Mitochondrial Defects Confer Tolerance against Cellulose Deficiency.
Identifieur interne : 001A17 ( PubMed/Corpus ); précédent : 001A16; suivant : 001A18Mitochondrial Defects Confer Tolerance against Cellulose Deficiency.
Auteurs : Zhubing Hu ; Rudy Vanderhaeghen ; Toon Cools ; Yan Wang ; Inge De Clercq ; Olivier Leroux ; Long Nguyen ; Katharina Belt ; A Harvey Millar ; Dominique Audenaert ; Pierre Hilson ; Ian D. Small ; Grégory Mouille ; Samantha Vernhettes ; Frank Van Breusegem ; James Whelan ; Herman Höfte ; Lieven De VeylderSource :
- The Plant cell [ 1532-298X ] ; 2016.
Abstract
Because the plant cell wall provides the first line of defence against biotic and abiotic assaults, its functional integrity needs to be maintained under stress conditions. Through a phenotype-based compound screening approach we identified a novel cellulose synthase inhibitor, designated C17. C17 administration depletes cellulose synthase complexes (CSCs) from the plasma membrane in Arabidopsis thaliana, resulting in anisotropic cell elongation and a weak cell wall. Surprisingly, in addition to mutations in CELLULOSE SYNTHASE 1 (CESA1) and CELLULOSE SYNTHASE 3 (CESA3), a forward genetic screen identified two independent defective genes encoding pentatricopeptide repeat (PPR)-like proteins [CELL WALL MAINTAINER 1 (CWM1) and 2 (CWM2)] as conferring tolerance to C17. Functional analysis revealed that mutations in these PPR proteins resulted in defective cytochrome c maturation and activation of mitochondrial retrograde signalling, as evidenced by the induction of an alternative oxidase. These mitochondrial perturbations increased tolerance to cell wall damage induced by cellulose deficiency. Likewise, administration of antimycin A, an inhibitor of mitochondrial complex III, and constitutive activation of mitochondrial retrograde signalling resulted in tolerance towards C17. The C17 tolerance of cwm2 was partially lost upon depletion of the mitochondrial retrograde regulator ANAC017, demonstrating that ANAC017 links mitochondrial dysfunction with the cell wall. In view of mitochondria being a major target of a variety of stresses, our data indicate that plant cells might modulate mitochondrial activity to maintain a functional cell wall when subjected to stresses.
DOI: 10.1105/tpc.16.00540
PubMed: 27543091
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Mitochondrial Defects Confer Tolerance against Cellulose Deficiency.</title><author><name sortKey="Hu, Zhubing" sort="Hu, Zhubing" uniqKey="Hu Z" first="Zhubing" last="Hu">Zhubing Hu</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Vanderhaeghen, Rudy" sort="Vanderhaeghen, Rudy" uniqKey="Vanderhaeghen R" first="Rudy" last="Vanderhaeghen">Rudy Vanderhaeghen</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Cools, Toon" sort="Cools, Toon" uniqKey="Cools T" first="Toon" last="Cools">Toon Cools</name><affiliation><nlm:affiliation>VIB CITY: Ghent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name><affiliation><nlm:affiliation>La Trobe University CITY: Melbourne STATE: Victoria Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="De Clercq, Inge" sort="De Clercq, Inge" uniqKey="De Clercq I" first="Inge" last="De Clercq">Inge De Clercq</name><affiliation><nlm:affiliation>VIB - Ghent university CITY: Gent POSTAL_CODE: 9052 Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Leroux, Olivier" sort="Leroux, Olivier" uniqKey="Leroux O" first="Olivier" last="Leroux">Olivier Leroux</name><affiliation><nlm:affiliation>Ghent University CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Nguyen, Long" sort="Nguyen, Long" uniqKey="Nguyen L" first="Long" last="Nguyen">Long Nguyen</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Belt, Katharina" sort="Belt, Katharina" uniqKey="Belt K" first="Katharina" last="Belt">Katharina Belt</name><affiliation><nlm:affiliation>The University of Western Australia CITY: Perth STATE: WA Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Millar, A Harvey" sort="Millar, A Harvey" uniqKey="Millar A" first="A Harvey" last="Millar">A Harvey Millar</name><affiliation><nlm:affiliation>The University of Western Australia CITY: Perth STATE: WA POSTAL_CODE: 6009 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Audenaert, Dominique" sort="Audenaert, Dominique" uniqKey="Audenaert D" first="Dominique" last="Audenaert">Dominique Audenaert</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Hilson, Pierre" sort="Hilson, Pierre" uniqKey="Hilson P" first="Pierre" last="Hilson">Pierre Hilson</name><affiliation><nlm:affiliation>Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech CITY: Versailles POSTAL_CODE: 78026 France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Small, Ian D" sort="Small, Ian D" uniqKey="Small I" first="Ian D" last="Small">Ian D. Small</name><affiliation><nlm:affiliation>University of Western Australia CITY: Crawley STATE: WA POSTAL_CODE: 6009 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Mouille, Gregory" sort="Mouille, Gregory" uniqKey="Mouille G" first="Grégory" last="Mouille">Grégory Mouille</name><affiliation><nlm:affiliation>INRA CITY: Versailles France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Vernhettes, Samantha" sort="Vernhettes, Samantha" uniqKey="Vernhettes S" first="Samantha" last="Vernhettes">Samantha Vernhettes</name><affiliation><nlm:affiliation>INRA INRA-Laboratoire de Biologie Cellulaire, Route de Saint Cyr CITY: Versailles POSTAL_CODE: 78026 France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Van Breusegem, Frank" sort="Van Breusegem, Frank" uniqKey="Van Breusegem F" first="Frank" last="Van Breusegem">Frank Van Breusegem</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Whelan, James" sort="Whelan, James" uniqKey="Whelan J" first="James" last="Whelan">James Whelan</name><affiliation><nlm:affiliation>La Trobe University CITY: Bundoora STATE: Vi POSTAL_CODE: 3086 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Hofte, Herman" sort="Hofte, Herman" uniqKey="Hofte H" first="Herman" last="Höfte">Herman Höfte</name><affiliation><nlm:affiliation>INRA CITY: Versailles France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="De Veylder, Lieven" sort="De Veylder, Lieven" uniqKey="De Veylder L" first="Lieven" last="De Veylder">Lieven De Veylder</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent POSTAL_CODE: 9000 Belgium [BE] livey@psb.vib-ugent.be.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2016">2016</date><idno type="RBID">pubmed:27543091</idno><idno type="pmid">27543091</idno><idno type="doi">10.1105/tpc.16.00540</idno><idno type="wicri:Area/PubMed/Corpus">001A17</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">001A17</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Mitochondrial Defects Confer Tolerance against Cellulose Deficiency.</title><author><name sortKey="Hu, Zhubing" sort="Hu, Zhubing" uniqKey="Hu Z" first="Zhubing" last="Hu">Zhubing Hu</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Vanderhaeghen, Rudy" sort="Vanderhaeghen, Rudy" uniqKey="Vanderhaeghen R" first="Rudy" last="Vanderhaeghen">Rudy Vanderhaeghen</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Cools, Toon" sort="Cools, Toon" uniqKey="Cools T" first="Toon" last="Cools">Toon Cools</name><affiliation><nlm:affiliation>VIB CITY: Ghent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name><affiliation><nlm:affiliation>La Trobe University CITY: Melbourne STATE: Victoria Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="De Clercq, Inge" sort="De Clercq, Inge" uniqKey="De Clercq I" first="Inge" last="De Clercq">Inge De Clercq</name><affiliation><nlm:affiliation>VIB - Ghent university CITY: Gent POSTAL_CODE: 9052 Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Leroux, Olivier" sort="Leroux, Olivier" uniqKey="Leroux O" first="Olivier" last="Leroux">Olivier Leroux</name><affiliation><nlm:affiliation>Ghent University CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Nguyen, Long" sort="Nguyen, Long" uniqKey="Nguyen L" first="Long" last="Nguyen">Long Nguyen</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Belt, Katharina" sort="Belt, Katharina" uniqKey="Belt K" first="Katharina" last="Belt">Katharina Belt</name><affiliation><nlm:affiliation>The University of Western Australia CITY: Perth STATE: WA Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Millar, A Harvey" sort="Millar, A Harvey" uniqKey="Millar A" first="A Harvey" last="Millar">A Harvey Millar</name><affiliation><nlm:affiliation>The University of Western Australia CITY: Perth STATE: WA POSTAL_CODE: 6009 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Audenaert, Dominique" sort="Audenaert, Dominique" uniqKey="Audenaert D" first="Dominique" last="Audenaert">Dominique Audenaert</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Hilson, Pierre" sort="Hilson, Pierre" uniqKey="Hilson P" first="Pierre" last="Hilson">Pierre Hilson</name><affiliation><nlm:affiliation>Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech CITY: Versailles POSTAL_CODE: 78026 France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Small, Ian D" sort="Small, Ian D" uniqKey="Small I" first="Ian D" last="Small">Ian D. Small</name><affiliation><nlm:affiliation>University of Western Australia CITY: Crawley STATE: WA POSTAL_CODE: 6009 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Mouille, Gregory" sort="Mouille, Gregory" uniqKey="Mouille G" first="Grégory" last="Mouille">Grégory Mouille</name><affiliation><nlm:affiliation>INRA CITY: Versailles France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Vernhettes, Samantha" sort="Vernhettes, Samantha" uniqKey="Vernhettes S" first="Samantha" last="Vernhettes">Samantha Vernhettes</name><affiliation><nlm:affiliation>INRA INRA-Laboratoire de Biologie Cellulaire, Route de Saint Cyr CITY: Versailles POSTAL_CODE: 78026 France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="Van Breusegem, Frank" sort="Van Breusegem, Frank" uniqKey="Van Breusegem F" first="Frank" last="Van Breusegem">Frank Van Breusegem</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</nlm:affiliation></affiliation></author><author><name sortKey="Whelan, James" sort="Whelan, James" uniqKey="Whelan J" first="James" last="Whelan">James Whelan</name><affiliation><nlm:affiliation>La Trobe University CITY: Bundoora STATE: Vi POSTAL_CODE: 3086 Australia [AU].</nlm:affiliation></affiliation></author><author><name sortKey="Hofte, Herman" sort="Hofte, Herman" uniqKey="Hofte H" first="Herman" last="Höfte">Herman Höfte</name><affiliation><nlm:affiliation>INRA CITY: Versailles France [FR].</nlm:affiliation></affiliation></author><author><name sortKey="De Veylder, Lieven" sort="De Veylder, Lieven" uniqKey="De Veylder L" first="Lieven" last="De Veylder">Lieven De Veylder</name><affiliation><nlm:affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent POSTAL_CODE: 9000 Belgium [BE] livey@psb.vib-ugent.be.</nlm:affiliation></affiliation></author></analytic><series><title level="j">The Plant cell</title><idno type="eISSN">1532-298X</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Because the plant cell wall provides the first line of defence against biotic and abiotic assaults, its functional integrity needs to be maintained under stress conditions. Through a phenotype-based compound screening approach we identified a novel cellulose synthase inhibitor, designated C17. C17 administration depletes cellulose synthase complexes (CSCs) from the plasma membrane in Arabidopsis thaliana, resulting in anisotropic cell elongation and a weak cell wall. Surprisingly, in addition to mutations in CELLULOSE SYNTHASE 1 (CESA1) and CELLULOSE SYNTHASE 3 (CESA3), a forward genetic screen identified two independent defective genes encoding pentatricopeptide repeat (PPR)-like proteins [CELL WALL MAINTAINER 1 (CWM1) and 2 (CWM2)] as conferring tolerance to C17. Functional analysis revealed that mutations in these PPR proteins resulted in defective cytochrome c maturation and activation of mitochondrial retrograde signalling, as evidenced by the induction of an alternative oxidase. These mitochondrial perturbations increased tolerance to cell wall damage induced by cellulose deficiency. Likewise, administration of antimycin A, an inhibitor of mitochondrial complex III, and constitutive activation of mitochondrial retrograde signalling resulted in tolerance towards C17. The C17 tolerance of cwm2 was partially lost upon depletion of the mitochondrial retrograde regulator ANAC017, demonstrating that ANAC017 links mitochondrial dysfunction with the cell wall. In view of mitochondria being a major target of a variety of stresses, our data indicate that plant cells might modulate mitochondrial activity to maintain a functional cell wall when subjected to stresses.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">27543091</PMID><DateCreated><Year>2016</Year><Month>08</Month><Day>20</Day></DateCreated><DateRevised><Year>2017</Year><Month>09</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1532-298X</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2016</Year><Month>Aug</Month><Day>19</Day></PubDate></JournalIssue><Title>The Plant cell</Title><ISOAbbreviation>Plant Cell</ISOAbbreviation></Journal><ArticleTitle>Mitochondrial Defects Confer Tolerance against Cellulose Deficiency.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">tpc.00540.2016</ELocationID><Abstract><AbstractText>Because the plant cell wall provides the first line of defence against biotic and abiotic assaults, its functional integrity needs to be maintained under stress conditions. Through a phenotype-based compound screening approach we identified a novel cellulose synthase inhibitor, designated C17. C17 administration depletes cellulose synthase complexes (CSCs) from the plasma membrane in Arabidopsis thaliana, resulting in anisotropic cell elongation and a weak cell wall. Surprisingly, in addition to mutations in CELLULOSE SYNTHASE 1 (CESA1) and CELLULOSE SYNTHASE 3 (CESA3), a forward genetic screen identified two independent defective genes encoding pentatricopeptide repeat (PPR)-like proteins [CELL WALL MAINTAINER 1 (CWM1) and 2 (CWM2)] as conferring tolerance to C17. Functional analysis revealed that mutations in these PPR proteins resulted in defective cytochrome c maturation and activation of mitochondrial retrograde signalling, as evidenced by the induction of an alternative oxidase. These mitochondrial perturbations increased tolerance to cell wall damage induced by cellulose deficiency. Likewise, administration of antimycin A, an inhibitor of mitochondrial complex III, and constitutive activation of mitochondrial retrograde signalling resulted in tolerance towards C17. The C17 tolerance of cwm2 was partially lost upon depletion of the mitochondrial retrograde regulator ANAC017, demonstrating that ANAC017 links mitochondrial dysfunction with the cell wall. In view of mitochondria being a major target of a variety of stresses, our data indicate that plant cells might modulate mitochondrial activity to maintain a functional cell wall when subjected to stresses.</AbstractText><CopyrightInformation>© 2016 American Society of Plant Biologists. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Hu</LastName><ForeName>Zhubing</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vanderhaeghen</LastName><ForeName>Rudy</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cools</LastName><ForeName>Toon</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>VIB CITY: Ghent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>La Trobe University CITY: Melbourne STATE: Victoria Australia [AU].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>De Clercq</LastName><ForeName>Inge</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>VIB - Ghent university CITY: Gent POSTAL_CODE: 9052 Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Leroux</LastName><ForeName>Olivier</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Ghent University CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nguyen</LastName><ForeName>Long</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Belt</LastName><ForeName>Katharina</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>The University of Western Australia CITY: Perth STATE: WA Australia [AU].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Millar</LastName><ForeName>A Harvey</ForeName><Initials>AH</Initials><AffiliationInfo><Affiliation>The University of Western Australia CITY: Perth STATE: WA POSTAL_CODE: 6009 Australia [AU].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Audenaert</LastName><ForeName>Dominique</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hilson</LastName><ForeName>Pierre</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech CITY: Versailles POSTAL_CODE: 78026 France [FR].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Small</LastName><ForeName>Ian D</ForeName><Initials>ID</Initials><AffiliationInfo><Affiliation>University of Western Australia CITY: Crawley STATE: WA POSTAL_CODE: 6009 Australia [AU].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mouille</LastName><ForeName>Grégory</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>INRA CITY: Versailles France [FR].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vernhettes</LastName><ForeName>Samantha</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>INRA INRA-Laboratoire de Biologie Cellulaire, Route de Saint Cyr CITY: Versailles POSTAL_CODE: 78026 France [FR].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Van Breusegem</LastName><ForeName>Frank</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent Belgium [BE].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Whelan</LastName><ForeName>James</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>La Trobe University CITY: Bundoora STATE: Vi POSTAL_CODE: 3086 Australia [AU].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Höfte</LastName><ForeName>Herman</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>INRA CITY: Versailles France [FR].</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>De Veylder</LastName><ForeName>Lieven</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Ghent University - VIB - Dept. of Plant Systems Biology CITY: Gent POSTAL_CODE: 9000 Belgium [BE] livey@psb.vib-ugent.be.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>08</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Plant 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