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Title: Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility

Abstract

Plant biomass is a large source of fermentable sugars for the synthesis of bioproducts using engineered microbes. These sugars are stored as cell wall polymers, mainly cellulose and hemicellulose, and are embedded with lignin, which makes their enzymatic hydrolysis challenging. One of the strategies to reduce cell wall recalcitrance is the modification of lignin content and composition. Lignin is a phenolic polymer of methylated aromatic alcohols and its synthesis in tissues developing secondary cell walls is a significant sink for the consumption of the methyl donor S-adenosylmethionine (AdoMet). In this study, we demonstrate in Arabidopsis stems that targeted expression of AdoMet hydrolase (AdoMetase, E.C. 3.3.1.2) in secondary cell wall synthesizing tissues reduces the AdoMet pool and impacts lignin content and composition. In particular, both NMR analysis and pyrolysis gas chromatography mass spectrometry of lignin in engineered biomass showed relative enrichment of non-methylated p-hydroxycinnamyl (H) units and a reduction of dimethylated syringyl (S) units. This indicates a lower degree of methylation compared to that in wild-type lignin. Quantification of cell wall-bound hydroxycinnamates revealed a reduction of ferulate in AdoMetase transgenic lines. Biomass from transgenic lines, in contrast to that in control plants, exhibits an enrichment of glucose content and a reductionmore » in the degree of hemicellulose glucuronoxylan methylation. We also show that these modifications resulted in a reduction of cell wall recalcitrance, because sugar yield generated by enzymatic biomass saccharification was greater than that of wild-type plants. Considering that transgenic plants show no important diminution of biomass yields, and that heterologous expression of AdoMetase protein can be spatiotemporally optimized, this novel approach provides a valuable option for the improvement of lignocellulosic biomass feedstock.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [1];  [2];  [1];  [4];  [1];  [2];  [5];  [6]
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering, Dept. of Chemical and Biomolecular Engineering
  3. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering, Dept. of Chemical and Biomolecular Engineering; Univ. of Louisville, KY (United States). Dept. of Chemical Engineering
  4. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  5. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  6. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Claude Bernard Uni., Villeurbanne (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1378985
Grant/Contract Number:  
AC02-05CH11231; 1355438
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Volume: 4; Journal ID: ISSN 2296-4185
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 09 BIOMASS FUELS; cell wall; lignin; S-adenosylmethionine; AdoMetase; Yang cycle; glucuronoxylan; saccharification

Citation Formats

Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., and Loqué, Dominique. Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility. United States: N. p., 2016. Web. doi:10.3389/fbioe.2016.00058.
Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., & Loqué, Dominique. Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility. United States. https://doi.org/10.3389/fbioe.2016.00058
Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., and Loqué, Dominique. 2016. "Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility". United States. https://doi.org/10.3389/fbioe.2016.00058. https://www.osti.gov/servlets/purl/1378985.
@article{osti_1378985,
title = {Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility},
author = {Eudes, Aymerick and Zhao, Nanxia and Sathitsuksanoh, Noppadon and Baidoo, Edward E. K. and Lao, Jeemeng and Wang, George and Yogiswara, Sasha and Lee, Taek Soon and Singh, Seema and Mortimer, Jenny C. and Keasling, Jay D. and Simmons, Blake A. and Loqué, Dominique},
abstractNote = {Plant biomass is a large source of fermentable sugars for the synthesis of bioproducts using engineered microbes. These sugars are stored as cell wall polymers, mainly cellulose and hemicellulose, and are embedded with lignin, which makes their enzymatic hydrolysis challenging. One of the strategies to reduce cell wall recalcitrance is the modification of lignin content and composition. Lignin is a phenolic polymer of methylated aromatic alcohols and its synthesis in tissues developing secondary cell walls is a significant sink for the consumption of the methyl donor S-adenosylmethionine (AdoMet). In this study, we demonstrate in Arabidopsis stems that targeted expression of AdoMet hydrolase (AdoMetase, E.C. 3.3.1.2) in secondary cell wall synthesizing tissues reduces the AdoMet pool and impacts lignin content and composition. In particular, both NMR analysis and pyrolysis gas chromatography mass spectrometry of lignin in engineered biomass showed relative enrichment of non-methylated p-hydroxycinnamyl (H) units and a reduction of dimethylated syringyl (S) units. This indicates a lower degree of methylation compared to that in wild-type lignin. Quantification of cell wall-bound hydroxycinnamates revealed a reduction of ferulate in AdoMetase transgenic lines. Biomass from transgenic lines, in contrast to that in control plants, exhibits an enrichment of glucose content and a reduction in the degree of hemicellulose glucuronoxylan methylation. We also show that these modifications resulted in a reduction of cell wall recalcitrance, because sugar yield generated by enzymatic biomass saccharification was greater than that of wild-type plants. Considering that transgenic plants show no important diminution of biomass yields, and that heterologous expression of AdoMetase protein can be spatiotemporally optimized, this novel approach provides a valuable option for the improvement of lignocellulosic biomass feedstock.},
doi = {10.3389/fbioe.2016.00058},
url = {https://www.osti.gov/biblio/1378985}, journal = {Frontiers in Bioengineering and Biotechnology},
issn = {2296-4185},
number = ,
volume = 4,
place = {United States},
year = {2016},
month = {7}
}

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