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Title: Overexpression of a Domain of Unknown Function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus

Abstract

Background: Domain of Unknown Function 231-containing proteins (DUF231) are plant specific and their function is largely unknown. Studies in the model plants Arabidopsis and rice suggested that some DUF231 proteins act in the process of O-acetyl substitution of hemicellulose and esterification of pectin. However, little is known about the function of DUF231 proteins in woody plant species.Results: This study provides evidence supporting that one member of DUF231 family proteins in the woody perennial plant Populus deltoides (genotype WV94), PdDUF231A, has a role in the acetylation of xylan and affects cellulose biosynthesis. A total of 52 DUF231-containing proteins were identified in the Populus genome. In P. deltoides transgenic lines overexpressing PdDUF231A (OXPdDUF231A), glucose and cellulose contents were increased. Consistent with these results, the transcript levels of cellulose biosynthesis-related genes were increased in the OXPdDUF231A transgenic lines. Furthermore, the relative content of total acetylated xylan was increased in the OXPdDUF231A transgenic lines. Enzymatic saccharification assays revealed that the rate of glucose release increased in OXPdDUF231A transgenic lines. Plant biomass productivity was also increased in OXPdDUF231A transgenic lines.Conclusions: These results suggest that PdDUF231A affects cellulose biosynthesis and plays a role in the acetylation of xylan. PdDUF231A is a promising target for genetic modificationmore » for biofuel production because biomass productivity and compositional quality can be simultaneously improved through overexpression.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1618712
Alternate Identifier(s):
OSTI ID: 1460243; OSTI ID: 1463990
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Name: Biotechnology for Biofuels Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
Springer Science + Business Media
Country of Publication:
Netherlands
Language:
English
Subject:
09 BIOMASS FUELS; Acetylation; Cell wall; Cellulose; DUF231; Populus; Sugar release; Xylan

Citation Formats

Yang, Yongil, Yoo, Chang Geun, Winkeler, Kimberly A., Collins, Cassandra M., Hinchee, Maud A. W., Jawdy, Sara S., Gunter, Lee E., Engle, Nancy L., Pu, Yunqiao, Yang, Xiaohan, Tschaplinski, Timothy J., Ragauskas, Arthur J., Tuskan, Gerald A., and Chen, Jin-Gui. Overexpression of a Domain of Unknown Function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus. Netherlands: N. p., 2017. Web. doi:10.1186/s13068-017-0998-3.
Yang, Yongil, Yoo, Chang Geun, Winkeler, Kimberly A., Collins, Cassandra M., Hinchee, Maud A. W., Jawdy, Sara S., Gunter, Lee E., Engle, Nancy L., Pu, Yunqiao, Yang, Xiaohan, Tschaplinski, Timothy J., Ragauskas, Arthur J., Tuskan, Gerald A., & Chen, Jin-Gui. Overexpression of a Domain of Unknown Function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus. Netherlands. https://doi.org/10.1186/s13068-017-0998-3
Yang, Yongil, Yoo, Chang Geun, Winkeler, Kimberly A., Collins, Cassandra M., Hinchee, Maud A. W., Jawdy, Sara S., Gunter, Lee E., Engle, Nancy L., Pu, Yunqiao, Yang, Xiaohan, Tschaplinski, Timothy J., Ragauskas, Arthur J., Tuskan, Gerald A., and Chen, Jin-Gui. Wed . "Overexpression of a Domain of Unknown Function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus". Netherlands. https://doi.org/10.1186/s13068-017-0998-3.
@article{osti_1618712,
title = {Overexpression of a Domain of Unknown Function 231-containing protein increases O-xylan acetylation and cellulose biosynthesis in Populus},
author = {Yang, Yongil and Yoo, Chang Geun and Winkeler, Kimberly A. and Collins, Cassandra M. and Hinchee, Maud A. W. and Jawdy, Sara S. and Gunter, Lee E. and Engle, Nancy L. and Pu, Yunqiao and Yang, Xiaohan and Tschaplinski, Timothy J. and Ragauskas, Arthur J. and Tuskan, Gerald A. and Chen, Jin-Gui},
abstractNote = {Background: Domain of Unknown Function 231-containing proteins (DUF231) are plant specific and their function is largely unknown. Studies in the model plants Arabidopsis and rice suggested that some DUF231 proteins act in the process of O-acetyl substitution of hemicellulose and esterification of pectin. However, little is known about the function of DUF231 proteins in woody plant species.Results: This study provides evidence supporting that one member of DUF231 family proteins in the woody perennial plant Populus deltoides (genotype WV94), PdDUF231A, has a role in the acetylation of xylan and affects cellulose biosynthesis. A total of 52 DUF231-containing proteins were identified in the Populus genome. In P. deltoides transgenic lines overexpressing PdDUF231A (OXPdDUF231A), glucose and cellulose contents were increased. Consistent with these results, the transcript levels of cellulose biosynthesis-related genes were increased in the OXPdDUF231A transgenic lines. Furthermore, the relative content of total acetylated xylan was increased in the OXPdDUF231A transgenic lines. Enzymatic saccharification assays revealed that the rate of glucose release increased in OXPdDUF231A transgenic lines. Plant biomass productivity was also increased in OXPdDUF231A transgenic lines.Conclusions: These results suggest that PdDUF231A affects cellulose biosynthesis and plays a role in the acetylation of xylan. PdDUF231A is a promising target for genetic modification for biofuel production because biomass productivity and compositional quality can be simultaneously improved through overexpression.},
doi = {10.1186/s13068-017-0998-3},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {Netherlands},
year = {Wed Dec 27 00:00:00 EST 2017},
month = {Wed Dec 27 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13068-017-0998-3

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Cited by: 15 works
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Works referenced in this record:

Involvement of TBL/DUF231 proteins into cell wall biology
journal, August 2010

  • Bischoff, Volker; Selbig, Joachim; Scheible, Wolf-Rüdiger
  • Plant Signaling & Behavior, Vol. 5, Issue 8
  • DOI: 10.4161/psb.5.8.12414

Novel eukaryotic enzymes modifying cell-surface biopolymers
journal, January 2010


Quantitative Analysis of Copy Number Variants Based on Real‐Time LightCycler PCR
journal, January 2014


Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition: PMR5 is required for powdery mildew susceptibility
journal, December 2004


Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009

  • Coleman, H. D.; Yan, J.; Mansfield, S. D.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
  • DOI: 10.1073/pnas.0900188106

New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Roles of Arabidopsis TBL34 and TBL35 in xylan acetylation and plant growth
journal, February 2016


Transcript, protein and metabolite temporal dynamics in the CAM plant Agave
journal, November 2016


The sucrose synthase gene family in Populus: structure, expression, and evolution
journal, October 2010


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

The challenge of enzyme cost in the production of lignocellulosic biofuels
journal, November 2011

  • Klein-Marcuschamer, Daniel; Oleskowicz-Popiel, Piotr; Simmons, Blake A.
  • Biotechnology and Bioengineering, Vol. 109, Issue 4
  • DOI: 10.1002/bit.24370

An update on the nomenclature for the cellulose synthase genes in Populus
journal, May 2009


Identification of a disaccharide side chain 2- O -α-D-galactopyranosyl-α-D-glucuronic acid in Arabidopsis xylan
journal, February 2014

  • Zhong, Ruiqin; Teng, Quincy; Lee, Chanhui
  • Plant Signaling & Behavior, Vol. 9, Issue 2
  • DOI: 10.4161/psb.27933

Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release
journal, April 2016

  • Bryan, Anthony C.; Jawdy, Sara; Gunter, Lee
  • Plant Biotechnology Journal, Vol. 14, Issue 10
  • DOI: 10.1111/pbi.12560

Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae
journal, August 2005


NMR characterization of endogenously O-acetylated oligosaccharides isolated from tomato (Lycopersicon esculentum) xyloglucan
journal, August 2005


Metabolic profiling reveals altered sugar and secondary metabolism in response to UGPase overexpression in Populus
journal, October 2014

  • Payyavula, Raja S.; Tschaplinski, Timothy J.; Jawdy, Sara S.
  • BMC Plant Biology, Vol. 14, Issue 1
  • DOI: 10.1186/s12870-014-0265-8

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
  • DOI: 10.1111/nph.14489

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Cellulose biosynthesis and deposition in higher plants
journal, April 2008


Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles
journal, April 2005


Acetylation of woody lignocellulose: significance and regulation
journal, January 2013

  • Pawar, Prashant Mohan-Anupama; Koutaniemi, Sanna; Tenkanen, Maija
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00118

Loss-of-Function Mutation of REDUCED WALL ACETYLATION2 in Arabidopsis Leads to Reduced Cell Wall Acetylation and Increased Resistance to Botrytis cinerea
journal, January 2011

  • Manabe, Yuzuki; Nafisi, Majse; Verhertbruggen, Yves
  • Plant Physiology, Vol. 155, Issue 3
  • DOI: 10.1104/pp.110.168989

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
  • DOI: 10.1104/pp.110.153320

Two Trichome Birefringence-Like Proteins Mediate Xylan Acetylation, Which Is Essential for Leaf Blight Resistance in Rice
journal, November 2016

  • Gao, Yaping; He, Congwu; Zhang, Dongmei
  • Plant Physiology, Vol. 173, Issue 1
  • DOI: 10.1104/pp.16.01618

Cellulose Synthases and Synthesis in Arabidopsis
journal, March 2011

  • Endler, Anne; Persson, Staffan
  • Molecular Plant, Vol. 4, Issue 2
  • DOI: 10.1093/mp/ssq079

Overexpression of Poplar Xylem Sucrose Synthase in Tobacco Leads to a Thickened Cell Wall and Increased Height
journal, March 2015


Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

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
  • DOI: 10.1093/mp/ssr035

Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5
journal, January 2010

  • Kim, Hoon; Ralph, John
  • Org. Biomol. Chem., Vol. 8, Issue 3
  • DOI: 10.1039/B916070A

Functions of Xyloglucan in Plant Cells
journal, January 2011

  • Hayashi, Takahisa; Kaida, Rumi
  • Molecular Plant, Vol. 4, Issue 1
  • DOI: 10.1093/mp/ssq063

O-Acetylation of Plant Cell Wall Polysaccharides
journal, January 2012


Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase
journal, March 2017


Reduced Wall Acetylation Proteins Play Vital and Distinct Roles in Cell Wall O -Acetylation in Arabidopsis
journal, September 2013

  • Manabe, Yuzuki; Verhertbruggen, Yves; Gille, Sascha
  • Plant Physiology, Vol. 163, Issue 3
  • DOI: 10.1104/pp.113.225193

Down-Regulation of KORRIGAN-Like Endo-β-1,4-Glucanase Genes Impacts Carbon Partitioning, Mycorrhizal Colonization and Biomass Production in Populus
journal, October 2016

  • Kalluri, Udaya C.; Payyavula, Raja S.; Labbé, Jessy L.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.01455

Mutations of Arabidopsis TBL32 and TBL33 Affect Xylan Acetylation and Secondary Wall Deposition
journal, January 2016


Xylan O-Acetylation Impacts Xylem Development and Enzymatic Recalcitrance as Indicated by the Arabidopsis Mutant tbl29
journal, July 2013

  • Xiong, Guangyan; Cheng, Kun; Pauly, Markus
  • Molecular Plant, Vol. 6, Issue 4
  • DOI: 10.1093/mp/sst014

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

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
  • DOI: 10.1105/tpc.111.091728

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
  • DOI: 10.1093/pcp/pct070

Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases
journal, September 2014

  • Jensen, Jacob Krüger; Johnson, Nathan Robert; Wilkerson, Curtis Gene
  • The Plant Journal, Vol. 80, Issue 2
  • DOI: 10.1111/tpj.12641

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
  • DOI: 10.1093/pcp/pcv172

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
  • DOI: 10.1111/tpj.12643

Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012

  • Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
  • Biotechnology for Biofuels, Vol. 5, Issue 1
  • DOI: 10.1186/1754-6834-5-71

Works referencing / citing this record:

A novel FC17/CESA4 mutation causes increased biomass saccharification and lodging resistance by remodeling cell wall in rice
journal, November 2018


A systems genetics analysis in Eucalyptus reveals coordination of metabolic pathways associated with xylan modification in wood‐forming tissues
journal, April 2019

  • Wierzbicki, Martin P.; Christie, Nanette; Pinard, Desré
  • New Phytologist, Vol. 223, Issue 4
  • DOI: 10.1111/nph.15972

Engineering Non-cellulosic Polysaccharides of Wood for the Biorefinery
journal, October 2018

  • Donev, Evgeniy; Gandla, Madhavi Latha; Jönsson, Leif J.
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01537