The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes

doi:10.1038/s41477-018-0142-9

Title: The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes

Abstract

Lignin is a complex and irregular biopolymer of cross-linked phenylpropanoid units in plant secondary cell walls. Its biosynthesis requires three endoplasmic reticulum (ER)-resident cytochrome P450 monooxygenases, C4H, C3'H and F5H, to establish the structural characteristics of its monomeric precursors. Those P450 enzymes were reported to associate with each other or potentially with other soluble monolignol biosynthetic enzymes to form enzyme complex or metabolone. However, molecular basis governing such enzyme or pathway organization remains elusive. Here we show that Arabidopsis membrane steroid binding proteins (MSBPs) serve as scaffold physically organizing monolignol P450 monooxygenases thereby regulating lignin biosynthetic process. We find that although C4H, C3'H and F5H are in spatial proximity to each other on ER membrane in vivo, they do not appear to directly interact with each other. Instead, two MSBP proteins physically interact with all three P450 enzymes and, moreover, MSBPs themselves associate as homo- and heteromers on the ER membrane, thereby organizing P450 clusters. Down-regulation of MSBPs does not affect the transcription levels of monolignol biosynthetic P450 genes but substantially impairs the stability and activity of the MSBP-interacting P450 enzymes and, consequently, the lignin deposition, the accumulation of soluble phenolics in monolignol branch but not in flavonoid pathway. Furthermore,more »« less

Authors:

^[1]; Ran, Xiuzhi ^[1]; Martin, Dwight W. ^[2];

^[1]

Brookhaven National Lab. (BNL), Upton, NY (United States)
Stony Brook Univ., Stony Brook, NY (United States)

Publication Date:: 2018-04-30

Research Org.:: Brookhaven National Lab. (BNL), Upton, NY (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

OSTI Identifier:: 1462422

Report Number(s):: BNL-207910-2018-JAAM
Journal ID: ISSN 2055-0278

Grant/Contract Number:: SC0012704

Resource Type:: Accepted Manuscript

Journal Name:: Nature Plants

Additional Journal Information:: Journal Volume: 4; Journal Issue: 5; Journal ID: ISSN 2055-0278

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Gou, Mingyue, Ran, Xiuzhi, Martin, Dwight W., and Liu, Chang -Jun. The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes.  United States: N. p., 2018. 
        Web.  doi:10.1038/s41477-018-0142-9.

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                    Gou, Mingyue, Ran, Xiuzhi, Martin, Dwight W., & Liu, Chang -Jun. The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes.  United States.  doi:10.1038/s41477-018-0142-9.

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                    Gou, Mingyue, Ran, Xiuzhi, Martin, Dwight W., and Liu, Chang -Jun. Mon .  
        "The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes".  United States.  doi:10.1038/s41477-018-0142-9.  https://www.osti.gov/servlets/purl/1462422.

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@article{osti_1462422,

  title        = {The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes},

  author       = {Gou, Mingyue and Ran, Xiuzhi and Martin, Dwight W. and Liu, Chang -Jun},

  abstractNote = {Lignin is a complex and irregular biopolymer of cross-linked phenylpropanoid units in plant secondary cell walls. Its biosynthesis requires three endoplasmic reticulum (ER)-resident cytochrome P450 monooxygenases, C4H, C3'H and F5H, to establish the structural characteristics of its monomeric precursors. Those P450 enzymes were reported to associate with each other or potentially with other soluble monolignol biosynthetic enzymes to form enzyme complex or metabolone. However, molecular basis governing such enzyme or pathway organization remains elusive. Here we show that Arabidopsis membrane steroid binding proteins (MSBPs) serve as scaffold physically organizing monolignol P450 monooxygenases thereby regulating lignin biosynthetic process. We find that although C4H, C3'H and F5H are in spatial proximity to each other on ER membrane in vivo, they do not appear to directly interact with each other. Instead, two MSBP proteins physically interact with all three P450 enzymes and, moreover, MSBPs themselves associate as homo- and heteromers on the ER membrane, thereby organizing P450 clusters. Down-regulation of MSBPs does not affect the transcription levels of monolignol biosynthetic P450 genes but substantially impairs the stability and activity of the MSBP-interacting P450 enzymes and, consequently, the lignin deposition, the accumulation of soluble phenolics in monolignol branch but not in flavonoid pathway. Furthermore, our study suggests that MSBP proteins are the essential structural component in ER membrane that physically organize and stabilize the monolignol biosynthetic P450 enzyme complex; thereby, specifically controlling phenylpropanoid-monolignol branch biosynthesis.},

  doi          = {10.1038/s41477-018-0142-9},

  journal      = {Nature Plants},

  number       = 5,

  volume       = 4,

  place        = {United States},

  year         = {2018},

  month        = {4}

}

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DOI: 10.1038/s41477-018-0142-9

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Works referenced in this record:

Lignin Biosynthesis
journal, June 2003

Boerjan, Wout; Ralph, John; Baucher, Marie
Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546
DOI: 10.1146/annurev.arplant.54.031902.134938

GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002

Karimi, Mansour; Inzé, Dirk; Depicker, Ann
Trends in Plant Science, Vol. 7, Issue 5, p. 193-195
DOI: 10.1016/S1360-1385(02)02251-3

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Title: The scaffold proteins of lignin biosynthetic cytochrome P450 enzymes

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