DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana
Identifieur interne : 000217 ( Pmc/Checkpoint ); précédent : 000216; suivant : 000218DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana
Auteurs : Jun Zhang ; Jinshan Ella Lin ; Chinchu Harris ; Fernanda Campos Mastrotti Pereira [Brésil] ; Fan Wu ; Joshua J. Blakeslee ; Wendy Ann PeerSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
Although auxin oxidation has long been known to be the primary mechanism of auxin catabolism and
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DOI: 10.1073/pnas.1604769113
PubMed: 27651492
PubMed Central: 5047167
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in <italic>Arabidopsis thaliana</italic></title><author><name sortKey="Zhang, Jun" sort="Zhang, Jun" uniqKey="Zhang J" first="Jun" last="Zhang">Jun Zhang</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Lin, Jinshan Ella" sort="Lin, Jinshan Ella" uniqKey="Lin J" first="Jinshan Ella" last="Lin">Jinshan Ella Lin</name><affiliation><nlm:aff id="aff2">Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Ohio Agricultural Research and Development Center Metabolite Analysis Cluster, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation></author><author><name sortKey="Harris, Chinchu" sort="Harris, Chinchu" uniqKey="Harris C" first="Chinchu" last="Harris">Chinchu Harris</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Campos Mastrotti Pereira, Fernanda" sort="Campos Mastrotti Pereira, Fernanda" uniqKey="Campos Mastrotti Pereira F" first="Fernanda" last="Campos Mastrotti Pereira">Fernanda Campos Mastrotti Pereira</name><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5">Plant Protection and Animal Health, Forestry, Agronomy,<institution>Universidade Estadual de São Paulo</institution>, Sao Paulo,<country>Brazil</country></nlm:aff><country xml:lang="fr">Brésil</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wu, Fan" sort="Wu, Fan" uniqKey="Wu F" first="Fan" last="Wu">Fan Wu</name><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Blakeslee, Joshua J" sort="Blakeslee, Joshua J" uniqKey="Blakeslee J" first="Joshua J." last="Blakeslee">Joshua J. Blakeslee</name><affiliation><nlm:aff id="aff2">Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Ohio Agricultural Research and Development Center Metabolite Analysis Cluster, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation></author><author><name sortKey="Peer, Wendy Ann" sort="Peer, Wendy Ann" uniqKey="Peer W" first="Wendy Ann" last="Peer">Wendy Ann Peer</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27651492</idno><idno type="pmc">5047167</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5047167</idno><idno type="RBID">PMC:5047167</idno><idno type="doi">10.1073/pnas.1604769113</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000D42</idno><idno type="wicri:Area/Pmc/Curation">000D41</idno><idno type="wicri:Area/Pmc/Checkpoint">000217</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in <italic>Arabidopsis thaliana</italic></title><author><name sortKey="Zhang, Jun" sort="Zhang, Jun" uniqKey="Zhang J" first="Jun" last="Zhang">Jun Zhang</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Lin, Jinshan Ella" sort="Lin, Jinshan Ella" uniqKey="Lin J" first="Jinshan Ella" last="Lin">Jinshan Ella Lin</name><affiliation><nlm:aff id="aff2">Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Ohio Agricultural Research and Development Center Metabolite Analysis Cluster, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation></author><author><name sortKey="Harris, Chinchu" sort="Harris, Chinchu" uniqKey="Harris C" first="Chinchu" last="Harris">Chinchu Harris</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Campos Mastrotti Pereira, Fernanda" sort="Campos Mastrotti Pereira, Fernanda" uniqKey="Campos Mastrotti Pereira F" first="Fernanda" last="Campos Mastrotti Pereira">Fernanda Campos Mastrotti Pereira</name><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5">Plant Protection and Animal Health, Forestry, Agronomy,<institution>Universidade Estadual de São Paulo</institution>, Sao Paulo,<country>Brazil</country></nlm:aff><country xml:lang="fr">Brésil</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wu, Fan" sort="Wu, Fan" uniqKey="Wu F" first="Fan" last="Wu">Fan Wu</name><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author><author><name sortKey="Blakeslee, Joshua J" sort="Blakeslee, Joshua J" uniqKey="Blakeslee J" first="Joshua J." last="Blakeslee">Joshua J. Blakeslee</name><affiliation><nlm:aff id="aff2">Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Ohio Agricultural Research and Development Center Metabolite Analysis Cluster, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</nlm:aff></affiliation></author><author><name sortKey="Peer, Wendy Ann" sort="Peer, Wendy Ann" uniqKey="Peer W" first="Wendy Ann" last="Peer">Wendy Ann Peer</name><affiliation><nlm:aff id="aff1">Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation><affiliation><nlm:aff id="aff4">Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</nlm:aff></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Although auxin oxidation has long been known to be the primary mechanism of auxin catabolism and <italic>Arabidopsis</italic> seedlings have 10–100 more 2-oxindole 3-acetic acid compared with other auxin catabolic products, the enzymes that constitutively catalyze this process remained unknown. This work fills the gap by identifying and characterizing the <italic>Arabidopsis</italic> proteins DIOXYGENASE FOR AUXIN OXIDATION 1 (DAO1) and DAO2, which catalyze auxin oxidation under normal growth conditions and shows that this activity has a physiological function in planta. The protein localization and phenotypes of the loss/gain of function mutants support that DAO1 is the primary constitutive mechanism of auxin catabolism in <italic>Arabidopsis</italic> and that the temporal- and tissue-specific oxidative inactivation of auxin by DAO adjusts indole-3-acetic acid levels throughout the life of the plant to optimize growth and development.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27651492</article-id><article-id pub-id-type="pmc">5047167</article-id><article-id pub-id-type="publisher-id">201604769</article-id><article-id pub-id-type="doi">10.1073/pnas.1604769113</article-id><article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Plant Biology</subject></subj-group></subj-group><series-title>From the Cover</series-title></article-categories><title-group><article-title>DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in <italic>Arabidopsis thaliana</italic></article-title><alt-title alt-title-type="short">DAO auxin oxidase in <italic>Arabidopsis</italic></alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Jun</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Jinshan Ella</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Harris</surname><given-names>Chinchu</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Campos Mastrotti Pereira</surname><given-names>Fernanda</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wu</surname><given-names>Fan</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Blakeslee</surname><given-names>Joshua J.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Peer</surname><given-names>Wendy Ann</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><aff id="aff1"><sup>a</sup>Department of Plant Science and Landscape Architecture,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</aff><aff id="aff2"><sup>b</sup>Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</aff><aff id="aff3"><sup>c</sup>Ohio Agricultural Research and Development Center Metabolite Analysis Cluster, Ohio Agricultural Research and Development Center,<institution>The Ohio State University</institution>, Wooster,<addr-line>OH</addr-line> 44691;</aff><aff id="aff4"><sup>d</sup>Department of Environmental Science and Technology,<institution>University of Maryland</institution>, College Park,<addr-line>MD</addr-line> 20742;</aff><aff id="aff5"><sup>e</sup>Plant Protection and Animal Health, Forestry, Agronomy,<institution>Universidade Estadual de São Paulo</institution>, Sao Paulo,<country>Brazil</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>1</sup>To whom correspondence should be addressed. Email: <email>wapeer@umd.edu</email>.</corresp><fn fn-type="edited-by"><p>Edited by Mark Estelle, University of California at San Diego, La Jolla, CA, and approved July 29, 2016 (received for review March 22, 2016)</p></fn><fn fn-type="con"><p>Author contributions: J.Z. and W.A.P. designed research; J.Z., J.E.L., C.H., F.C.M.P., F.W., J.J.B., and W.A.P. performed research; J.Z., J.E.L., F.C.M.P., J.J.B., and W.A.P. analyzed data; and J.Z., J.E.L., J.J.B., and W.A.P. wrote the paper.</p></fn></author-notes><pub-date pub-type="ppub"><day>27</day><month>9</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>20</day><month>9</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>20</day><month>9</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>113</volume><issue>39</issue><fpage>11010</fpage><lpage>11015</lpage><permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p></license></permissions><self-uri xlink:title="pdf" xlink:href="pnas.201604769.pdf"></self-uri><related-article id="d36e219" related-article-type="companion" ext-link-type="doi" xlink:href="10.1073/pnas.1604375113"></related-article><related-article id="d36e220" related-article-type="companion" ext-link-type="doi" xlink:href="10.1073/pnas.1604458113"></related-article><abstract abstract-type="executive-summary"><title>Significance</title><p>Although auxin oxidation has long been known to be the primary mechanism of auxin catabolism and <italic>Arabidopsis</italic> seedlings have 10–100 more 2-oxindole 3-acetic acid compared with other auxin catabolic products, the enzymes that constitutively catalyze this process remained unknown. This work fills the gap by identifying and characterizing the <italic>Arabidopsis</italic> proteins DIOXYGENASE FOR AUXIN OXIDATION 1 (DAO1) and DAO2, which catalyze auxin oxidation under normal growth conditions and shows that this activity has a physiological function in planta. The protein localization and phenotypes of the loss/gain of function mutants support that DAO1 is the primary constitutive mechanism of auxin catabolism in <italic>Arabidopsis</italic> and that the temporal- and tissue-specific oxidative inactivation of auxin by DAO adjusts indole-3-acetic acid levels throughout the life of the plant to optimize growth and development.</p></abstract><abstract><p>Tight homeostatic regulation of the phytohormone auxin [indole-3-acetic acid (IAA)] is essential to plant growth. Auxin biosynthetic pathways and the processes that inactivate auxin by conjugation to amino acids and sugars have been thoroughly characterized. However, the enzyme that catalyzes oxidation of IAA to its primary catabolite 2-oxindole-3-acetic acid (oxIAA) remains uncharacterized. Here, we show that DIOXYGENASE FOR AUXIN OXIDATION 1 (DAO1) catalyzes formation of oxIAA in vitro and in vivo and that this mechanism regulates auxin homeostasis and plant growth. Null <italic>dao1-1</italic> mutants contain 95% less oxIAA compared with wild type, and complementation of <italic>dao1</italic> restores wild-type oxIAA levels, indicating that DAO1 is the primary IAA oxidase in seedlings. Furthermore, <italic>dao1</italic> loss of function plants have altered morphology, including larger cotyledons, increased lateral root density, delayed sepal opening, elongated pistils, and reduced fertility in the primary inflorescence stem. These phenotypes are tightly correlated with <italic>DAO1</italic> spatiotemporal expression patterns as shown by <italic>DAO1pro</italic>:β-glucuronidase (GUS) activity and <italic>DAO1pro</italic>:YFP-DAO1 signals, and transformation with <italic>DAO1pro</italic>:YFP-DAO1 complemented the mutant phenotypes. The dominant <italic>dao1-2D</italic> mutant has increased oxIAA levels and decreased stature with shorter leaves and inflorescence stems, thus supporting DAO1 IAA oxidase function in vivo. A second isoform, DAO2, is very weakly expressed in seedling root apices. Together, these data confirm that IAA oxidation by DAO1 is the principal auxin catabolic process in <italic>Arabidopsis</italic> and that localized IAA oxidation plays a role in plant morphogenesis.</p></abstract><kwd-group><kwd>auxin homeostasis</kwd><kwd>auxin oxidation</kwd><kwd>auxin oxidase</kwd><kwd>lateral roots</kwd><kwd>flowers</kwd></kwd-group><funding-group><award-group id="gs1"><funding-source id="sp1">Maryland Agricultural Experiment Station</funding-source><award-id rid="sp1">none</award-id></award-group><award-group id="gs2"><funding-source id="sp2">OARDC SEEDS</funding-source><award-id rid="sp2">none</award-id></award-group><award-group id="gs3"><funding-source id="sp3">CAPES</funding-source><award-id rid="sp3">none</award-id></award-group></funding-group><counts><page-count count="6"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Brésil</li></country></list><tree><noCountry><name sortKey="Blakeslee, Joshua J" sort="Blakeslee, Joshua J" uniqKey="Blakeslee J" first="Joshua J." last="Blakeslee">Joshua J. Blakeslee</name><name sortKey="Harris, Chinchu" sort="Harris, Chinchu" uniqKey="Harris C" first="Chinchu" last="Harris">Chinchu Harris</name><name sortKey="Lin, Jinshan Ella" sort="Lin, Jinshan Ella" uniqKey="Lin J" first="Jinshan Ella" last="Lin">Jinshan Ella Lin</name><name sortKey="Peer, Wendy Ann" sort="Peer, Wendy Ann" uniqKey="Peer W" first="Wendy Ann" last="Peer">Wendy Ann Peer</name><name sortKey="Wu, Fan" sort="Wu, Fan" uniqKey="Wu F" first="Fan" last="Wu">Fan Wu</name><name sortKey="Zhang, Jun" sort="Zhang, Jun" uniqKey="Zhang J" first="Jun" last="Zhang">Jun Zhang</name></noCountry><country name="Brésil"><noRegion><name sortKey="Campos Mastrotti Pereira, Fernanda" sort="Campos Mastrotti Pereira, Fernanda" uniqKey="Campos Mastrotti Pereira F" first="Fernanda" last="Campos Mastrotti Pereira">Fernanda Campos Mastrotti Pereira</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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