A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan
Abstract
Wood represents the most abundant biomass produced by plants and one of its major components is acetyl xylan. Acetylation in xylan can occur at O-2 or O-3 of a xylosyl residue, at both O-2 and O-3 of a xylosyl residue, and at O-3 of a xylosyl residue substituted at O-2 with glucuronic acid. Acetyltransferases responsible for the regiospecific acetylation of xylan in tree species have not yet been characterized. Here we report the biochemical characterization of twelve Populus trichocarpa DUF231-containing proteins, named PtrXOATs, for their roles in the regiospecific acetylation of xylan. The PtrXOAT genes were found to be differentially expressed in Populus organs and among them, PtrXOAT1, PtrXOAT2, PtrXOAT9 and PtrXOAT10 exhibited the highest level of expression in stems undergoing wood formation. Activity assays of recombinant proteins demonstrated that all twelve PtrXOAT proteins were able to transfer acetyl groups from acetyl CoA onto a xylohexaose acceptor with PtrXOAT1, PtrXOAT2, PtrXOAT3, PtrXOAT11 and PtrXOAT12 having the highest activity. Structural analysis of the PtrXOAT-catalyzed reaction products using 1H NMR spectroscopy revealed that PtrXOAT1, PtrXAOT2 and PtrXOAT3 mediated 2-O- and 3-O-monoacetylation and 2,3-di-O-acetylation of xylosyl residues and PtrXOAT11 and PtrXOAT12 only catalyzed 2-O- and 3-O-monoacetylation of xylosyl residues. Of the twelve PtrXOATs,more »
- Authors:
-
[1];
- Univ. of Georgia, Athens, GA (United States). Dept. of Plant Biology
- Univ. of Georgia, Athens, GA (United States). Dept. of Chemistry
- Iowa State Univ., Ames, IA (United States)
- Publication Date:
- Research Org.:
- Univ. of Georgia, Athens, GA (United States). Research Foundation, Inc.
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1499881
- Grant/Contract Number:
- FG02-03ER15415
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS
Citation Formats
Zhong, Ruiqin, Cui, Dongtao, Ye, Zheng-Hua, and Zabotina, Olga A. A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan. United States: N. p., 2018.
Web. doi:10.1371/journal.pone.0194532.
Zhong, Ruiqin, Cui, Dongtao, Ye, Zheng-Hua, & Zabotina, Olga A. A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan. United States. https://doi.org/10.1371/journal.pone.0194532
Zhong, Ruiqin, Cui, Dongtao, Ye, Zheng-Hua, and Zabotina, Olga A. Wed .
"A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan". United States. https://doi.org/10.1371/journal.pone.0194532. https://www.osti.gov/servlets/purl/1499881.
@article{osti_1499881,
title = {A group of Populus trichocarpa DUF231 proteins exhibit differential O-acetyltransferase activities toward xylan},
author = {Zhong, Ruiqin and Cui, Dongtao and Ye, Zheng-Hua and Zabotina, Olga A.},
abstractNote = {Wood represents the most abundant biomass produced by plants and one of its major components is acetyl xylan. Acetylation in xylan can occur at O-2 or O-3 of a xylosyl residue, at both O-2 and O-3 of a xylosyl residue, and at O-3 of a xylosyl residue substituted at O-2 with glucuronic acid. Acetyltransferases responsible for the regiospecific acetylation of xylan in tree species have not yet been characterized. Here we report the biochemical characterization of twelve Populus trichocarpa DUF231-containing proteins, named PtrXOATs, for their roles in the regiospecific acetylation of xylan. The PtrXOAT genes were found to be differentially expressed in Populus organs and among them, PtrXOAT1, PtrXOAT2, PtrXOAT9 and PtrXOAT10 exhibited the highest level of expression in stems undergoing wood formation. Activity assays of recombinant proteins demonstrated that all twelve PtrXOAT proteins were able to transfer acetyl groups from acetyl CoA onto a xylohexaose acceptor with PtrXOAT1, PtrXOAT2, PtrXOAT3, PtrXOAT11 and PtrXOAT12 having the highest activity. Structural analysis of the PtrXOAT-catalyzed reaction products using 1H NMR spectroscopy revealed that PtrXOAT1, PtrXAOT2 and PtrXOAT3 mediated 2-O- and 3-O-monoacetylation and 2,3-di-O-acetylation of xylosyl residues and PtrXOAT11 and PtrXOAT12 only catalyzed 2-O- and 3-O-monoacetylation of xylosyl residues. Of the twelve PtrXOATs, only PtrXOAT9 and PtrXOAT10 were capable of transferring acetyl groups onto the O-3 position of 2-O-glucuronic acid-substituted xylosyl residues. Furthermore, when expressed in the Arabidopsis eskimo1 mutant, PtrXOAT1, PtrXAOT2 and PtrXOAT3 were able to rescue the defects in xylan acetylation. Together, these results demonstrate that the twelve PtrXOATs are acetyltransferases with different roles in xylan acetylation in P. trichocarpa.},
doi = {10.1371/journal.pone.0194532},
journal = {PLoS ONE},
number = 4,
volume = 13,
place = {United States},
year = {Wed Apr 04 00:00:00 EDT 2018},
month = {Wed Apr 04 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 14 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen
journal, February 2005
- Aspeborg, Henrik; Schrader, Jarmo; Coutinho, Pedro M.
- Plant Physiology, Vol. 137, Issue 3
Reducing end groups in brich xylan and their alkaline degradation
journal, January 1977
- Johansson, M. H.; Samuelson, O.
- Wood Science and Technology, Vol. 11, Issue 4
Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar
journal, March 2012
- Lee, Chanhui; Zhong, Ruiqin; Ye, Zheng-Hua
- Plant Signaling & Behavior, Vol. 7, Issue 3
Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors
journal, December 2008
- Wilkins, Olivia; Nahal, Hardeep; Foong, Justin
- Plant Physiology, Vol. 149, Issue 2
Structural characterization of the acetylated heteroxylan from the natural hybrid Paulownia elongata/Paulownia fortunei
journal, February 2008
- Gonçalves, Virgínia M. F.; Evtuguin, Dmitry V.; Domingues, M. Rosário M.
- Carbohydrate Research, Vol. 343, Issue 2
Structure of the reducing end-groups in spruce xylan
journal, January 1983
- Andersson, Sven-Ingvar; Samuelson, Olof; Ishihara, Mitsuro
- Carbohydrate Research, Vol. 111, Issue 2
TRICHOME BIREFRINGENCE and Its Homolog AT5G01360 Encode Plant-Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis
journal, April 2010
- Bischoff, Volker; Nita, Silvia; Neumetzler, Lutz
- Plant Physiology, Vol. 153, Issue 2
Identification and Biochemical Characterization of Four Wood-Associated Glucuronoxylan Methyltransferases in Populus
journal, February 2014
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- PLoS ONE, Vol. 9, Issue 2
Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth
journal, February 2016
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- Plant Science, Vol. 243
Dissection of the Transcriptional Program Regulating Secondary Wall Biosynthesis during Wood Formation in Poplar
journal, September 2011
- Zhong, Ruiqin; McCarthy, Ryan L.; Lee, Chanhui
- Plant Physiology, Vol. 157, Issue 3
Molecular control of wood formation in trees
journal, March 2015
- Ye, Zheng-Hua; Zhong, Ruiqin
- Journal of Experimental Botany, Vol. 66, Issue 14
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
- The Plant Cell, Vol. 17, Issue 12
Positional preferences of acetyl esterases from different CE families towards acetylated 4-O-methyl glucuronic acid-substituted xylo-oligosaccharides
journal, January 2015
- Neumüller, Klaus G.; de Souza, Adriana; van Rijn, Jozef
- Biotechnology for Biofuels, Vol. 8, Issue 1
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998
- Field, C. B.
- Science, Vol. 281, Issue 5374
Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa
journal, January 2010
- Dharmawardhana, Palitha; Brunner, Amy M.; Strauss, Steven H.
- BMC Genomics, Vol. 11, Issue 1
Down-Regulation of PoGT47C Expression in Poplar Results in a Reduced Glucuronoxylan Content and an Increased Wood Digestibility by Cellulase
journal, April 2009
- Lee, C.; Teng, Q.; Huang, W.
- Plant and Cell Physiology, Vol. 50, Issue 6
Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa
journal, June 2013
- Lu, S.; Li, Q.; Wei, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
Regiospecific Acetylation of Xylan is Mediated by a Group of DUF231-Containing O-Acetyltransferases
journal, October 2017
- Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng-Hua
- Plant and Cell Physiology, Vol. 58, Issue 12
Molecular Dissection of Xylan Biosynthesis during Wood Formation in Poplar
journal, July 2011
- Lee, Chanhui; Teng, Quincy; Zhong, Ruiqin
- Molecular Plant, Vol. 4, 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
Effect of inhibitory compounds found in biomass hydrolysates on growth and xylose fermentation by a genetically engineered strain of S. cerevisiae
journal, November 2003
- Helle, Steve; Cameron, David; Lam, Janet
- Enzyme and Microbial Technology, Vol. 33, Issue 6
Perturbation of Wood Cellulose Synthesis Causes Pleiotropic Effects in Transgenic Aspen
journal, March 2011
- Joshi, Chandrashekhar P.; Thammannagowda, Shivegowda; Fujino, Takeshi
- Molecular Plant, Vol. 4, Issue 2
Modification of the degree of 4-O-methylation of secondary wall glucuronoxylan
journal, April 2014
- Yuan, Youxi; Teng, Quincy; Lee, Chanhui
- Plant Science, Vol. 219-220
Mutations of Arabidopsis TBL32 and TBL33 Affect Xylan Acetylation and Secondary Wall Deposition
journal, January 2016
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- PLOS ONE, Vol. 11, Issue 1
The Cellulose Synthase Gene Superfamily and Biochemical Functions of Xylem-Specific Cellulose Synthase-Like Genes in Populus trichocarpa
journal, September 2006
- Suzuki, Shiro; Li, Laigeng; Sun, Ying-Hsuan
- Plant Physiology, Vol. 142, Issue 3
Structural differences of xylans affect their interaction with cellulose
journal, May 2007
- Kabel, Mirjam A.; van den Borne, Hein; Vincken, Jean-Paul
- Carbohydrate Polymers, Vol. 69, Issue 1
The Arabidopsis DUF231 Domain-Containing Protein ESK1 Mediates 2-O- and 3-O-Acetylation of Xylosyl Residues in Xylan
journal, May 2013
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- Plant and Cell Physiology, Vol. 54, Issue 7
O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain
journal, November 2011
- Gille, Sascha; de Souza, Amancio; Xiong, Guangyan
- The Plant Cell, Vol. 23, Issue 11
TBL3 and TBL31, Two Arabidopsis DUF231 Domain Proteins, are Required for 3- O -Monoacetylation of Xylan
journal, November 2015
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- Plant and Cell Physiology, Vol. 57, Issue 1
Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification
journal, March 2017
- Pawar, Prashant Mohan-Anupama; Ratke, Christine; Balasubramanian, Vimal K.
- New Phytologist, Vol. 214, Issue 4
Two Arabidopsis proteins synthesize acetylated xylan in vitro
journal, September 2014
- Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A.
- The Plant Journal, Vol. 80, Issue 2
Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation
journal, October 2014
- Zhong, Ruiqin; Ye, Zheng-Hua
- Plant and Cell Physiology, Vol. 56, 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
Cellulosic Biofuels
journal, June 2009
- Carroll, Andrew; Somerville, Chris
- Annual Review of Plant Biology, Vol. 60, Issue 1
Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes
journal, December 2009
- Shi, Rui; Sun, Ying-Hsuan; Li, Quanzi
- Plant and Cell Physiology, Vol. 51, Issue 1
The Poplar GT8E and GT8F Glycosyltransferases are Functional Orthologs of Arabidopsis PARVUS Involved in Glucuronoxylan Biosynthesis
journal, September 2009
- Lee, Chanhui; Teng, Quincy; Huang, Wenlin
- Plant and Cell Physiology, Vol. 50, Issue 11
The impact of cell wall acetylation on corn stover hydrolysis by cellulolytic and xylanolytic enzymes
journal, June 2009
- Selig, Michael J.; Adney, William S.; Himmel, Michael E.
- Cellulose, Vol. 16, Issue 4
CcBLH6, a bell-like homeodomain-containing transcription factor, regulates the fruit lignification pattern
journal, April 2021
- Yan, Chao; Hu, Zhikang; Nie, Ziyan
- Planta, Vol. 253, Issue 5
Recent progress in the chemistry of wood hemicelluloses
journal, January 1967
- Timell, T. E.
- Wood Science and Technology, Vol. 1, Issue 1
Structural characterization of the acetylated heteroxylan from the natural hybrid Paulownia elongata/Paulownia fortunei
journal, February 2008
- Gonçalves, Virgínia M. F.; Evtuguin, Dmitry V.; Domingues, M. Rosário M.
- Carbohydrate Research, Vol. 343, Issue 2
Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth
journal, February 2016
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- Plant Science, Vol. 243
Characterization of acetylated 4-O-methylglucuronoxylan isolated from aspen employing 1H and 13C NMR spectroscopy
journal, December 2000
- Teleman, Anita; Lundqvist, Jon; Tjerneld, Folke
- Carbohydrate Research, Vol. 329, Issue 4
Characterization of O-acetyl-(4-O-methylglucurono)xylan isolated from birch and beech
journal, February 2002
- Teleman, Anita; Tenkanen, Maija; Jacobs, Anna
- Carbohydrate Research, Vol. 337, Issue 4
Characterization of an acetylated heteroxylan from Eucalyptus globulus Labill
journal, March 2003
- Evtuguin, DmitryV.; Tomás, JorgeL.; Silva, ArturM. S.
- Carbohydrate Research, Vol. 338, Issue 7
Effect of acetylation on the material properties of glucuronoxylan from aspen wood
journal, June 2003
- Gröndahl, Maria; Teleman, Anita; Gatenholm, Paul
- Carbohydrate Polymers, Vol. 52, Issue 4
Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa
journal, June 2013
- Lu, S.; Li, Q.; Wei, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
Mechanism of Action of Neisseria gonorrhoeae O -Acetylpeptidoglycan Esterase, an SGNH Serine Esterase
journal, December 2012
- Pfeffer, John M.; Weadge, Joel T.; Clarke, Anthony J.
- Journal of Biological Chemistry, Vol. 288, Issue 4
Molecular control of wood formation in trees
journal, March 2015
- Ye, Zheng-Hua; Zhong, Ruiqin
- Journal of Experimental Botany, Vol. 66, Issue 14
Perturbation of Wood Cellulose Synthesis Causes Pleiotropic Effects in Transgenic Aspen
journal, March 2011
- Joshi, Chandrashekhar P.; Thammannagowda, Shivegowda; Fujino, Takeshi
- Molecular Plant, Vol. 4, Issue 2
Molecular Dissection of Xylan Biosynthesis during Wood Formation in Poplar
journal, July 2011
- Lee, Chanhui; Teng, Quincy; Zhong, Ruiqin
- Molecular Plant, Vol. 4, Issue 4
The Poplar GT8E and GT8F Glycosyltransferases are Functional Orthologs of Arabidopsis PARVUS Involved in Glucuronoxylan Biosynthesis
journal, September 2009
- Lee, Chanhui; Teng, Quincy; Huang, Wenlin
- Plant and Cell Physiology, Vol. 50, Issue 11
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 Arabidopsis DUF231 Domain-Containing Protein ESK1 Mediates 2-O- and 3-O-Acetylation of Xylosyl Residues in Xylan
journal, May 2013
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- Plant and Cell Physiology, Vol. 54, Issue 7
Cytosol-Localized UDP-Xylose Synthases Provide the Major Source of UDP-Xylose for the Biosynthesis of Xylan and Xyloglucan
journal, December 2016
- Zhong, Ruiqin; Teng, Quincy; Haghighat, Marziyeh
- Plant and Cell Physiology
Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors
journal, December 2008
- Wilkins, Olivia; Nahal, Hardeep; Foong, Justin
- Plant Physiology, Vol. 149, Issue 2
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
- The Plant Cell, Vol. 17, Issue 12
O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain
journal, November 2011
- Gille, Sascha; de Souza, Amancio; Xiong, Guangyan
- The Plant Cell, Vol. 23, Issue 11
Downregulation of RWA genes in hybrid aspen affects xylan acetylation and wood saccharification
journal, March 2017
- Pawar, Prashant Mohan-Anupama; Ratke, Christine; Balasubramanian, Vimal K.
- New Phytologist, Vol. 214, Issue 4
Two Arabidopsis proteins synthesize acetylated xylan in vitro
journal, September 2014
- Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A.
- The Plant Journal, Vol. 80, Issue 2
Cellulosic Biofuels
journal, June 2009
- Carroll, Andrew; Somerville, Chris
- Annual Review of Plant Biology, Vol. 60, Issue 1
Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa
journal, January 2010
- Dharmawardhana, Palitha; Brunner, Amy M.; Strauss, Steven H.
- BMC Genomics, Vol. 11, Issue 1
Mutations of Arabidopsis TBL32 and TBL33 Affect Xylan Acetylation and Secondary Wall Deposition
journal, January 2016
- Yuan, Youxi; Teng, Quincy; Zhong, Ruiqin
- PLOS ONE, Vol. 11, Issue 1
Biochemical characterization of xylan xylosyltransferases involved in wood formation in poplar
journal, March 2012
- Lee, Chanhui; Zhong, Ruiqin; Ye, Zheng-Hua
- Plant Signaling & Behavior, Vol. 7, Issue 3
Works referencing / citing this record:
Secondary cell wall biosynthesis
journal, November 2018
- Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
- New Phytologist, Vol. 221, Issue 4
Evolutionary origin of O ‐acetyltransferases responsible for glucomannan acetylation in land plants
journal, June 2019
- Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng‐Hua
- New Phytologist, Vol. 224, Issue 1
Biochemical characterization of rice xylan O-acetyltransferases
journal, March 2018
- Zhong, Ruiqin; Cui, Dongtao; Dasher, Robert L.
- Planta, Vol. 247, Issue 6
Xyloglucan O-acetyltransferases from Arabidopsis thaliana and Populus trichocarpa catalyze acetylation of fucosylated galactose residues on xyloglucan side chains
journal, August 2018
- Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng-Hua
- Planta, Vol. 248, Issue 5
Members of the DUF231 Family are O-Acetyltransferases Catalyzing 2-O- and 3-O-Acetylation of Mannan
journal, August 2018
- Zhong, Ruiqin; Cui, Dongtao; Ye, Zheng-Hua
- Plant and Cell Physiology
Cytosolic Acetyl-CoA Generated by ATP-Citrate Lyase Is Essential for Acetylation of Cell Wall Polysaccharides
journal, September 2019
- Zhong, Ruiqin; Cui, Dongtao; Richardson, Elizabeth A.
- Plant and Cell Physiology, Vol. 61, Issue 1