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4-Coumaroyl and caffeoyl shikimic acids inhibit 4-coumaric acid:coenzyme A ligases and modulate metabolic flux for 3-hydroxylation in monolignol biosynthesis of Populus trichocarpa.

Identifieur interne : 001F28 ( Main/Exploration ); précédent : 001F27; suivant : 001F29

4-Coumaroyl and caffeoyl shikimic acids inhibit 4-coumaric acid:coenzyme A ligases and modulate metabolic flux for 3-hydroxylation in monolignol biosynthesis of Populus trichocarpa.

Auteurs : Chien-Yuan Lin [États-Unis] ; Jack P. Wang [États-Unis] ; Quanzi Li [République populaire de Chine] ; Hsi-Chuan Chen [États-Unis] ; Jie Liu [États-Unis] ; Philip Loziuk [États-Unis] ; Jina Song [États-Unis] ; Cranos Williams [États-Unis] ; David C. Muddiman [États-Unis] ; Ronald R. Sederoff [États-Unis] ; Vincent L. Chiang [États-Unis]

Source :

RBID : pubmed:25578281

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English descriptors

Abstract

Downregulation of 4-coumaric acid:coenzyme A ligase (4CL) can reduce lignin content in a number of plant species. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes, Ptr4CL3 and Ptr4CL5, catalyze the coenzyme A (CoA) ligation of 4-coumaric acid to 4-coumaroyl-CoA and caffeic acid to caffeoyl-CoA. CoA ligation of 4-coumaric acid is essential for the 3-hydroxylation of 4-coumaroyl shikimic acid. This hydroxylation results from sequential reactions of 4-hydroxycinnamoyl-CoA:shikimic acid hydroxycinnamoyl transferases (PtrHCT1 and PtrHCT6) and 4-coumaric acid 3-hydroxylase 3 (PtrC3H3). Alternatively, 3-hydroxylation of 4-coumaric acid to caffeic acid may occur through an enzyme complex of cinnamic acid 4-hydroxylase 1 and 2 (PtrC4H1 and PtrC4H2) and PtrC3H3. We found that 4-coumaroyl and caffeoyl shikimic acids are inhibitors of Ptr4CL3 and Ptr4CL5. 4-Coumaroyl shikimic acid strongly inhibits the formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only the formation of 4-coumaroyl-CoA. 4-Coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Metabolic flux in wild-type and PtrC3H3 downregulated P. trichocarpa transgenics has been estimated by absolute protein and metabolite quantification based on liquid chromatography-tandem mass spectrometry, mass action kinetics, and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate.

DOI: 10.1016/j.molp.2014.12.003
PubMed: 25578281


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<term>Acyl Coenzyme A (metabolism)</term>
<term>Coenzyme A Ligases (metabolism)</term>
<term>Coumaric Acids (metabolism)</term>
<term>Coumaric Acids (pharmacology)</term>
<term>Hydroxylation (drug effects)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (drug effects)</term>
<term>Populus (enzymology)</term>
<term>Populus (metabolism)</term>
<term>Propionates (MeSH)</term>
<term>Shikimic Acid (pharmacology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acide shikimique (pharmacologie)</term>
<term>Acides coumariques (métabolisme)</term>
<term>Acides coumariques (pharmacologie)</term>
<term>Acyl coenzyme A (métabolisme)</term>
<term>Coenzyme A ligases (métabolisme)</term>
<term>Hydroxylation (effets des médicaments et des substances chimiques)</term>
<term>Populus (effets des médicaments et des substances chimiques)</term>
<term>Populus (enzymologie)</term>
<term>Populus (métabolisme)</term>
<term>Propionates (MeSH)</term>
<term>Protéines végétales (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Acyl Coenzyme A</term>
<term>Coenzyme A Ligases</term>
<term>Coumaric Acids</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Coumaric Acids</term>
<term>Shikimic Acid</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Hydroxylation</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Hydroxylation</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Acides coumariques</term>
<term>Acyl coenzyme A</term>
<term>Coenzyme A ligases</term>
<term>Populus</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acide shikimique</term>
<term>Acides coumariques</term>
</keywords>
<keywords scheme="MESH" type="chemical" xml:lang="en">
<term>Propionates</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Propionates</term>
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<front>
<div type="abstract" xml:lang="en">Downregulation of 4-coumaric acid:coenzyme A ligase (4CL) can reduce lignin content in a number of plant species. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes, Ptr4CL3 and Ptr4CL5, catalyze the coenzyme A (CoA) ligation of 4-coumaric acid to 4-coumaroyl-CoA and caffeic acid to caffeoyl-CoA. CoA ligation of 4-coumaric acid is essential for the 3-hydroxylation of 4-coumaroyl shikimic acid. This hydroxylation results from sequential reactions of 4-hydroxycinnamoyl-CoA:shikimic acid hydroxycinnamoyl transferases (PtrHCT1 and PtrHCT6) and 4-coumaric acid 3-hydroxylase 3 (PtrC3H3). Alternatively, 3-hydroxylation of 4-coumaric acid to caffeic acid may occur through an enzyme complex of cinnamic acid 4-hydroxylase 1 and 2 (PtrC4H1 and PtrC4H2) and PtrC3H3. We found that 4-coumaroyl and caffeoyl shikimic acids are inhibitors of Ptr4CL3 and Ptr4CL5. 4-Coumaroyl shikimic acid strongly inhibits the formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only the formation of 4-coumaroyl-CoA. 4-Coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Metabolic flux in wild-type and PtrC3H3 downregulated P. trichocarpa transgenics has been estimated by absolute protein and metabolite quantification based on liquid chromatography-tandem mass spectrometry, mass action kinetics, and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate. </div>
</front>
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<ELocationID EIdType="pii" ValidYN="Y">S1674-2052(14)00015-X</ELocationID>
<Abstract>
<AbstractText>Downregulation of 4-coumaric acid:coenzyme A ligase (4CL) can reduce lignin content in a number of plant species. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes, Ptr4CL3 and Ptr4CL5, catalyze the coenzyme A (CoA) ligation of 4-coumaric acid to 4-coumaroyl-CoA and caffeic acid to caffeoyl-CoA. CoA ligation of 4-coumaric acid is essential for the 3-hydroxylation of 4-coumaroyl shikimic acid. This hydroxylation results from sequential reactions of 4-hydroxycinnamoyl-CoA:shikimic acid hydroxycinnamoyl transferases (PtrHCT1 and PtrHCT6) and 4-coumaric acid 3-hydroxylase 3 (PtrC3H3). Alternatively, 3-hydroxylation of 4-coumaric acid to caffeic acid may occur through an enzyme complex of cinnamic acid 4-hydroxylase 1 and 2 (PtrC4H1 and PtrC4H2) and PtrC3H3. We found that 4-coumaroyl and caffeoyl shikimic acids are inhibitors of Ptr4CL3 and Ptr4CL5. 4-Coumaroyl shikimic acid strongly inhibits the formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only the formation of 4-coumaroyl-CoA. 4-Coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Metabolic flux in wild-type and PtrC3H3 downregulated P. trichocarpa transgenics has been estimated by absolute protein and metabolite quantification based on liquid chromatography-tandem mass spectrometry, mass action kinetics, and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate. </AbstractText>
<CopyrightInformation>Copyright © 2015 The Author. Published by Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Lin</LastName>
<ForeName>Chien-Yuan</ForeName>
<Initials>CY</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China; Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Jack P</ForeName>
<Initials>JP</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China; Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Quanzi</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China; State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing 100091, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Hsi-Chuan</ForeName>
<Initials>HC</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Jie</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Loziuk</LastName>
<ForeName>Philip</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>W.M. Keck FT-ICR Mass Spectrometry Laboratory, Department of Chemistry, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Song</LastName>
<ForeName>Jina</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Department of Electrical and Computer Engineering, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Williams</LastName>
<ForeName>Cranos</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Department of Electrical and Computer Engineering, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Muddiman</LastName>
<ForeName>David C</ForeName>
<Initials>DC</Initials>
<AffiliationInfo>
<Affiliation>W.M. Keck FT-ICR Mass Spectrometry Laboratory, Department of Chemistry, North Carolina State University, Raleigh, NC 27695, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sederoff</LastName>
<ForeName>Ronald R</ForeName>
<Initials>RR</Initials>
<AffiliationInfo>
<Affiliation>Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA. Electronic address: ron_sederoff@ncsu.edu.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chiang</LastName>
<ForeName>Vincent L</ForeName>
<Initials>VL</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China; Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695, USA. Electronic address: vchiang@ncsu.edu.</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>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>12</Month>
<Day>11</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Mol Plant</MedlineTA>
<NlmUniqueID>101465514</NlmUniqueID>
<ISSNLinking>1674-2052</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C403206">4-hydroxycinnamoyl-CoA</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000214">Acyl Coenzyme A</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D003373">Coumaric Acids</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011422">Propionates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>119785-99-8</RegistryNumber>
<NameOfSubstance UI="C058644">4-coumaroyl-coenzyme A</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>29MS2WI2NU</RegistryNumber>
<NameOfSubstance UI="D012765">Shikimic Acid</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 6.2.1.-</RegistryNumber>
<NameOfSubstance UI="D003066">Coenzyme A Ligases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>IBS9D1EU3J</RegistryNumber>
<NameOfSubstance UI="C495469">trans-3-(4'-hydroxyphenyl)-2-propenoic acid</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000214" MajorTopicYN="N">Acyl Coenzyme A</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003066" MajorTopicYN="N">Coenzyme A Ligases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003373" MajorTopicYN="N">Coumaric Acids</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006900" MajorTopicYN="N">Hydroxylation</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="Y">drug effects</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011422" MajorTopicYN="N">Propionates</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012765" MajorTopicYN="N">Shikimic Acid</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="Y">pharmacology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">4-coumaroyl and caffeoyl shikimic acids</Keyword>
<Keyword MajorTopicYN="N">LC-MS/MS</Keyword>
<Keyword MajorTopicYN="N">Populus trichocarpa</Keyword>
<Keyword MajorTopicYN="N">metabolic flux</Keyword>
<Keyword MajorTopicYN="N">monolignol biosynthesis</Keyword>
<Keyword MajorTopicYN="N">reaction and inhibition kinetics</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2014</Year>
<Month>09</Month>
<Day>04</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2014</Year>
<Month>10</Month>
<Day>07</Day>
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<Month>1</Month>
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</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">25578281</ArticleId>
<ArticleId IdType="pii">S1674-2052(14)00015-X</ArticleId>
<ArticleId IdType="doi">10.1016/j.molp.2014.12.003</ArticleId>
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</pubmed>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region>
<li>Caroline du Nord</li>
</region>
<settlement>
<li>Pékin</li>
</settlement>
</list>
<tree>
<country name="États-Unis">
<region name="Caroline du Nord">
<name sortKey="Lin, Chien Yuan" sort="Lin, Chien Yuan" uniqKey="Lin C" first="Chien-Yuan" last="Lin">Chien-Yuan Lin</name>
</region>
<name sortKey="Chen, Hsi Chuan" sort="Chen, Hsi Chuan" uniqKey="Chen H" first="Hsi-Chuan" last="Chen">Hsi-Chuan Chen</name>
<name sortKey="Chiang, Vincent L" sort="Chiang, Vincent L" uniqKey="Chiang V" first="Vincent L" last="Chiang">Vincent L. Chiang</name>
<name sortKey="Liu, Jie" sort="Liu, Jie" uniqKey="Liu J" first="Jie" last="Liu">Jie Liu</name>
<name sortKey="Loziuk, Philip" sort="Loziuk, Philip" uniqKey="Loziuk P" first="Philip" last="Loziuk">Philip Loziuk</name>
<name sortKey="Muddiman, David C" sort="Muddiman, David C" uniqKey="Muddiman D" first="David C" last="Muddiman">David C. Muddiman</name>
<name sortKey="Sederoff, Ronald R" sort="Sederoff, Ronald R" uniqKey="Sederoff R" first="Ronald R" last="Sederoff">Ronald R. Sederoff</name>
<name sortKey="Song, Jina" sort="Song, Jina" uniqKey="Song J" first="Jina" last="Song">Jina Song</name>
<name sortKey="Wang, Jack P" sort="Wang, Jack P" uniqKey="Wang J" first="Jack P" last="Wang">Jack P. Wang</name>
<name sortKey="Williams, Cranos" sort="Williams, Cranos" uniqKey="Williams C" first="Cranos" last="Williams">Cranos Williams</name>
</country>
<country name="République populaire de Chine">
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<name sortKey="Li, Quanzi" sort="Li, Quanzi" uniqKey="Li Q" first="Quanzi" last="Li">Quanzi Li</name>
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