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Dawei</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhuge</LastName><ForeName>Qiang</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Key Laboratory of Forest Genetics & Biotechnology of Ministry of Education, Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Ann Bot</MedlineTA><NlmUniqueID>0372347</NlmUniqueID><ISSNLinking>0305-7364</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D055864" MajorTopicYN="N">Droughts</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055049" MajorTopicYN="Y">Salt Tolerance</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D013312" MajorTopicYN="N">Stress, Physiological</DescriptorName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">HMGR
</Keyword><Keyword MajorTopicYN="Y">Populus trichocarpa
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