Chemical inhibition of xylem cellular activity impedes the removal of drought-induced embolisms in poplar stems - new insights from micro-CT analysis.
Identifieur interne : 000516 ( Main/Exploration ); précédent : 000515; suivant : 000517Chemical inhibition of xylem cellular activity impedes the removal of drought-induced embolisms in poplar stems - new insights from micro-CT analysis.
Auteurs : Francesca Secchi [Italie] ; Chiara Pagliarani [Italie] ; Silvia Cavalletto [Italie] ; Francesco Petruzzellis [Italie] ; Giulia Tonel [Italie] ; Tadeja Savi [Autriche] ; Giuliana Tromba [Italie] ; Maria Margherita Obertino [Italie] ; Claudio Lovisolo [Italie] ; Andrea Nardini [Italie] ; Maciej A. Zwieniecki [États-Unis]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
In drought-stressed plants a coordinated cascade of chemical and transcriptional adjustments occurs at the same time as embolism formation. While these processes do not affect embolism formation during stress, they may prime stems for recovery during rehydration by modifying apoplast pH and increasing sugar concentration in the xylem sap. Here we show that in vivo treatments modifying apoplastic pH (stem infiltration with a pH buffer) or reducing stem metabolic activity (infiltration with sodium vanadate and sodium cyanide; plant exposure to carbon monoxide) can reduce sugar accumulation, thus disrupting or delaying the recovery process. Application of the vanadate treatment (NaVO3, an inhibitor of many ATPases) completely halted recovery from drought-induced embolism for up to 24 h after re-irrigation, while partial recovery was observed in vivo in control plants using X-ray microcomputed tomography. Our results suggest that stem hydraulic recovery in poplar is a biological, energy-dependent process that coincides with accumulation of sugars in the apoplast during stress. Recovery and damage are spatially coordinated, with embolism formation occurring from the inside out and refilling from the outside in. The outside-in pattern highlights the importance of xylem proximity to the sugars within the phloem to the embolism recovery process.
DOI: 10.1111/nph.16912
PubMed: 32890423
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10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Lovisolo, Claudio" sort="Lovisolo, Claudio" uniqKey="Lovisolo C" first="Claudio" last="Lovisolo">Claudio Lovisolo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Nardini, Andrea" sort="Nardini, Andrea" uniqKey="Nardini A" first="Andrea" last="Nardini">Andrea Nardini</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127, Italy.</nlm:affiliation><country 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Zwieniecki</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, CA, 95616, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, CA, 95616</wicri:regionArea><wicri:noRegion>95616</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32890423</idno><idno type="pmid">32890423</idno><idno type="doi">10.1111/nph.16912</idno><idno type="wicri:Area/Main/Corpus">000118</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000118</idno><idno type="wicri:Area/Main/Curation">000118</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000118</idno><idno 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Pagliarani</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Sustainable Plant Protection, National Research Council, Strada delle Cacce 73, Torino, 10135, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Institute for Sustainable Plant Protection, National Research Council, Strada delle Cacce 73, Torino, 10135</wicri:regionArea><wicri:noRegion>10135</wicri:noRegion></affiliation></author><author><name sortKey="Cavalletto, Silvia" sort="Cavalletto, Silvia" uniqKey="Cavalletto S" first="Silvia" last="Cavalletto">Silvia Cavalletto</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Petruzzellis, Francesco" sort="Petruzzellis, Francesco" uniqKey="Petruzzellis F" first="Francesco" last="Petruzzellis">Francesco Petruzzellis</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127</wicri:regionArea><wicri:noRegion>34127</wicri:noRegion></affiliation></author><author><name sortKey="Tonel, Giulia" sort="Tonel, Giulia" uniqKey="Tonel G" first="Giulia" last="Tonel">Giulia Tonel</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Savi, Tadeja" sort="Savi, Tadeja" uniqKey="Savi T" first="Tadeja" last="Savi">Tadeja Savi</name><affiliation wicri:level="3"><nlm:affiliation>Institute of Botany, Department of Integrative Biology and Biodiversity Research, BOKU, Gregor-Mendel-Straße 33, Vienna, 1180, Austria.</nlm:affiliation><country xml:lang="fr">Autriche</country><wicri:regionArea>Institute of Botany, Department of Integrative Biology and Biodiversity Research, BOKU, Gregor-Mendel-Straße 33, Vienna, 1180</wicri:regionArea><placeName><region type="land" nuts="2">Vienne (Autriche)</region><settlement type="city">Vienne (Autriche)</settlement></placeName></affiliation></author><author><name sortKey="Tromba, Giuliana" sort="Tromba, Giuliana" uniqKey="Tromba G" first="Giuliana" last="Tromba">Giuliana Tromba</name><affiliation wicri:level="1"><nlm:affiliation>Elettra-Sincrotrone Trieste, Area Science Park, Basovizza, Trieste, 34149, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Elettra-Sincrotrone Trieste, Area Science Park, Basovizza, Trieste, 34149</wicri:regionArea><wicri:noRegion>34149</wicri:noRegion></affiliation></author><author><name sortKey="Obertino, Maria Margherita" sort="Obertino, Maria Margherita" uniqKey="Obertino M" first="Maria Margherita" last="Obertino">Maria Margherita Obertino</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Lovisolo, Claudio" sort="Lovisolo, Claudio" uniqKey="Lovisolo C" first="Claudio" last="Lovisolo">Claudio Lovisolo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095</wicri:regionArea><wicri:noRegion>10095</wicri:noRegion></affiliation></author><author><name sortKey="Nardini, Andrea" sort="Nardini, Andrea" uniqKey="Nardini A" first="Andrea" last="Nardini">Andrea Nardini</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127</wicri:regionArea><wicri:noRegion>34127</wicri:noRegion></affiliation></author><author><name sortKey="Zwieniecki, Maciej A" sort="Zwieniecki, Maciej A" uniqKey="Zwieniecki M" first="Maciej A" last="Zwieniecki">Maciej A. Zwieniecki</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, CA, 95616, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, CA, 95616</wicri:regionArea><wicri:noRegion>95616</wicri:noRegion></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">In drought-stressed plants a coordinated cascade of chemical and transcriptional adjustments occurs at the same time as embolism formation. While these processes do not affect embolism formation during stress, they may prime stems for recovery during rehydration by modifying apoplast pH and increasing sugar concentration in the xylem sap. Here we show that in vivo treatments modifying apoplastic pH (stem infiltration with a pH buffer) or reducing stem metabolic activity (infiltration with sodium vanadate and sodium cyanide; plant exposure to carbon monoxide) can reduce sugar accumulation, thus disrupting or delaying the recovery process. Application of the vanadate treatment (NaVO<sub>3,</sub> an inhibitor of many ATPases) completely halted recovery from drought-induced embolism for up to 24 h after re-irrigation, while partial recovery was observed in vivo in control plants using X-ray microcomputed tomography. Our results suggest that stem hydraulic recovery in poplar is a biological, energy-dependent process that coincides with accumulation of sugars in the apoplast during stress. Recovery and damage are spatially coordinated, with embolism formation occurring from the inside out and refilling from the outside in. The outside-in pattern highlights the importance of xylem proximity to the sugars within the phloem to the embolism recovery process.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32890423</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Sep</Month><Day>05</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Chemical inhibition of xylem cellular activity impedes the removal of drought-induced embolisms in poplar stems - new insights from micro-CT analysis.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16912</ELocationID><Abstract><AbstractText>In drought-stressed plants a coordinated cascade of chemical and transcriptional adjustments occurs at the same time as embolism formation. While these processes do not affect embolism formation during stress, they may prime stems for recovery during rehydration by modifying apoplast pH and increasing sugar concentration in the xylem sap. Here we show that in vivo treatments modifying apoplastic pH (stem infiltration with a pH buffer) or reducing stem metabolic activity (infiltration with sodium vanadate and sodium cyanide; plant exposure to carbon monoxide) can reduce sugar accumulation, thus disrupting or delaying the recovery process. Application of the vanadate treatment (NaVO<sub>3,</sub> an inhibitor of many ATPases) completely halted recovery from drought-induced embolism for up to 24 h after re-irrigation, while partial recovery was observed in vivo in control plants using X-ray microcomputed tomography. Our results suggest that stem hydraulic recovery in poplar is a biological, energy-dependent process that coincides with accumulation of sugars in the apoplast during stress. Recovery and damage are spatially coordinated, with embolism formation occurring from the inside out and refilling from the outside in. The outside-in pattern highlights the importance of xylem proximity to the sugars within the phloem to the embolism recovery process.</AbstractText><CopyrightInformation>© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Secchi</LastName><ForeName>Francesca</ForeName><Initials>F</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3161-1643</Identifier><AffiliationInfo><Affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pagliarani</LastName><ForeName>Chiara</ForeName><Initials>C</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-4656-6192</Identifier><AffiliationInfo><Affiliation>Institute for Sustainable Plant Protection, National Research Council, Strada delle Cacce 73, Torino, 10135, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cavalletto</LastName><ForeName>Silvia</ForeName><Initials>S</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-6478-6936</Identifier><AffiliationInfo><Affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Petruzzellis</LastName><ForeName>Francesco</ForeName><Initials>F</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3635-8501</Identifier><AffiliationInfo><Affiliation>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tonel</LastName><ForeName>Giulia</ForeName><Initials>G</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-1194-4763</Identifier><AffiliationInfo><Affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Savi</LastName><ForeName>Tadeja</ForeName><Initials>T</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-7585-763X</Identifier><AffiliationInfo><Affiliation>Institute of Botany, Department of Integrative Biology and Biodiversity Research, BOKU, Gregor-Mendel-Straße 33, Vienna, 1180, Austria.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tromba</LastName><ForeName>Giuliana</ForeName><Initials>G</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-4576-6099</Identifier><AffiliationInfo><Affiliation>Elettra-Sincrotrone Trieste, Area Science Park, Basovizza, Trieste, 34149, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Obertino</LastName><ForeName>Maria Margherita</ForeName><Initials>MM</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-8781-8192</Identifier><AffiliationInfo><Affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lovisolo</LastName><ForeName>Claudio</ForeName><Initials>C</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8825-2904</Identifier><AffiliationInfo><Affiliation>Department of Agricultural, Forest and Food Sciences, University of Turin, Largo Paolo Braccini 2, Grugliasco, 10095, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nardini</LastName><ForeName>Andrea</ForeName><Initials>A</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5208-0087</Identifier><AffiliationInfo><Affiliation>Dipartimento di Scienze della Vita, University of Trieste, via Giorgieri 10, Trieste, 34127, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zwieniecki</LastName><ForeName>Maciej A</ForeName><Initials>MA</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-3774-4455</Identifier><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, CA, 95616, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>Ateneo CSP/2016 Project</GrantID><Agency>University of Turin</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>05</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus
</Keyword><Keyword MajorTopicYN="N">X-ray microcomputed tomography (micro-CT)</Keyword><Keyword MajorTopicYN="N">apoplastic pH</Keyword><Keyword MajorTopicYN="N">embolism</Keyword><Keyword MajorTopicYN="N">recovery</Keyword><Keyword MajorTopicYN="N">sugars</Keyword><Keyword MajorTopicYN="N">vanadate</Keyword><Keyword MajorTopicYN="N">xylem</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>07</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>9</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>9</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>9</Month><Day>5</Day><Hour>17</Hour><Minute>7</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32890423</ArticleId><ArticleId IdType="doi">10.1111/nph.16912</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Brodersen CR, Knipfer T, McElrone AJ. 2018. 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