Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus
Abstract
Wood is one of the promising bioenergy feedstocks for lignocellulosic biofuel production. Understanding how wood components are synthesized will help us design strategies for better utilization of wood for biofuel production. One of the major wood components is xylan, in which about 10% of xylosyl residues are substituted with glucuronic acid (GlcA) side chains. All the GlcA side chains of xylan in wood of Populus trichocarpa are methylated, which is different from Arabidopsis xylan in which about 60% of GlcA side chains are methylated. Genes responsible for methylation of GlcA side chains in Populus xylan have not been identified. Here, we report genetic and biochemical analyses of four DUF579 domain-containing proteins, PtrGXM1, PtrGXM2, PtrGXM3 and PtrGXM4, from Populus trichocarpa and their roles in GlcA methylation in xylan. The PtrGXM genes were found to be highly expressed in wood-forming cells and their encoded proteins were shown to be localized in the Golgi. When overexpressed in the Arabidopsis gxm1/2/3 triple mutant, PtrGXMs were able to partially complement the mutant phenotypes including defects in glucuronoxylan methyltransferase activity and GlcA methylation in xylan, indicating that PtrGXMs most likely function as glucuronoxylan methyltransferases. Direct evidence was provided by enzymatic analysis of recombinant PtrGXM proteins showingmore »
- Authors:
-
- University of Georgia, Athens, GA (United States)
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
- OSTI Identifier:
- 1904685
- Grant/Contract Number:
- FG02-03ER15415
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; methyltransferases; Arabidopsis thaliana; methylation; wood; recombinant proteins; microsomes; poplars; biosynthesis
Citation Formats
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, and Ye, Zheng-Hua. Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus. United States: N. p., 2014.
Web. doi:10.1371/journal.pone.0087370.
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, & Ye, Zheng-Hua. Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus. United States. https://doi.org/10.1371/journal.pone.0087370
Yuan, Youxi, Teng, Quincy, Zhong, Ruiqin, and Ye, Zheng-Hua. Tue .
"Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus". United States. https://doi.org/10.1371/journal.pone.0087370. https://www.osti.gov/servlets/purl/1904685.
@article{osti_1904685,
title = {Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus},
author = {Yuan, Youxi and Teng, Quincy and Zhong, Ruiqin and Ye, Zheng-Hua},
abstractNote = {Wood is one of the promising bioenergy feedstocks for lignocellulosic biofuel production. Understanding how wood components are synthesized will help us design strategies for better utilization of wood for biofuel production. One of the major wood components is xylan, in which about 10% of xylosyl residues are substituted with glucuronic acid (GlcA) side chains. All the GlcA side chains of xylan in wood of Populus trichocarpa are methylated, which is different from Arabidopsis xylan in which about 60% of GlcA side chains are methylated. Genes responsible for methylation of GlcA side chains in Populus xylan have not been identified. Here, we report genetic and biochemical analyses of four DUF579 domain-containing proteins, PtrGXM1, PtrGXM2, PtrGXM3 and PtrGXM4, from Populus trichocarpa and their roles in GlcA methylation in xylan. The PtrGXM genes were found to be highly expressed in wood-forming cells and their encoded proteins were shown to be localized in the Golgi. When overexpressed in the Arabidopsis gxm1/2/3 triple mutant, PtrGXMs were able to partially complement the mutant phenotypes including defects in glucuronoxylan methyltransferase activity and GlcA methylation in xylan, indicating that PtrGXMs most likely function as glucuronoxylan methyltransferases. Direct evidence was provided by enzymatic analysis of recombinant PtrGXM proteins showing that they possessed a methyltransferase activity capable of transferring the methyl group onto GlcA-substituted xylooligomers. Kinetic analysis showed that PtrGXMs exhibited differential affinities toward the GlcA-substituted xylooligomer acceptor with PtrGXM3 and PtrGXM4 having 10 times higher Km values than PtrGXM1 and PtrGXM2. Together, these findings indicate that PtrGXMs are methyltransferases mediating GlcA methylation in Populus xylan during wood formation.},
doi = {10.1371/journal.pone.0087370},
journal = {PLoS ONE},
number = 2,
volume = 9,
place = {United States},
year = {Tue Feb 11 00:00:00 EST 2014},
month = {Tue Feb 11 00:00:00 EST 2014}
}
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Perturbation of Wood Cellulose Synthesis Causes Pleiotropic Effects in Transgenic Aspen
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Molecular Dissection of Xylan Biosynthesis during Wood Formation in Poplar
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Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29
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The Poplar Glycosyltransferase GT47C is Functionally Conserved with
Arabidopsis Fragile Fiber8
journal, September 2006
- Zhou, Gong-Ke; Zhong, Ruiqin; Richardson, Elizabeth A.
- Plant and Cell Physiology, Vol. 47, Issue 9
Molecular Characterization of PoGT8D and PoGT43B, Two Secondary Wall-Associated Glycosyltransferases in Poplar
journal, March 2007
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The Four Arabidopsis REDUCED WALL ACETYLATION Genes are Expressed in Secondary Wall-Containing Cells and Required for the Acetylation of Xylan
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Arabidopsis GUX Proteins Are Glucuronyltransferases Responsible for the Addition of Glucuronic Acid Side Chains onto Xylan
journal, April 2012
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- Plant and Cell Physiology, Vol. 53, Issue 7
Three Arabidopsis DUF579 Domain-Containing GXM Proteins are Methyltransferases Catalyzing 4-O-Methylation of Glucuronic Acid on Xylan
journal, October 2012
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- Plant and Cell Physiology, Vol. 53, Issue 11
Down-regulation of glycosyltransferase 8D genes in Populus trichocarpa caused reduced mechanical strength and xylan content in wood
journal, February 2011
- Li, Q.; Min, D.; Wang, J. P. -Y.
- Tree Physiology, Vol. 31, Issue 2
Functional Genomic Analysis Supports Conservation of Function Among Cellulose Synthase-Like A Gene Family Members and Suggests Diverse Roles of Mannans in Plants
journal, February 2007
- Liepman, Aaron H.; Nairn, C. Joseph; Willats, William G. T.
- Plant Physiology, Vol. 143, Issue 4
Arabidopsis Fragile Fiber8 , Which Encodes a Putative Glucuronyltransferase, Is Essential for Normal Secondary Wall Synthesis
journal, November 2005
- Zhong, Ruiqin; Peña, Maria J.; Zhou, Gong-Ke
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Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis
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Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
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Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
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- Field, C. B.
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Cellulosic Biofuels
journal, June 2009
- Carroll, Andrew; Somerville, Chris
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Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar
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- Lee, Chanhui; Zhong, Ruiqin; Ye, Zheng-Hua
- Plant Signaling & Behavior, Vol. 7, Issue 3
The poplar PtrWNDs are transcriptional activators of secondary cell wall biosynthesis
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A Genome Wide Association Study of arabinoxylan content in 2-row spring barley grain
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