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 »
- Authors:
-
- Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
- 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
- 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
- Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
- 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)
- 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 Laboratory (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:
- 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. Tue .
"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},
journal = {Frontiers in Bioengineering and Biotechnology},
number = ,
volume = 4,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}
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Works referenced in this record:
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Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy
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- Yelle, Daniel J.; Ralph, John; Frihart, Charles R.
- Magnetic Resonance in Chemistry, Vol. 46, Issue 6
Determination of S-Adenosyl-l-methionine in Fruits by Capillary Electrophoresis
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Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase
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Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis
journal, June 2007
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- Planta, Vol. 226, Issue 5
Lignin bioengineering
journal, April 2014
- Eudes, Aymerick; Liang, Yan; Mitra, Prajakta
- Current Opinion in Biotechnology, Vol. 26
Designer lignins: harnessing the plasticity of lignification
journal, February 2016
- Mottiar, Yaseen; Vanholme, Ruben; Boerjan, Wout
- Current Opinion in Biotechnology, Vol. 37
Modification of the degree of 4-O-methylation of secondary wall glucuronoxylan
journal, April 2014
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- Plant Science, Vol. 219-220
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959
- Miller, G. L.
- Analytical Chemistry, Vol. 31, Issue 3
Pyrolysis-GC-MS characterization of forage materials
journal, August 1991
- Ralph, John; Hatfield, Ronald D.
- Journal of Agricultural and Food Chemistry, Vol. 39, Issue 8
Chemical Composition of Abaca ( Musa textilis ) Leaf Fibers Used for Manufacturing of High Quality Paper Pulps
journal, June 2006
- del Río, José C.; Gutiérrez, Ana
- Journal of Agricultural and Food Chemistry, Vol. 54, Issue 13
Cellular and subcellular localization of the lignin biosynthetic enzymes caffeic acid-O-methyltransferase, cinnamyl alcohol dehydrogenase and cinnamoyl-coenzyme A reductase in two monocots, sugarcane and maize
journal, January 2003
- Ruelland, Eric; Campalans, Anna; Selman-Housein, Guillermo
- Physiologia Plantarum, Vol. 117, Issue 1
Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007
- Chen, Fang; Dixon, Richard A.
- Nature Biotechnology, Vol. 25, Issue 7, p. 759-761
Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012
- Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang
- Nature Protocols, Vol. 7, Issue 9
4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein
journal, August 2012
- Urbanowicz, B. R.; Pena, M. J.; Ratnaparkhe, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms
journal, August 1999
- Osakabe, K.; Tsao, C. C.; Li, L.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 16
5-Hydroxyconiferyl Aldehyde Modulates Enzymatic Methylation for Syringyl Monolignol Formation, a New View of Monolignol Biosynthesis in Angiosperms
journal, February 2000
- Li, Laigeng; Popko, Jacqueline L.; Umezawa, Toshiaki
- Journal of Biological Chemistry, Vol. 275, Issue 9
Efficiency of Lignin Biosynthesis: a Quantitative Analysis
journal, March 2003
- Amthor, J. S.
- Annals of Botany, Vol. 91, Issue 6
Xylem cell death: emerging understanding of regulation and function
journal, January 2012
- Bollhoner, B.; Prestele, J.; Tuominen, H.
- Journal of Experimental Botany, Vol. 63, Issue 3
SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis
journal, November 2012
- Tanz, Sandra K.; Castleden, Ian; Hooper, Cornelia M.
- Nucleic Acids Research, Vol. 41, Issue D1
Thermospermine is Not a Minor Polyamine in the Plant Kingdom
journal, February 2012
- Takano, A.; Kakehi, J. -I.; Takahashi, T.
- Plant and Cell Physiology, Vol. 53, Issue 4
Three Arabidopsis DUF579 Domain-Containing GXM Proteins are Methyltransferases Catalyzing 4-O-Methylation of Glucuronic Acid on Xylan
journal, October 2012
- Lee, C.; Teng, Q.; Zhong, R.
- Plant and Cell Physiology, Vol. 53, Issue 11
The Folylpolyglutamate Synthetase Plastidial Isoform Is Required for Postembryonic Root Development in Arabidopsis
journal, January 2011
- Srivastava, A. C.; Ramos-Parra, P. A.; Bedair, M.
- Plant Physiology, Vol. 155, Issue 3, p. 1237-1251
Downregulation of Caffeic Acid 3- O -Methyltransferase and Caffeoyl CoA 3- O -Methyltransferase in Transgenic Alfalfa: Impacts on Lignin Structure and Implications for the Biosynthesis of G and S Lignin
journal, January 2001
- Guo, Dianjing; Chen, Fang; Inoue, Kentaro
- The Plant Cell, Vol. 13, Issue 1
Engineering secondary cell wall deposition in plants
journal, November 2012
- Yang, Fan; Mitra, Prajakta; Zhang, Ling
- Plant Biotechnology Journal, Vol. 11, Issue 3
Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency
journal, January 2015
- Eudes, Aymerick; Sathitsuksanoh, Noppadon; Baidoo, Edward E. K.
- Plant Biotechnology Journal, Vol. 13, Issue 9
The maize brown midrib2 ( bm2 ) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation
journal, January 2014
- Tang, Ho Man; Liu, Sanzhen; Hill-Skinner, Sarah
- The Plant Journal, Vol. 77, Issue 3
The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase
journal, January 2015
- Li, Li; Hill-Skinner, Sarah; Liu, Sanzhen
- The Plant Journal, Vol. 81, Issue 3, p. 493-504
Hemicelluloses
journal, June 2010
- Scheller, Henrik Vibe; Ulvskov, Peter
- Annual Review of Plant Biology, Vol. 61, Issue 1
O NE -C ARBON M ETABOLISM IN H IGHER P LANTS
journal, June 2001
- Hanson, Andrew D.; Roje, Sanja
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1
Lignin Biosynthesis
journal, June 2003
- Boerjan, Wout; Ralph, John; Baucher, Marie
- Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546
Production of hydroxycinnamoyl anthranilates from glucose in Escherichia coli
journal, January 2013
- Eudes, Aymerick; Juminaga, Darmawi; Baidoo, Edward E. K.
- Microbial Cell Factories, Vol. 12, Issue 1
Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis
journal, December 2015
- Srivastava, Avinash C.; Chen, Fang; Ray, Tui
- Biotechnology for Biofuels, Vol. 8, Article No. 224
Aspartate-Derived Amino Acid Biosynthesis in Arabidopsis thaliana
journal, January 2009
- Jander, Georg; Joshi, Vijay
- The Arabidopsis Book, Vol. 7
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