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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 : 002404 ( Main/Exploration ); précédent : 002403; suivant : 002405

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:25336570

Abstract

In a number of plant species, downregulation of 4-coumaric acid: coenzyme A ligase (4CL) can reduce lignin content. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes Ptr4CL3 and Ptr4CL5 catalyze the 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 formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only formation of 4-coumaroyl-CoA. 4-coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Estimates of metabolic flux in wildtype and PtrC3H3 downregulated P. trichocarpa transgenics have been made using LC-MS/MS based absolute protein and metabolite quantification, mass action kinetics and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate.

DOI: 10.1093/mp/ssu117
PubMed: 25336570


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<div type="abstract" xml:lang="en">In a number of plant species, downregulation of 4-coumaric acid: coenzyme A ligase (4CL) can reduce lignin content. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes Ptr4CL3 and Ptr4CL5 catalyze the 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 formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only formation of 4-coumaroyl-CoA. 4-coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Estimates of metabolic flux in wildtype and PtrC3H3 downregulated P. trichocarpa transgenics have been made using LC-MS/MS based absolute protein and metabolite quantification, mass action kinetics and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate.</div>
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<AbstractText>In a number of plant species, downregulation of 4-coumaric acid: coenzyme A ligase (4CL) can reduce lignin content. In lignin precursor (monolignol) biosynthesis during stem wood formation in Populus trichocarpa, two enzymes Ptr4CL3 and Ptr4CL5 catalyze the 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 formation of 4-coumaroyl-CoA and caffeoyl-CoA. Caffeoyl shikimic acid inhibits only formation of 4-coumaroyl-CoA. 4-coumaroyl and caffeoyl shikimic acids both act as competitive and uncompetitive inhibitors. Estimates of metabolic flux in wildtype and PtrC3H3 downregulated P. trichocarpa transgenics have been made using LC-MS/MS based absolute protein and metabolite quantification, mass action kinetics and inhibition equations. Inhibition by 4-coumaroyl and caffeoyl shikimic acids may play significant regulatory roles when these inhibitors accumulate.</AbstractText>
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<Affiliation>Department of Electrical and Computer Engineering, North Carolina State University, Raleigh North Carolina, 27695, U.S.A.</Affiliation>
</AffiliationInfo>
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<LastName>Williams</LastName>
<ForeName>Cranos</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Department of Electrical and Computer Engineering, North Carolina State University, Raleigh North Carolina, 27695, U.S.A.</Affiliation>
</AffiliationInfo>
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<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, North Carolina 27695, U.S.A.</Affiliation>
</AffiliationInfo>
</Author>
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<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, North Carolina 27695, U.S.A 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, North Carolina 27695, U.S.A vchiang@ncsu.edu.</Affiliation>
</AffiliationInfo>
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<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>10</Month>
<Day>20</Day>
</ArticleDate>
</Article>
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<Country>England</Country>
<MedlineTA>Mol Plant</MedlineTA>
<NlmUniqueID>101465514</NlmUniqueID>
<ISSNLinking>1674-2052</ISSNLinking>
</MedlineJournalInfo>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">4-coumaroyl shikimic acid</Keyword>
<Keyword MajorTopicYN="N">LC-MS/MS</Keyword>
<Keyword MajorTopicYN="N">Populus trichocarpa</Keyword>
<Keyword MajorTopicYN="N">caffeoyl shikimic acid</Keyword>
<Keyword MajorTopicYN="N">metabolic flux</Keyword>
<Keyword MajorTopicYN="N">monolignol biosynthesis</Keyword>
<Keyword MajorTopicYN="N">reaction and inhibition kinetics</Keyword>
</KeywordList>
</MedlineCitation>
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<Year>2014</Year>
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<Hour>6</Hour>
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<Month>10</Month>
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<Minute>0</Minute>
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<Year>2014</Year>
<Month>10</Month>
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</History>
<PublicationStatus>aheadofprint</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">25336570</ArticleId>
<ArticleId IdType="pii">S167420521400015X</ArticleId>
<ArticleId IdType="doi">10.1093/mp/ssu117</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
</list>
<tree>
<country name="États-Unis">
<noRegion>
<name sortKey="Lin, Chien Yuan" sort="Lin, Chien Yuan" uniqKey="Lin C" first="Chien-Yuan" last="Lin">Chien-Yuan Lin</name>
</noRegion>
<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">
<noRegion>
<name sortKey="Li, Quanzi" sort="Li, Quanzi" uniqKey="Li Q" first="Quanzi" last="Li">Quanzi Li</name>
</noRegion>
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