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Evolution of coumaroyl conjugate 3-hydroxylases in land plants: lignin biosynthesis and defense.

Identifieur interne : 000975 ( Main/Exploration ); précédent : 000974; suivant : 000976

Evolution of coumaroyl conjugate 3-hydroxylases in land plants: lignin biosynthesis and defense.

Auteurs : Annette V. Alber [France, Canada] ; Hugues Renault [France] ; Alexandra Basilio-Lopes [France] ; Jean-Etienne Bassard [France] ; Zhenhua Liu [France] ; Pascaline Ullmann [France] ; Agnès Lesot [France] ; Frédéric Bihel [France] ; Martine Schmitt [France] ; Danièle Werck-Reichhart [France] ; Jürgen Ehlting [Canada]

Source :

RBID : pubmed:31038800

Descripteurs français

English descriptors

Abstract

Multiple adaptations were necessary when plants conquered the land. Among them were soluble phenylpropanoids related to plant protection and lignin necessary for upright growth and long-distance water transport. Cytochrome P450 monooxygenase 98 (CYP98) catalyzes a rate-limiting step in phenylpropanoid biosynthesis. Phylogenetic reconstructions suggest that a single copy of CYP98 founded each major land plant lineage (bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms), and was maintained as a single copy in all lineages but the angiosperms. In angiosperms, a series of independent gene duplications and losses occurred. Biochemical assays in four angiosperm species tested showed that 4-coumaroyl-shikimate, a known intermediate in lignin biosynthesis, was the preferred substrate of one member in each species, while independent duplicates in Populus trichocarpa and Amborella trichopoda each showed broad substrate ranges, accepting numerous 4-coumaroyl-esters and -amines, and were thus capable of producing a wide range of hydroxycinnamoyl conjugates. The gymnosperm CYP98 from Pinus taeda showed a broad substrate range, but preferred 4-coumaroyl-shikimate as its best substrate. In contrast, CYP98s from the lycophyte Selaginella moellendorffii and the fern Pteris vittata converted 4-coumaroyl-shikimate poorly in vitro, but were able to use alternative substrates, in particular 4-coumaroyl-anthranilate. Thus, caffeoyl-shikimate appears unlikely to be an intermediate in monolignol biosynthesis in non-seed vascular plants, including ferns. The best substrate for CYP98A34 from the moss Physcomitrella patens was also 4-coumaroyl-anthranilate, while 4-coumaroyl-shikimate was converted to lower extents. Despite having in vitro activity with 4-coumaroyl-shikimate, CYP98A34 was unable to complement the Arabidopsis thaliana cyp98a3 loss-of-function phenotype, suggesting distinct properties also in vivo.

DOI: 10.1111/tpj.14373
PubMed: 31038800


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Le document en format XML

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<term>Arabidopsis (metabolism)</term>
<term>Bryophyta (metabolism)</term>
<term>Bryopsida (metabolism)</term>
<term>Cytochrome P-450 Enzyme System (classification)</term>
<term>Cytochrome P-450 Enzyme System (genetics)</term>
<term>Cytochrome P-450 Enzyme System (metabolism)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Lignin (biosynthesis)</term>
<term>Magnoliopsida (metabolism)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Proteins (classification)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (MeSH)</term>
<term>Pteris (metabolism)</term>
<term>Selaginellaceae (metabolism)</term>
<term>Shikimic Acid (MeSH)</term>
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<term>Acide shikimique (MeSH)</term>
<term>Arabidopsis (métabolisme)</term>
<term>Bryophyta (métabolisme)</term>
<term>Bryopsida (métabolisme)</term>
<term>Cytochrome P-450 enzyme system (classification)</term>
<term>Cytochrome P-450 enzyme system (génétique)</term>
<term>Cytochrome P-450 enzyme system (métabolisme)</term>
<term>Lignine (biosynthèse)</term>
<term>Magnoliopsida (métabolisme)</term>
<term>Phylogenèse (MeSH)</term>
<term>Populus (MeSH)</term>
<term>Protéines végétales (classification)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Pteris (métabolisme)</term>
<term>Selaginellaceae (métabolisme)</term>
<term>Évolution moléculaire (MeSH)</term>
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<term>Lignin</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="classification" xml:lang="en">
<term>Cytochrome P-450 Enzyme System</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Cytochrome P-450 Enzyme System</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr">
<term>Lignine</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="fr">
<term>Cytochrome P-450 enzyme system</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Cytochrome P-450 enzyme system</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Arabidopsis</term>
<term>Bryophyta</term>
<term>Bryopsida</term>
<term>Cytochrome P-450 Enzyme System</term>
<term>Magnoliopsida</term>
<term>Plant Proteins</term>
<term>Pteris</term>
<term>Selaginellaceae</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Arabidopsis</term>
<term>Bryophyta</term>
<term>Bryopsida</term>
<term>Cytochrome P-450 enzyme system</term>
<term>Magnoliopsida</term>
<term>Protéines végétales</term>
<term>Pteris</term>
<term>Selaginellaceae</term>
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<term>Evolution, Molecular</term>
<term>Phylogeny</term>
<term>Populus</term>
<term>Shikimic Acid</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Acide shikimique</term>
<term>Phylogenèse</term>
<term>Populus</term>
<term>Évolution moléculaire</term>
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<front>
<div type="abstract" xml:lang="en">Multiple adaptations were necessary when plants conquered the land. Among them were soluble phenylpropanoids related to plant protection and lignin necessary for upright growth and long-distance water transport. Cytochrome P450 monooxygenase 98 (CYP98) catalyzes a rate-limiting step in phenylpropanoid biosynthesis. Phylogenetic reconstructions suggest that a single copy of CYP98 founded each major land plant lineage (bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms), and was maintained as a single copy in all lineages but the angiosperms. In angiosperms, a series of independent gene duplications and losses occurred. Biochemical assays in four angiosperm species tested showed that 4-coumaroyl-shikimate, a known intermediate in lignin biosynthesis, was the preferred substrate of one member in each species, while independent duplicates in Populus trichocarpa and Amborella trichopoda each showed broad substrate ranges, accepting numerous 4-coumaroyl-esters and -amines, and were thus capable of producing a wide range of hydroxycinnamoyl conjugates. The gymnosperm CYP98 from Pinus taeda showed a broad substrate range, but preferred 4-coumaroyl-shikimate as its best substrate. In contrast, CYP98s from the lycophyte Selaginella moellendorffii and the fern Pteris vittata converted 4-coumaroyl-shikimate poorly in vitro, but were able to use alternative substrates, in particular 4-coumaroyl-anthranilate. Thus, caffeoyl-shikimate appears unlikely to be an intermediate in monolignol biosynthesis in non-seed vascular plants, including ferns. The best substrate for CYP98A34 from the moss Physcomitrella patens was also 4-coumaroyl-anthranilate, while 4-coumaroyl-shikimate was converted to lower extents. Despite having in vitro activity with 4-coumaroyl-shikimate, CYP98A34 was unable to complement the Arabidopsis thaliana cyp98a3 loss-of-function phenotype, suggesting distinct properties also in vivo.</div>
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<DateCompleted>
<Year>2020</Year>
<Month>06</Month>
<Day>29</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>06</Month>
<Day>29</Day>
</DateRevised>
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<Journal>
<ISSN IssnType="Electronic">1365-313X</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>99</Volume>
<Issue>5</Issue>
<PubDate>
<Year>2019</Year>
<Month>09</Month>
</PubDate>
</JournalIssue>
<Title>The Plant journal : for cell and molecular biology</Title>
<ISOAbbreviation>Plant J</ISOAbbreviation>
</Journal>
<ArticleTitle>Evolution of coumaroyl conjugate 3-hydroxylases in land plants: lignin biosynthesis and defense.</ArticleTitle>
<Pagination>
<MedlinePgn>924-936</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.14373</ELocationID>
<Abstract>
<AbstractText>Multiple adaptations were necessary when plants conquered the land. Among them were soluble phenylpropanoids related to plant protection and lignin necessary for upright growth and long-distance water transport. Cytochrome P450 monooxygenase 98 (CYP98) catalyzes a rate-limiting step in phenylpropanoid biosynthesis. Phylogenetic reconstructions suggest that a single copy of CYP98 founded each major land plant lineage (bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms), and was maintained as a single copy in all lineages but the angiosperms. In angiosperms, a series of independent gene duplications and losses occurred. Biochemical assays in four angiosperm species tested showed that 4-coumaroyl-shikimate, a known intermediate in lignin biosynthesis, was the preferred substrate of one member in each species, while independent duplicates in Populus trichocarpa and Amborella trichopoda each showed broad substrate ranges, accepting numerous 4-coumaroyl-esters and -amines, and were thus capable of producing a wide range of hydroxycinnamoyl conjugates. The gymnosperm CYP98 from Pinus taeda showed a broad substrate range, but preferred 4-coumaroyl-shikimate as its best substrate. In contrast, CYP98s from the lycophyte Selaginella moellendorffii and the fern Pteris vittata converted 4-coumaroyl-shikimate poorly in vitro, but were able to use alternative substrates, in particular 4-coumaroyl-anthranilate. Thus, caffeoyl-shikimate appears unlikely to be an intermediate in monolignol biosynthesis in non-seed vascular plants, including ferns. The best substrate for CYP98A34 from the moss Physcomitrella patens was also 4-coumaroyl-anthranilate, while 4-coumaroyl-shikimate was converted to lower extents. Despite having in vitro activity with 4-coumaroyl-shikimate, CYP98A34 was unable to complement the Arabidopsis thaliana cyp98a3 loss-of-function phenotype, suggesting distinct properties also in vivo.</AbstractText>
<CopyrightInformation>© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Alber</LastName>
<ForeName>Annette V</ForeName>
<Initials>AV</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, Victoria, BC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Renault</LastName>
<ForeName>Hugues</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Basilio-Lopes</LastName>
<ForeName>Alexandra</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire d'Innovation Thérapeutique, UMR CNRS 7200, Illkirch, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bassard</LastName>
<ForeName>Jean-Etienne</ForeName>
<Initials>JE</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Zhenhua</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ullmann</LastName>
<ForeName>Pascaline</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lesot</LastName>
<ForeName>Agnès</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bihel</LastName>
<ForeName>Frédéric</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire d'Innovation Thérapeutique, UMR CNRS 7200, Illkirch, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schmitt</LastName>
<ForeName>Martine</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Laboratoire d'Innovation Thérapeutique, UMR CNRS 7200, Illkirch, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Werck-Reichhart</LastName>
<ForeName>Danièle</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Institute of Plant Molecular Biology, CNRS, University of Strasbourg, Strasbourg, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ehlting</LastName>
<ForeName>Jürgen</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0003-2302-696X</Identifier>
<AffiliationInfo>
<Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, Victoria, BC, Canada.</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>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>06</Month>
<Day>08</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Plant J</MedlineTA>
<NlmUniqueID>9207397</NlmUniqueID>
<ISSNLinking>0960-7412</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>29MS2WI2NU</RegistryNumber>
<NameOfSubstance UI="D012765">Shikimic Acid</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>9005-53-2</RegistryNumber>
<NameOfSubstance UI="D008031">Lignin</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>9035-51-2</RegistryNumber>
<NameOfSubstance UI="D003577">Cytochrome P-450 Enzyme System</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 1.14.-</RegistryNumber>
<NameOfSubstance UI="C110890">cytochrome P-450 CYP98A1 (Sorghum bicolor)</NameOfSubstance>
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<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D044002" MajorTopicYN="N">Bryophyta</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019068" MajorTopicYN="N">Bryopsida</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003577" MajorTopicYN="N">Cytochrome P-450 Enzyme System</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<MeshHeading>
<DescriptorName UI="D019143" MajorTopicYN="Y">Evolution, Molecular</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D008031" MajorTopicYN="N">Lignin</DescriptorName>
<QualifierName UI="Q000096" MajorTopicYN="Y">biosynthesis</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019684" MajorTopicYN="N">Magnoliopsida</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032495" MajorTopicYN="N">Pteris</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032503" MajorTopicYN="N">Selaginellaceae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012765" MajorTopicYN="N">Shikimic Acid</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">cell wall</Keyword>
<Keyword MajorTopicYN="Y">cytochrome P450 CYP98</Keyword>
<Keyword MajorTopicYN="Y">molecular evolution</Keyword>
<Keyword MajorTopicYN="Y">phenylpropanoids</Keyword>
<Keyword MajorTopicYN="Y">plant chemical defenses</Keyword>
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<Day>27</Day>
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<Year>2019</Year>
<Month>04</Month>
<Day>03</Day>
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