Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism

Bastian Daniel; Tea Pavkov-keller; Barbara Steiner; Andela Dordic; Alexander Gutmann; Bernd Nidetzky; Christoph W. Sensen; Eric Van Der Graaff; Silvia Wallner; Karl Gruber; Peter Macheroux

doi:10.1074/jbc.m115.659631

Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism

Bastian Daniel, Tea Pavkov-keller, Barbara Steiner, Andela Dordic, Alexander Gutmann, Bernd Nidetzky, Christoph W. Sensen, Eric Van Der Graaff, Silvia Wallner, Karl Gruber, Peter Macheroux

Section for Crop Sciences

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Abstract

Plant genomes contain a large number of genes encoding for berberine bridge enzyme (BBE)-like enzymes. Despite the wide-spread occurrence and abundance of this protein family in the plant kingdom, the biochemical function remains largely unexplored. In this study, we have expressed two members of the BBE-like enzyme family from Arabidopsis thaliana in the host organism Komagataella pastoris. The two proteins, termed AtBBE-like 13 and AtBBE-like 15, were purified, and their catalytic properties were determined. In addition, AtBBE-like 15 was crystallized and structurally characterized by x-ray crystallography. Here, we show that the enzymes catalyze the oxidation of aromatic allylic alcohols, such as coumaryl, sinapyl, and coniferyl alcohol, to the corresponding aldehydes and that AtBBE-like 15 adopts the same fold as vanillyl alcohol oxidase as reported previously for berberine bridge enzyme and other FAD-dependent oxidoreductases. Further analysis of the substrate range identified coniferin, the glycosylated storage form of coniferyl alcohol, as a substrate of the enzymes, whereas other glycosylated monolignols were rather poor substrates. A detailed analysis of the motifs present in the active sites of the BBE-like enzymes in A. thaliana suggested that 14 out of 28 members of the family might catalyze similar reactions. Based on these findings, we propose a novel role of BBE-like enzymes in monolignol metabolism that was previously not recognized for this enzyme family.

Original language	English
Journal	Journal of Biological Chemistry
Volume	290
Issue number	30
Pages (from-to)	18770-18781
Number of pages	12
ISSN	0021-9258
DOIs	https://doi.org/10.1074/jbc.m115.659631
Publication status	Published - 24 Jul 2015

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Daniel, B., Pavkov-keller, T., Steiner, B., Dordic, A., Gutmann, A., Nidetzky, B., Sensen, C. W., Van Der Graaff, E., Wallner, S., Gruber, K., & Macheroux, P. (2015). Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism. Journal of Biological Chemistry, 290(30), 18770-18781. https://doi.org/10.1074/jbc.m115.659631

Daniel, B, Pavkov-keller, T, Steiner, B, Dordic, A, Gutmann, A, Nidetzky, B, Sensen, CW, Van Der Graaff, E, Wallner, S, Gruber, K & Macheroux, P 2015, 'Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism', Journal of Biological Chemistry, vol. 290, no. 30, pp. 18770-18781. https://doi.org/10.1074/jbc.m115.659631

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title = "Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism",

abstract = "Plant genomes contain a large number of genes encoding for berberine bridge enzyme (BBE)-like enzymes. Despite the wide-spread occurrence and abundance of this protein family in the plant kingdom, the biochemical function remains largely unexplored. In this study, we have expressed two members of the BBE-like enzyme family from Arabidopsis thaliana in the host organism Komagataella pastoris. The two proteins, termed AtBBE-like 13 and AtBBE-like 15, were purified, and their catalytic properties were determined. In addition, AtBBE-like 15 was crystallized and structurally characterized by x-ray crystallography. Here, we show that the enzymes catalyze the oxidation of aromatic allylic alcohols, such as coumaryl, sinapyl, and coniferyl alcohol, to the corresponding aldehydes and that AtBBE-like 15 adopts the same fold as vanillyl alcohol oxidase as reported previously for berberine bridge enzyme and other FAD-dependent oxidoreductases. Further analysis of the substrate range identified coniferin, the glycosylated storage form of coniferyl alcohol, as a substrate of the enzymes, whereas other glycosylated monolignols were rather poor substrates. A detailed analysis of the motifs present in the active sites of the BBE-like enzymes in A. thaliana suggested that 14 out of 28 members of the family might catalyze similar reactions. Based on these findings, we propose a novel role of BBE-like enzymes in monolignol metabolism that was previously not recognized for this enzyme family.",

author = "Bastian Daniel and Tea Pavkov-keller and Barbara Steiner and Andela Dordic and Alexander Gutmann and Bernd Nidetzky and Sensen, {Christoph W.} and {Van Der Graaff}, Eric and Silvia Wallner and Karl Gruber and Peter Macheroux",

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AU - Daniel, Bastian

AU - Pavkov-keller, Tea

AU - Steiner, Barbara

AU - Dordic, Andela

AU - Gutmann, Alexander

AU - Nidetzky, Bernd

AU - Sensen, Christoph W.

AU - Van Der Graaff, Eric

AU - Wallner, Silvia

AU - Gruber, Karl

AU - Macheroux, Peter

PY - 2015/7/24

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N2 - Plant genomes contain a large number of genes encoding for berberine bridge enzyme (BBE)-like enzymes. Despite the wide-spread occurrence and abundance of this protein family in the plant kingdom, the biochemical function remains largely unexplored. In this study, we have expressed two members of the BBE-like enzyme family from Arabidopsis thaliana in the host organism Komagataella pastoris. The two proteins, termed AtBBE-like 13 and AtBBE-like 15, were purified, and their catalytic properties were determined. In addition, AtBBE-like 15 was crystallized and structurally characterized by x-ray crystallography. Here, we show that the enzymes catalyze the oxidation of aromatic allylic alcohols, such as coumaryl, sinapyl, and coniferyl alcohol, to the corresponding aldehydes and that AtBBE-like 15 adopts the same fold as vanillyl alcohol oxidase as reported previously for berberine bridge enzyme and other FAD-dependent oxidoreductases. Further analysis of the substrate range identified coniferin, the glycosylated storage form of coniferyl alcohol, as a substrate of the enzymes, whereas other glycosylated monolignols were rather poor substrates. A detailed analysis of the motifs present in the active sites of the BBE-like enzymes in A. thaliana suggested that 14 out of 28 members of the family might catalyze similar reactions. Based on these findings, we propose a novel role of BBE-like enzymes in monolignol metabolism that was previously not recognized for this enzyme family.

AB - Plant genomes contain a large number of genes encoding for berberine bridge enzyme (BBE)-like enzymes. Despite the wide-spread occurrence and abundance of this protein family in the plant kingdom, the biochemical function remains largely unexplored. In this study, we have expressed two members of the BBE-like enzyme family from Arabidopsis thaliana in the host organism Komagataella pastoris. The two proteins, termed AtBBE-like 13 and AtBBE-like 15, were purified, and their catalytic properties were determined. In addition, AtBBE-like 15 was crystallized and structurally characterized by x-ray crystallography. Here, we show that the enzymes catalyze the oxidation of aromatic allylic alcohols, such as coumaryl, sinapyl, and coniferyl alcohol, to the corresponding aldehydes and that AtBBE-like 15 adopts the same fold as vanillyl alcohol oxidase as reported previously for berberine bridge enzyme and other FAD-dependent oxidoreductases. Further analysis of the substrate range identified coniferin, the glycosylated storage form of coniferyl alcohol, as a substrate of the enzymes, whereas other glycosylated monolignols were rather poor substrates. A detailed analysis of the motifs present in the active sites of the BBE-like enzymes in A. thaliana suggested that 14 out of 28 members of the family might catalyze similar reactions. Based on these findings, we propose a novel role of BBE-like enzymes in monolignol metabolism that was previously not recognized for this enzyme family.

U2 - 10.1074/jbc.m115.659631

DO - 10.1074/jbc.m115.659631

M3 - Journal article

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SN - 0021-9258

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SP - 18770

EP - 18781

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

IS - 30

ER -

Oxidation of Monolignols by Members of the Berberine Bridge Enzyme Family Suggests a Role in Plant Cell Wall Metabolism

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