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Monolignol pathway 4-coumaric acid:coenzyme A ligases in Populus trichocarpa: novel specificity, metabolic regulation, and simulation of coenzyme A ligation fluxes.

Identifieur interne : 002579 ( Main/Exploration ); précédent : 002578; suivant : 002580

Monolignol pathway 4-coumaric acid:coenzyme A ligases in Populus trichocarpa: novel specificity, metabolic regulation, and simulation of coenzyme A ligation fluxes.

Auteurs : Hsi-Chuan Chen [États-Unis] ; Jina Song ; Cranos M. Williams ; Christopher M. Shuford ; Jie Liu ; Jack P. Wang ; Quanzi Li ; Rui Shi ; Emine Gokce ; Joel Ducoste ; David C. Muddiman ; Ronald R. Sederoff ; Vincent L. Chiang

Source :

RBID : pubmed:23344904

Descripteurs français

English descriptors

Abstract

4-Coumaric acid:coenzyme A ligase (4CL) is involved in monolignol biosynthesis for lignification in plant cell walls. It ligates coenzyme A (CoA) with hydroxycinnamic acids, such as 4-coumaric and caffeic acids, into hydroxycinnamoyl-CoA thioesters. The ligation ensures the activated state of the acid for reduction into monolignols. In Populus spp., it has long been thought that one monolignol-specific 4CL is involved. Here, we present evidence of two monolignol 4CLs, Ptr4CL3 and Ptr4CL5, in Populus trichocarpa. Ptr4CL3 is the ortholog of the monolignol 4CL reported for many other species. Ptr4CL5 is novel. The two Ptr4CLs exhibited distinct Michaelis-Menten kinetic properties. Inhibition kinetics demonstrated that hydroxycinnamic acid substrates are also inhibitors of 4CL and suggested that Ptr4CL5 is an allosteric enzyme. Experimentally validated flux simulation, incorporating reaction/inhibition kinetics, suggested two CoA ligation paths in vivo: one through 4-coumaric acid and the other through caffeic acid. We previously showed that a membrane protein complex mediated the 3-hydroxylation of 4-coumaric acid to caffeic acid. The demonstration here of two ligation paths requiring these acids supports this 3-hydroxylation function. Ptr4CL3 regulates both CoA ligation paths with similar efficiencies, whereas Ptr4CL5 regulates primarily the caffeic acid path. Both paths can be inhibited by caffeic acid. The Ptr4CL5-catalyzed caffeic acid metabolism, therefore, may also act to mitigate the inhibition by caffeic acid to maintain a proper ligation flux. A high level of caffeic acid was detected in stem-differentiating xylem of P. trichocarpa. Our results suggest that Ptr4CL5 and caffeic acid coordinately modulate the CoA ligation flux for monolignol biosynthesis.

DOI: 10.1104/pp.112.210971
PubMed: 23344904
PubMed Central: PMC3585612


Affiliations:


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Le document en format XML

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<term>Allosteric Regulation (drug effects)</term>
<term>Binding Sites (MeSH)</term>
<term>Biosynthetic Pathways (drug effects)</term>
<term>Blotting, Western (MeSH)</term>
<term>Caffeic Acids (pharmacology)</term>
<term>Coenzyme A (metabolism)</term>
<term>Coenzyme A Ligases (antagonists & inhibitors)</term>
<term>Coenzyme A Ligases (metabolism)</term>
<term>Computer Simulation (MeSH)</term>
<term>Coumaric Acids (chemistry)</term>
<term>Coumaric Acids (metabolism)</term>
<term>Coumaric Acids (pharmacology)</term>
<term>Kinetics (MeSH)</term>
<term>Lignin (biosynthesis)</term>
<term>Lignin (chemistry)</term>
<term>Phenylpropionates (metabolism)</term>
<term>Phosphoproteins (metabolism)</term>
<term>Phosphorylation (drug effects)</term>
<term>Plant Extracts (MeSH)</term>
<term>Populus (drug effects)</term>
<term>Populus (enzymology)</term>
<term>Propionates (MeSH)</term>
<term>Proteomics (MeSH)</term>
<term>Recombinant Fusion Proteins (metabolism)</term>
<term>Sequence Homology, Amino Acid (MeSH)</term>
<term>Substrate Specificity (drug effects)</term>
<term>Xylem (drug effects)</term>
<term>Xylem (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acides caféiques (pharmacologie)</term>
<term>Acides coumariques (composition chimique)</term>
<term>Acides coumariques (métabolisme)</term>
<term>Acides coumariques (pharmacologie)</term>
<term>Cinétique (MeSH)</term>
<term>Coenzyme A (métabolisme)</term>
<term>Coenzyme A ligases (antagonistes et inhibiteurs)</term>
<term>Coenzyme A ligases (métabolisme)</term>
<term>Extraits de plantes (MeSH)</term>
<term>Lignine (biosynthèse)</term>
<term>Lignine (composition chimique)</term>
<term>Phosphoprotéines (métabolisme)</term>
<term>Phosphorylation (effets des médicaments et des substances chimiques)</term>
<term>Phénylpropionates (métabolisme)</term>
<term>Populus (effets des médicaments et des substances chimiques)</term>
<term>Populus (enzymologie)</term>
<term>Propionates (MeSH)</term>
<term>Protéines de fusion recombinantes (métabolisme)</term>
<term>Protéomique (MeSH)</term>
<term>Régulation allostérique (effets des médicaments et des substances chimiques)</term>
<term>Similitude de séquences d'acides aminés (MeSH)</term>
<term>Simulation numérique (MeSH)</term>
<term>Sites de fixation (MeSH)</term>
<term>Spécificité du substrat (effets des médicaments et des substances chimiques)</term>
<term>Technique de Western (MeSH)</term>
<term>Voies de biosynthèse (effets des médicaments et des substances chimiques)</term>
<term>Xylème (effets des médicaments et des substances chimiques)</term>
<term>Xylème (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="antagonists & inhibitors" xml:lang="en">
<term>Coenzyme A Ligases</term>
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<keywords scheme="MESH" type="chemical" qualifier="biosynthesis" xml:lang="en">
<term>Lignin</term>
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<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Coumaric Acids</term>
<term>Lignin</term>
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<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Coenzyme A</term>
<term>Coenzyme A Ligases</term>
<term>Coumaric Acids</term>
<term>Phenylpropionates</term>
<term>Phosphoproteins</term>
<term>Recombinant Fusion Proteins</term>
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<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Caffeic Acids</term>
<term>Coumaric Acids</term>
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<keywords scheme="MESH" qualifier="antagonistes et inhibiteurs" xml:lang="fr">
<term>Coenzyme A ligases</term>
</keywords>
<keywords scheme="MESH" qualifier="biosynthèse" xml:lang="fr">
<term>Lignine</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Acides coumariques</term>
<term>Lignine</term>
</keywords>
<keywords scheme="MESH" qualifier="drug effects" xml:lang="en">
<term>Allosteric Regulation</term>
<term>Biosynthetic Pathways</term>
<term>Phosphorylation</term>
<term>Populus</term>
<term>Substrate Specificity</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Phosphorylation</term>
<term>Populus</term>
<term>Régulation allostérique</term>
<term>Spécificité du substrat</term>
<term>Voies de biosynthèse</term>
<term>Xylème</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>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Acides coumariques</term>
<term>Coenzyme A</term>
<term>Coenzyme A ligases</term>
<term>Phosphoprotéines</term>
<term>Phénylpropionates</term>
<term>Protéines de fusion recombinantes</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acides caféiques</term>
<term>Acides coumariques</term>
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<term>Binding Sites</term>
<term>Blotting, Western</term>
<term>Computer Simulation</term>
<term>Kinetics</term>
<term>Plant Extracts</term>
<term>Propionates</term>
<term>Proteomics</term>
<term>Sequence Homology, Amino Acid</term>
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<keywords scheme="MESH" xml:lang="fr">
<term>Cinétique</term>
<term>Extraits de plantes</term>
<term>Propionates</term>
<term>Protéomique</term>
<term>Similitude de séquences d'acides aminés</term>
<term>Simulation numérique</term>
<term>Sites de fixation</term>
<term>Technique de Western</term>
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<div type="abstract" xml:lang="en">4-Coumaric acid:coenzyme A ligase (4CL) is involved in monolignol biosynthesis for lignification in plant cell walls. It ligates coenzyme A (CoA) with hydroxycinnamic acids, such as 4-coumaric and caffeic acids, into hydroxycinnamoyl-CoA thioesters. The ligation ensures the activated state of the acid for reduction into monolignols. In Populus spp., it has long been thought that one monolignol-specific 4CL is involved. Here, we present evidence of two monolignol 4CLs, Ptr4CL3 and Ptr4CL5, in Populus trichocarpa. Ptr4CL3 is the ortholog of the monolignol 4CL reported for many other species. Ptr4CL5 is novel. The two Ptr4CLs exhibited distinct Michaelis-Menten kinetic properties. Inhibition kinetics demonstrated that hydroxycinnamic acid substrates are also inhibitors of 4CL and suggested that Ptr4CL5 is an allosteric enzyme. Experimentally validated flux simulation, incorporating reaction/inhibition kinetics, suggested two CoA ligation paths in vivo: one through 4-coumaric acid and the other through caffeic acid. We previously showed that a membrane protein complex mediated the 3-hydroxylation of 4-coumaric acid to caffeic acid. The demonstration here of two ligation paths requiring these acids supports this 3-hydroxylation function. Ptr4CL3 regulates both CoA ligation paths with similar efficiencies, whereas Ptr4CL5 regulates primarily the caffeic acid path. Both paths can be inhibited by caffeic acid. The Ptr4CL5-catalyzed caffeic acid metabolism, therefore, may also act to mitigate the inhibition by caffeic acid to maintain a proper ligation flux. A high level of caffeic acid was detected in stem-differentiating xylem of P. trichocarpa. Our results suggest that Ptr4CL5 and caffeic acid coordinately modulate the CoA ligation flux for monolignol biosynthesis.</div>
</front>
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<AbstractText>4-Coumaric acid:coenzyme A ligase (4CL) is involved in monolignol biosynthesis for lignification in plant cell walls. It ligates coenzyme A (CoA) with hydroxycinnamic acids, such as 4-coumaric and caffeic acids, into hydroxycinnamoyl-CoA thioesters. The ligation ensures the activated state of the acid for reduction into monolignols. In Populus spp., it has long been thought that one monolignol-specific 4CL is involved. Here, we present evidence of two monolignol 4CLs, Ptr4CL3 and Ptr4CL5, in Populus trichocarpa. Ptr4CL3 is the ortholog of the monolignol 4CL reported for many other species. Ptr4CL5 is novel. The two Ptr4CLs exhibited distinct Michaelis-Menten kinetic properties. Inhibition kinetics demonstrated that hydroxycinnamic acid substrates are also inhibitors of 4CL and suggested that Ptr4CL5 is an allosteric enzyme. Experimentally validated flux simulation, incorporating reaction/inhibition kinetics, suggested two CoA ligation paths in vivo: one through 4-coumaric acid and the other through caffeic acid. We previously showed that a membrane protein complex mediated the 3-hydroxylation of 4-coumaric acid to caffeic acid. The demonstration here of two ligation paths requiring these acids supports this 3-hydroxylation function. Ptr4CL3 regulates both CoA ligation paths with similar efficiencies, whereas Ptr4CL5 regulates primarily the caffeic acid path. Both paths can be inhibited by caffeic acid. The Ptr4CL5-catalyzed caffeic acid metabolism, therefore, may also act to mitigate the inhibition by caffeic acid to maintain a proper ligation flux. A high level of caffeic acid was detected in stem-differentiating xylem of P. trichocarpa. Our results suggest that Ptr4CL5 and caffeic acid coordinately modulate the CoA ligation flux for monolignol biosynthesis.</AbstractText>
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