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Priming xylem for stress recovery depends on coordinated activity of sugar metabolic pathways and changes in xylem sap pH.

Identifieur interne : 000756 ( Main/Exploration ); précédent : 000755; suivant : 000757

Priming xylem for stress recovery depends on coordinated activity of sugar metabolic pathways and changes in xylem sap pH.

Auteurs : Chiara Pagliarani [Italie] ; Valentino Casolo [Italie] ; Maryam Ashofteh Beiragi [Italie] ; Silvia Cavalletto [Italie] ; Ilenia Siciliano [Italie] ; Andrea Schubert [Italie] ; Maria Lodovica Gullino [Italie] ; Maciej A. Zwieniecki [États-Unis] ; Francesca Secchi [Italie]

Source :

RBID : pubmed:30756400

Descripteurs français

English descriptors

Abstract

Some plant species are capable of significant reduction of xylem embolism during recovery from drought despite stem water potential remains negative. However, the functional biology underlying this process is elusive. We subjected poplar trees to drought stress followed by a period of recovery. Water potential, hydraulic conductivity, gas exchange, xylem sap pH, and carbohydrate content in sap and woody stems were monitored in combination with an analysis of carbohydrate metabolism, enzyme activity, and expression of genes involved in sugar metabolic and transport pathways. Drought resulted in an alteration of differential partitioning between starch and soluble sugars. Upon stress, an increase in the starch degradation rate and the overexpression of sugar symporter genes promoted the efflux of disaccharides (mostly maltose and sucrose) to the apoplast. In turn, the efflux activity of the sugar-proton cotransporters caused a drop in xylem pH. The newly acidic environment induced the activity of apoplastic invertases leading to the accumulation of monosaccharides in the apoplast, thus providing the main osmoticum necessary for recovery. During drought and recovery, a complex network of coordinated molecular and biochemical signals was activated at the interface between xylem and parenchyma cells that appeared to prime the xylem for hydraulic recovery.

DOI: 10.1111/pce.13533
PubMed: 30756400


Affiliations:


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Le document en format XML

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<term>Carbohydrate Metabolism (physiology)</term>
<term>Carbohydrates (MeSH)</term>
<term>Droughts (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Glucose (analysis)</term>
<term>Hydrogen-Ion Concentration (MeSH)</term>
<term>Metabolic Networks and Pathways (genetics)</term>
<term>Metabolic Networks and Pathways (physiology)</term>
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<term>Populus (metabolism)</term>
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<term>Xylem (metabolism)</term>
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<term>Amidon (analyse)</term>
<term>Bois (composition chimique)</term>
<term>Concentration en ions d'hydrogène (MeSH)</term>
<term>Eau (métabolisme)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Glucides (MeSH)</term>
<term>Glucose (analyse)</term>
<term>Métabolisme glucidique (génétique)</term>
<term>Métabolisme glucidique (physiologie)</term>
<term>Oses (métabolisme)</term>
<term>Osmose (MeSH)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Stress physiologique (MeSH)</term>
<term>Sécheresses (MeSH)</term>
<term>Tiges de plante (métabolisme)</term>
<term>Voies et réseaux métaboliques (génétique)</term>
<term>Voies et réseaux métaboliques (physiologie)</term>
<term>Xylème (composition chimique)</term>
<term>Xylème (métabolisme)</term>
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<term>Water</term>
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<term>Amidon</term>
<term>Glucose</term>
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<term>Wood</term>
<term>Xylem</term>
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<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Bois</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Carbohydrate Metabolism</term>
<term>Metabolic Networks and Pathways</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Métabolisme glucidique</term>
<term>Populus</term>
<term>Voies et réseaux métaboliques</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Plant Leaves</term>
<term>Plant Stems</term>
<term>Populus</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Eau</term>
<term>Feuilles de plante</term>
<term>Oses</term>
<term>Populus</term>
<term>Tiges de plante</term>
<term>Xylème</term>
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<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Métabolisme glucidique</term>
<term>Voies et réseaux métaboliques</term>
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<term>Hydrogen-Ion Concentration</term>
<term>Osmosis</term>
<term>Stress, Physiological</term>
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<term>Concentration en ions d'hydrogène</term>
<term>Glucides</term>
<term>Osmose</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Stress physiologique</term>
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<div type="abstract" xml:lang="en">Some plant species are capable of significant reduction of xylem embolism during recovery from drought despite stem water potential remains negative. However, the functional biology underlying this process is elusive. We subjected poplar trees to drought stress followed by a period of recovery. Water potential, hydraulic conductivity, gas exchange, xylem sap pH, and carbohydrate content in sap and woody stems were monitored in combination with an analysis of carbohydrate metabolism, enzyme activity, and expression of genes involved in sugar metabolic and transport pathways. Drought resulted in an alteration of differential partitioning between starch and soluble sugars. Upon stress, an increase in the starch degradation rate and the overexpression of sugar symporter genes promoted the efflux of disaccharides (mostly maltose and sucrose) to the apoplast. In turn, the efflux activity of the sugar-proton cotransporters caused a drop in xylem pH. The newly acidic environment induced the activity of apoplastic invertases leading to the accumulation of monosaccharides in the apoplast, thus providing the main osmoticum necessary for recovery. During drought and recovery, a complex network of coordinated molecular and biochemical signals was activated at the interface between xylem and parenchyma cells that appeared to prime the xylem for hydraulic recovery.</div>
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<AbstractText>Some plant species are capable of significant reduction of xylem embolism during recovery from drought despite stem water potential remains negative. However, the functional biology underlying this process is elusive. We subjected poplar trees to drought stress followed by a period of recovery. Water potential, hydraulic conductivity, gas exchange, xylem sap pH, and carbohydrate content in sap and woody stems were monitored in combination with an analysis of carbohydrate metabolism, enzyme activity, and expression of genes involved in sugar metabolic and transport pathways. Drought resulted in an alteration of differential partitioning between starch and soluble sugars. Upon stress, an increase in the starch degradation rate and the overexpression of sugar symporter genes promoted the efflux of disaccharides (mostly maltose and sucrose) to the apoplast. In turn, the efflux activity of the sugar-proton cotransporters caused a drop in xylem pH. The newly acidic environment induced the activity of apoplastic invertases leading to the accumulation of monosaccharides in the apoplast, thus providing the main osmoticum necessary for recovery. During drought and recovery, a complex network of coordinated molecular and biochemical signals was activated at the interface between xylem and parenchyma cells that appeared to prime the xylem for hydraulic recovery.</AbstractText>
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<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute for Sustainable Plant Protection, National Research Council, Turin, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Casolo</LastName>
<ForeName>Valentino</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Food, Environmental and Animal Sciences, University of Udine, Udine, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ashofteh Beiragi</LastName>
<ForeName>Maryam</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Cavalletto</LastName>
<ForeName>Silvia</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Siciliano</LastName>
<ForeName>Ilenia</ForeName>
<Initials>I</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>AGROINNOVA, Centre for Innovation in the Agro-Environmental Sector, University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schubert</LastName>
<ForeName>Andrea</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gullino</LastName>
<ForeName>Maria Lodovica</ForeName>
<Initials>ML</Initials>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>AGROINNOVA, Centre for Innovation in the Agro-Environmental Sector, University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zwieniecki</LastName>
<ForeName>Maciej A</ForeName>
<Initials>MA</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Sciences, UC Davis, Davis, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Secchi</LastName>
<ForeName>Francesca</ForeName>
<Initials>F</Initials>
<Identifier Source="ORCID">0000-0002-3161-1643</Identifier>
<AffiliationInfo>
<Affiliation>Department of Agriculture, Forest and Food Sciences (DISAFA), University of Turin, Grugliasco, Italy.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
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<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>03</Month>
<Day>08</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Plant Cell Environ</MedlineTA>
<NlmUniqueID>9309004</NlmUniqueID>
<ISSNLinking>0140-7791</ISSNLinking>
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<NameOfSubstance UI="D009005">Monosaccharides</NameOfSubstance>
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<NameOfSubstance UI="D014867">Water</NameOfSubstance>
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<Chemical>
<RegistryNumber>9005-25-8</RegistryNumber>
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<RegistryNumber>IY9XDZ35W2</RegistryNumber>
<NameOfSubstance UI="D005947">Glucose</NameOfSubstance>
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</MeshHeading>
<MeshHeading>
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</MeshHeading>
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<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005947" MajorTopicYN="N">Glucose</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D006863" MajorTopicYN="N">Hydrogen-Ion Concentration</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D018547" MajorTopicYN="N">Plant Stems</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013213" MajorTopicYN="N">Starch</DescriptorName>
<QualifierName UI="Q000032" MajorTopicYN="N">analysis</QualifierName>
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<MeshHeading>
<DescriptorName UI="D013312" MajorTopicYN="Y">Stress, Physiological</DescriptorName>
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<MeshHeading>
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<MeshHeading>
<DescriptorName UI="D014934" MajorTopicYN="N">Wood</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D052584" MajorTopicYN="N">Xylem</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Populus</Keyword>
<Keyword MajorTopicYN="Y">apoplastic pH</Keyword>
<Keyword MajorTopicYN="Y">disaccharides</Keyword>
<Keyword MajorTopicYN="Y">drought</Keyword>
<Keyword MajorTopicYN="Y">gene expression</Keyword>
<Keyword MajorTopicYN="Y">monosaccharides</Keyword>
<Keyword MajorTopicYN="Y">recovery</Keyword>
<Keyword MajorTopicYN="Y">starch</Keyword>
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</MedlineCitation>
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<Year>2018</Year>
<Month>08</Month>
<Day>03</Day>
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<PubMedPubDate PubStatus="revised">
<Year>2019</Year>
<Month>01</Month>
<Day>29</Day>
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<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>01</Month>
<Day>30</Day>
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<Month>2</Month>
<Day>14</Day>
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<Month>4</Month>
<Day>28</Day>
<Hour>6</Hour>
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<PubMedPubDate PubStatus="entrez">
<Year>2019</Year>
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</History>
<PublicationStatus>ppublish</PublicationStatus>
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<ArticleId IdType="pubmed">30756400</ArticleId>
<ArticleId IdType="doi">10.1111/pce.13533</ArticleId>
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</pubmed>
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<list>
<country>
<li>Italie</li>
<li>États-Unis</li>
</country>
<region>
<li>Californie</li>
<li>Piémont</li>
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<settlement>
<li>Turin</li>
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<name sortKey="Pagliarani, Chiara" sort="Pagliarani, Chiara" uniqKey="Pagliarani C" first="Chiara" last="Pagliarani">Chiara Pagliarani</name>
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<name sortKey="Ashofteh Beiragi, Maryam" sort="Ashofteh Beiragi, Maryam" uniqKey="Ashofteh Beiragi M" first="Maryam" last="Ashofteh Beiragi">Maryam Ashofteh Beiragi</name>
<name sortKey="Casolo, Valentino" sort="Casolo, Valentino" uniqKey="Casolo V" first="Valentino" last="Casolo">Valentino Casolo</name>
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<name sortKey="Pagliarani, Chiara" sort="Pagliarani, Chiara" uniqKey="Pagliarani C" first="Chiara" last="Pagliarani">Chiara Pagliarani</name>
<name sortKey="Schubert, Andrea" sort="Schubert, Andrea" uniqKey="Schubert A" first="Andrea" last="Schubert">Andrea Schubert</name>
<name sortKey="Secchi, Francesca" sort="Secchi, Francesca" uniqKey="Secchi F" first="Francesca" last="Secchi">Francesca Secchi</name>
<name sortKey="Siciliano, Ilenia" sort="Siciliano, Ilenia" uniqKey="Siciliano I" first="Ilenia" last="Siciliano">Ilenia Siciliano</name>
<name sortKey="Siciliano, Ilenia" sort="Siciliano, Ilenia" uniqKey="Siciliano I" first="Ilenia" last="Siciliano">Ilenia Siciliano</name>
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<name sortKey="Zwieniecki, Maciej A" sort="Zwieniecki, Maciej A" uniqKey="Zwieniecki M" first="Maciej A" last="Zwieniecki">Maciej A. Zwieniecki</name>
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