A cinnamoyl esterase from Aspergillus niger can break plant cell wall cross-links without release of free diferulic acids

Maria Teresa Garcia-Conesa, Paul A. Kroon, John Ralph, Fred A. Mellon, Ian J. Colquhoun, Luc Saulnier, Jean François Thibault, Gary Williamson

Research output: Contribution to journalArticleResearchpeer-review

Abstract

A cinnamoyl esterase, ferulic acid esterase A, from Aspergillus niger releases ferulic acid and 5-5- and 8-O-4-dehydrodiferulic acids from plant cell walls. The breakage of one or both ester bonds from dehydrodimer cross- links between plant cell wall polymers is essential for optimal action of carbohydrases on these substrates, but it is not known if cinnamoyl esterases can break these cross-links by cleaving one of the ester linkages which would not release the free dimer. It is difficult to determine the mechanism of the reaction on complex substrates, and so we have examined the catalytic properties of ferulic acid esterase A from Aspergillus niger using a range of synthetic ethyl esterified dehydrodimers (5-5-, 8-5-benzofuran and 8-O-4-) and two 5-5-diferulate oligosaccharides. Our results show that the esterase is able to cleave the three major dehydrodiferulate crosslinks present in plant cell walls. The enzyme is highly specific at hydrolysing the 5-5- and the 8-5-benzofuran diferulates but the 8-O-4-is a poorer substrate. The hydrolysis of dehydrodiferulates to free acids occurs in two discrete steps, one involving dissociation of a monoesterified intermediate which is negatively charged at the pH of the reaction. Although ferulic acid esterase A was able to release monoesters as products of reactions with all three forms of diesters, only the 5-5- and the 8-O-4-monoesters were substrates for the enzyme, forming the corresponding free diferulic acids. The esterase cannot hydrolyse the second ester bond from the 8-5-benzofuran monoester and therefore, ferulic acid esterase A does not form 8-5-benzofuran diferulic acid. Therefore, ferulic acid esterase A from Aspergillus niger contributes to total plant cell wall degradation by cleaving at least one ester bond from the diferulate cross-links that exist between wall polymers but does not always release the free acid product.

Original languageEnglish
Pages (from-to)644-652
Number of pages9
JournalEuropean Journal of Biochemistry
Volume266
Issue number2
DOIs
Publication statusPublished - 1 Dec 1999
Externally publishedYes

Keywords

  • Cross-links
  • Dehydrodiferulic acids
  • Esterase
  • Ferulic acid
  • Plant cell walls

Cite this

Garcia-Conesa, Maria Teresa ; Kroon, Paul A. ; Ralph, John ; Mellon, Fred A. ; Colquhoun, Ian J. ; Saulnier, Luc ; Thibault, Jean François ; Williamson, Gary. / A cinnamoyl esterase from Aspergillus niger can break plant cell wall cross-links without release of free diferulic acids. In: European Journal of Biochemistry. 1999 ; Vol. 266, No. 2. pp. 644-652.
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abstract = "A cinnamoyl esterase, ferulic acid esterase A, from Aspergillus niger releases ferulic acid and 5-5- and 8-O-4-dehydrodiferulic acids from plant cell walls. The breakage of one or both ester bonds from dehydrodimer cross- links between plant cell wall polymers is essential for optimal action of carbohydrases on these substrates, but it is not known if cinnamoyl esterases can break these cross-links by cleaving one of the ester linkages which would not release the free dimer. It is difficult to determine the mechanism of the reaction on complex substrates, and so we have examined the catalytic properties of ferulic acid esterase A from Aspergillus niger using a range of synthetic ethyl esterified dehydrodimers (5-5-, 8-5-benzofuran and 8-O-4-) and two 5-5-diferulate oligosaccharides. Our results show that the esterase is able to cleave the three major dehydrodiferulate crosslinks present in plant cell walls. The enzyme is highly specific at hydrolysing the 5-5- and the 8-5-benzofuran diferulates but the 8-O-4-is a poorer substrate. The hydrolysis of dehydrodiferulates to free acids occurs in two discrete steps, one involving dissociation of a monoesterified intermediate which is negatively charged at the pH of the reaction. Although ferulic acid esterase A was able to release monoesters as products of reactions with all three forms of diesters, only the 5-5- and the 8-O-4-monoesters were substrates for the enzyme, forming the corresponding free diferulic acids. The esterase cannot hydrolyse the second ester bond from the 8-5-benzofuran monoester and therefore, ferulic acid esterase A does not form 8-5-benzofuran diferulic acid. Therefore, ferulic acid esterase A from Aspergillus niger contributes to total plant cell wall degradation by cleaving at least one ester bond from the diferulate cross-links that exist between wall polymers but does not always release the free acid product.",
keywords = "Cross-links, Dehydrodiferulic acids, Esterase, Ferulic acid, Plant cell walls",
author = "Garcia-Conesa, {Maria Teresa} and Kroon, {Paul A.} and John Ralph and Mellon, {Fred A.} and Colquhoun, {Ian J.} and Luc Saulnier and Thibault, {Jean Fran{\cc}ois} and Gary Williamson",
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A cinnamoyl esterase from Aspergillus niger can break plant cell wall cross-links without release of free diferulic acids. / Garcia-Conesa, Maria Teresa; Kroon, Paul A.; Ralph, John; Mellon, Fred A.; Colquhoun, Ian J.; Saulnier, Luc; Thibault, Jean François; Williamson, Gary.

In: European Journal of Biochemistry, Vol. 266, No. 2, 01.12.1999, p. 644-652.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - A cinnamoyl esterase from Aspergillus niger can break plant cell wall cross-links without release of free diferulic acids

AU - Garcia-Conesa, Maria Teresa

AU - Kroon, Paul A.

AU - Ralph, John

AU - Mellon, Fred A.

AU - Colquhoun, Ian J.

AU - Saulnier, Luc

AU - Thibault, Jean François

AU - Williamson, Gary

PY - 1999/12/1

Y1 - 1999/12/1

N2 - A cinnamoyl esterase, ferulic acid esterase A, from Aspergillus niger releases ferulic acid and 5-5- and 8-O-4-dehydrodiferulic acids from plant cell walls. The breakage of one or both ester bonds from dehydrodimer cross- links between plant cell wall polymers is essential for optimal action of carbohydrases on these substrates, but it is not known if cinnamoyl esterases can break these cross-links by cleaving one of the ester linkages which would not release the free dimer. It is difficult to determine the mechanism of the reaction on complex substrates, and so we have examined the catalytic properties of ferulic acid esterase A from Aspergillus niger using a range of synthetic ethyl esterified dehydrodimers (5-5-, 8-5-benzofuran and 8-O-4-) and two 5-5-diferulate oligosaccharides. Our results show that the esterase is able to cleave the three major dehydrodiferulate crosslinks present in plant cell walls. The enzyme is highly specific at hydrolysing the 5-5- and the 8-5-benzofuran diferulates but the 8-O-4-is a poorer substrate. The hydrolysis of dehydrodiferulates to free acids occurs in two discrete steps, one involving dissociation of a monoesterified intermediate which is negatively charged at the pH of the reaction. Although ferulic acid esterase A was able to release monoesters as products of reactions with all three forms of diesters, only the 5-5- and the 8-O-4-monoesters were substrates for the enzyme, forming the corresponding free diferulic acids. The esterase cannot hydrolyse the second ester bond from the 8-5-benzofuran monoester and therefore, ferulic acid esterase A does not form 8-5-benzofuran diferulic acid. Therefore, ferulic acid esterase A from Aspergillus niger contributes to total plant cell wall degradation by cleaving at least one ester bond from the diferulate cross-links that exist between wall polymers but does not always release the free acid product.

AB - A cinnamoyl esterase, ferulic acid esterase A, from Aspergillus niger releases ferulic acid and 5-5- and 8-O-4-dehydrodiferulic acids from plant cell walls. The breakage of one or both ester bonds from dehydrodimer cross- links between plant cell wall polymers is essential for optimal action of carbohydrases on these substrates, but it is not known if cinnamoyl esterases can break these cross-links by cleaving one of the ester linkages which would not release the free dimer. It is difficult to determine the mechanism of the reaction on complex substrates, and so we have examined the catalytic properties of ferulic acid esterase A from Aspergillus niger using a range of synthetic ethyl esterified dehydrodimers (5-5-, 8-5-benzofuran and 8-O-4-) and two 5-5-diferulate oligosaccharides. Our results show that the esterase is able to cleave the three major dehydrodiferulate crosslinks present in plant cell walls. The enzyme is highly specific at hydrolysing the 5-5- and the 8-5-benzofuran diferulates but the 8-O-4-is a poorer substrate. The hydrolysis of dehydrodiferulates to free acids occurs in two discrete steps, one involving dissociation of a monoesterified intermediate which is negatively charged at the pH of the reaction. Although ferulic acid esterase A was able to release monoesters as products of reactions with all three forms of diesters, only the 5-5- and the 8-O-4-monoesters were substrates for the enzyme, forming the corresponding free diferulic acids. The esterase cannot hydrolyse the second ester bond from the 8-5-benzofuran monoester and therefore, ferulic acid esterase A does not form 8-5-benzofuran diferulic acid. Therefore, ferulic acid esterase A from Aspergillus niger contributes to total plant cell wall degradation by cleaving at least one ester bond from the diferulate cross-links that exist between wall polymers but does not always release the free acid product.

KW - Cross-links

KW - Dehydrodiferulic acids

KW - Esterase

KW - Ferulic acid

KW - Plant cell walls

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U2 - 10.1046/j.1432-1327.1999.00910.x

DO - 10.1046/j.1432-1327.1999.00910.x

M3 - Article

VL - 266

SP - 644

EP - 652

JO - European Journal of Biochemistry

JF - European Journal of Biochemistry

SN - 0014-2956

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