Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana

Wang, Xin; Zhuo, Chunliu; Xiao, Xirong; Wang, Xiaoqiang; Docampo-Palacios, Maite; Chen, Fang; Dixon, Richard A.

doi:10.1105/tpc.20.00598

Title: Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana

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Abstract

Catechyl lignin (C-lignin) is a linear homopolymer of caffeyl alcohol found in the seed coats of diverse plant species. Its properties make it a natural source of carbon fibers and high-value chemicals, but the mechanism of in planta polymerization of caffeyl alcohol remains unclear. In the ornamental plant Cleome hassleriana, lignin biosynthesis in the seed coat switches from guaiacyl lignin to C-lignin at ~12 d after pollination. Here we found that the transcript profile of the laccase gene ChLAC8 parallels the accumulation of C-lignin during seed coat development. Recombinant ChLAC8 oxidizes caffeyl and sinapyl alcohols, generating their corresponding dimers or trimers in vitro, but cannot oxidize coniferyl alcohol. We propose a basis for this substrate preference based on molecular modeling/docking experiments. Suppression of ChLAC8 expression led to significantly reduced C-lignin content in the seed coats of transgenic Cleome plants. Feeding of ¹³C-caffeyl alcohol to the Arabidopsis (Arabidopsis thaliana) caffeic acid o-methyltransferase mutant resulted in no incorporation of ¹³C into C-lignin, but expressing ChLAC8 in this genetic background led to appearance of C-lignin with >40% label incorporation. These results indicate that ChLAC8 is required for C-lignin polymerization and determines lignin composition when caffeyl alcohol is available.

Authors:

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BioDiscovery Institute and Department of Biological Sciences, University of North Texas, Denton, Texas 76203, Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan 430062, China
BioDiscovery Institute and Department of Biological Sciences, University of North Texas, Denton, Texas 76203, Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
BioDiscovery Institute and Department of Biological Sciences, University of North Texas, Denton, Texas 76203

Publication Date:: Fri Oct 09 00:00:00 EDT 2020

Research Org.:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1671834

Alternate Identifier(s):: OSTI ID: 1785640

Grant/Contract Number:: 1456286; 31770339; 201704910208

Resource Type:: Published Article

Journal Name:: The Plant Cell

Additional Journal Information:: Journal Name: The Plant Cell Journal Volume: 32 Journal Issue: 12; Journal ID: ISSN 1040-4651

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Wang, Xin, Zhuo, Chunliu, Xiao, Xirong, Wang, Xiaoqiang, Docampo-Palacios, Maite, Chen, Fang, and Dixon, Richard A. Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana.  United States: N. p., 2020. 
Web.  doi:10.1105/tpc.20.00598.

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                    Wang, Xin, Zhuo, Chunliu, Xiao, Xirong, Wang, Xiaoqiang, Docampo-Palacios, Maite, Chen, Fang, & Dixon, Richard A. Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana.  United States.  https://doi.org/10.1105/tpc.20.00598

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                    Wang, Xin, Zhuo, Chunliu, Xiao, Xirong, Wang, Xiaoqiang, Docampo-Palacios, Maite, Chen, Fang, and Dixon, Richard A. Fri .  
"Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana".  United States.  https://doi.org/10.1105/tpc.20.00598.

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@article{osti_1671834,

  title        = {Substrate Specificity of LACCASE8 Facilitates Polymerization of Caffeyl Alcohol for C-Lignin Biosynthesis in the Seed Coat of Cleome hassleriana},

  author       = {Wang, Xin and Zhuo, Chunliu and Xiao, Xirong and Wang, Xiaoqiang and Docampo-Palacios, Maite and Chen, Fang and Dixon, Richard A.},

  abstractNote = {Catechyl lignin (C-lignin) is a linear homopolymer of caffeyl alcohol found in the seed coats of diverse plant species. Its properties make it a natural source of carbon fibers and high-value chemicals, but the mechanism of in planta polymerization of caffeyl alcohol remains unclear. In the ornamental plant Cleome hassleriana, lignin biosynthesis in the seed coat switches from guaiacyl lignin to C-lignin at ~12 d after pollination. Here we found that the transcript profile of the laccase gene ChLAC8 parallels the accumulation of C-lignin during seed coat development. Recombinant ChLAC8 oxidizes caffeyl and sinapyl alcohols, generating their corresponding dimers or trimers in vitro, but cannot oxidize coniferyl alcohol. We propose a basis for this substrate preference based on molecular modeling/docking experiments. Suppression of ChLAC8 expression led to significantly reduced C-lignin content in the seed coats of transgenic Cleome plants. Feeding of 13C-caffeyl alcohol to the Arabidopsis (Arabidopsis thaliana) caffeic acid o-methyltransferase mutant resulted in no incorporation of 13C into C-lignin, but expressing ChLAC8 in this genetic background led to appearance of C-lignin with >40% label incorporation. These results indicate that ChLAC8 is required for C-lignin polymerization and determines lignin composition when caffeyl alcohol is available.},

  doi          = {10.1105/tpc.20.00598},

  journal      = {The Plant Cell},

  number       = 12,

  volume       = 32,

  place        = {United States},

  year         = {Fri Oct 09 00:00:00 EDT 2020},

  month        = {Fri Oct 09 00:00:00 EDT 2020}

}

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