Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus

Abstract

Background: The development of fast-growing hardwood trees as a source of lignocellulosic biomass for biofuel and biomaterial production requires a thorough understanding of the plant cell wall structure and function that underlie the inherent recalcitrance properties of woody biomass. Downregulation of GAUT12.1 in Populus deltoides was recently reported to result in improved biomass saccharification, plant growth, and biomass yield. To further understand GAUT12.1 function in biomass recalcitrance and plant growth, here we report the effects of P. trichocarpa GAUT12.1 overexpression in P. deltoides.Results: Increasing GAUT12.1 transcript expression by 7–49% in P. deltoides PtGAUT12.1-overexpression (OE) lines resulted in a nearly complete opposite biomass saccharification and plant growth phenotype to that observed previously in PdGAUT12.1-knockdown (KD) lines. This included significantly reduced glucose, xylose, and total sugar release (12–13%), plant height (6–54%), stem diameter (8–40%), and overall total aerial biomass yield (48–61%) in 3-month-old, greenhouse-grown PtGAUT12.1-OE lines compared to controls. Total lignin content was unaffected by the gene overexpression. Importantly, selected PtGAUT12.1-OE lines retained the recalcitrance and growth phenotypes upon growth for 9 months in the greenhouse and 2.8 years in the field. PtGAUT12.1-OE plants had significantly smaller leaves with lower relative water content, and significantly reduced stem wood xylem cell numbers andmore » size. At the cell wall level, xylose and galacturonic acid contents increased markedly in total cell walls as well as in soluble and insoluble cell wall extracts, consistent with increased amounts of xylan and homogalacturonan in the PtGAUT12.1-OE lines. This led to increased cell wall recalcitrance, as manifested by the 9–15% reduced amounts of recovered extractable wall materials and 8–15% greater amounts of final insoluble pellet in the PtGAUT12.1-OE lines compared to controls.Conclusions: The combined phenotype and chemotype data from P. deltoides PtGAUT12.1-OE and PdGAUT12.1-KD transgenics clearly establish GAUT12.1 as a recalcitrance- and growth-associated gene in poplar. Overall, the data support the hypothesis that GAUT12.1 synthesizes either an HG-containing primer for xylan synthesis or an HG glycan required for proper xylan deposition, anchoring, and/or architecture in the wall, and the possibility of HG and xylan glycans being connected to each other by a base-sensitive covalent linkage.« less

Authors:
 [1];  [1];  [2];  [1];  [3];  [4];  [4];  [5];  [5];  [1];  [5];  [6];  [7];  [8];  [9]; ORCiD logo [9]; ORCiD logo [9];  [10];  [1]
+ Show Author Affiliations
  1. Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology and Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  2. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Mascoma LLC (Lallemand Inc.), Lebanon, NH (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC) and Bioscience Division
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); ArborGen, Inc., Ridgeville, SC (United States)
  5. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  6. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); South Georgia State College, Douglas, GA (United States)
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Nuclear Materials Science
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States); Nu Mark LLC, Richmond, VA (United States)
  9. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States)
  10. Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology and Dept. of Plant Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); BioEnergy Science Center (BESC); National Science Foundation (NSF)
OSTI Identifier:
1422869
Alternate Identifier(s):
OSTI ID: 1468032
Report Number(s):
NREL/JA-2700-70640
Journal ID: ISSN 1754-6834
Grant/Contract Number:  
AC36-08GO28308; PS02-06ER64304; SC0015662; DBI-0421683; IOS-0923992; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; plant cell wall; biofuel; biomass; pectin; xylan; yield

Citation Formats

Biswal, Ajaya K., Atmodjo, Melani A., Pattathil, Sivakumar, Amos, Robert A., Yang, Xiaohan, Winkeler, Kim, Collins, Cassandra, Mohanty, Sushree S., Ryno, David, Tan, Li, Gelineo-Albersheim, Ivana, Hunt, Kimberly, Sykes, Robert W., Turner, Geoffrey B., Ziebell, Angela, Davis, Mark F., Decker, Stephen R., Hahn, Michael G., and Mohnen, Debra. Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus. United States: N. p., 2018. Web. doi:10.1186/s13068-017-1002-y.
Copy to clipboard
Biswal, Ajaya K., Atmodjo, Melani A., Pattathil, Sivakumar, Amos, Robert A., Yang, Xiaohan, Winkeler, Kim, Collins, Cassandra, Mohanty, Sushree S., Ryno, David, Tan, Li, Gelineo-Albersheim, Ivana, Hunt, Kimberly, Sykes, Robert W., Turner, Geoffrey B., Ziebell, Angela, Davis, Mark F., Decker, Stephen R., Hahn, Michael G., & Mohnen, Debra. Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus. United States. https://doi.org/10.1186/s13068-017-1002-y
Copy to clipboard
Biswal, Ajaya K., Atmodjo, Melani A., Pattathil, Sivakumar, Amos, Robert A., Yang, Xiaohan, Winkeler, Kim, Collins, Cassandra, Mohanty, Sushree S., Ryno, David, Tan, Li, Gelineo-Albersheim, Ivana, Hunt, Kimberly, Sykes, Robert W., Turner, Geoffrey B., Ziebell, Angela, Davis, Mark F., Decker, Stephen R., Hahn, Michael G., and Mohnen, Debra. Wed . "Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus". United States. https://doi.org/10.1186/s13068-017-1002-y. https://www.osti.gov/servlets/purl/1422869.
Copy to clipboard
@article{osti_1422869,
title = {Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus},
author = {Biswal, Ajaya K. and Atmodjo, Melani A. and Pattathil, Sivakumar and Amos, Robert A. and Yang, Xiaohan and Winkeler, Kim and Collins, Cassandra and Mohanty, Sushree S. and Ryno, David and Tan, Li and Gelineo-Albersheim, Ivana and Hunt, Kimberly and Sykes, Robert W. and Turner, Geoffrey B. and Ziebell, Angela and Davis, Mark F. and Decker, Stephen R. and Hahn, Michael G. and Mohnen, Debra},
abstractNote = {Background: The development of fast-growing hardwood trees as a source of lignocellulosic biomass for biofuel and biomaterial production requires a thorough understanding of the plant cell wall structure and function that underlie the inherent recalcitrance properties of woody biomass. Downregulation of GAUT12.1 in Populus deltoides was recently reported to result in improved biomass saccharification, plant growth, and biomass yield. To further understand GAUT12.1 function in biomass recalcitrance and plant growth, here we report the effects of P. trichocarpa GAUT12.1 overexpression in P. deltoides.Results: Increasing GAUT12.1 transcript expression by 7–49% in P. deltoides PtGAUT12.1-overexpression (OE) lines resulted in a nearly complete opposite biomass saccharification and plant growth phenotype to that observed previously in PdGAUT12.1-knockdown (KD) lines. This included significantly reduced glucose, xylose, and total sugar release (12–13%), plant height (6–54%), stem diameter (8–40%), and overall total aerial biomass yield (48–61%) in 3-month-old, greenhouse-grown PtGAUT12.1-OE lines compared to controls. Total lignin content was unaffected by the gene overexpression. Importantly, selected PtGAUT12.1-OE lines retained the recalcitrance and growth phenotypes upon growth for 9 months in the greenhouse and 2.8 years in the field. PtGAUT12.1-OE plants had significantly smaller leaves with lower relative water content, and significantly reduced stem wood xylem cell numbers and size. At the cell wall level, xylose and galacturonic acid contents increased markedly in total cell walls as well as in soluble and insoluble cell wall extracts, consistent with increased amounts of xylan and homogalacturonan in the PtGAUT12.1-OE lines. This led to increased cell wall recalcitrance, as manifested by the 9–15% reduced amounts of recovered extractable wall materials and 8–15% greater amounts of final insoluble pellet in the PtGAUT12.1-OE lines compared to controls.Conclusions: The combined phenotype and chemotype data from P. deltoides PtGAUT12.1-OE and PdGAUT12.1-KD transgenics clearly establish GAUT12.1 as a recalcitrance- and growth-associated gene in poplar. Overall, the data support the hypothesis that GAUT12.1 synthesizes either an HG-containing primer for xylan synthesis or an HG glycan required for proper xylan deposition, anchoring, and/or architecture in the wall, and the possibility of HG and xylan glycans being connected to each other by a base-sensitive covalent linkage.},
doi = {10.1186/s13068-017-1002-y},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 11,
place = {United States},
year = {2018},
month = {1}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13068-017-1002-y
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
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:

Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls
journal, September 2015

  • Wang, Tuo; Hong, Mei
  • Journal of Experimental Botany, Vol. 67, Issue 2
  • DOI: 10.1093/jxb/erv416

Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis
journal, February 2018

  • Biswal, Ajaya K.; Atmodjo, Melani A.; Li, Mi
  • Nature Biotechnology, Vol. 36, Issue 3
  • DOI: 10.1038/nbt.4067

Automated Synthesis of Arabinoxylan-Oligosaccharides Enables Characterization of Antibodies that Recognize Plant Cell Wall Glycans
journal, February 2015

  • Schmidt, Deborah; Schuhmacher, Frank; Geissner, Andreas
  • Chemistry - A European Journal, Vol. 21, Issue 15
  • DOI: 10.1002/chem.201500065

A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies
journal, April 2010

  • Pattathil, S.; Avci, U.; Baldwin, D.
  • Plant Physiology, Vol. 153, Issue 2, p. 514-525
  • DOI: 10.1104/pp.109.151985

Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing
journal, January 2017

  • Mizrachi, Eshchar; Verbeke, Lieven; Christie, Nanette
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
  • DOI: 10.1073/pnas.1620119114

A transcriptional roadmap to wood formation
journal, November 2001

  • Hertzberg, M.; Aspeborg, H.; Schrader, J.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 25
  • DOI: 10.1073/pnas.261293398

Plant Physiology
journal, January 1949

  • Metcalfe, C. R.; Went, F. W.
  • Kew Bulletin, Vol. 4, Issue 4
  • DOI: 10.2307/4109069

Pectin Methyl Esterase Inhibits Intrusive and Symplastic Cell Growth in Developing Wood Cells of Populus
journal, December 2007

  • Siedlecka, Anna; Wiklund, Susanne; Péronne, Marie-Amélie
  • Plant Physiology, Vol. 146, Issue 2
  • DOI: 10.1104/pp.107.111963

Arabidopsis irregular xylem8 and irregular xylem9 : Implications for the Complexity of Glucuronoxylan Biosynthesis
journal, February 2007

Immunological Approaches to Biomass Characterization and Utilization
journal, October 2015

  • Pattathil, Sivakumar; Avci, Utku; Zhang, Tiantian
  • Frontiers in Bioengineering and Biotechnology, Vol. 3
  • DOI: 10.3389/fbioe.2015.00173

Engineering of plants with improved properties as biofuels feedstocks by vessel-specific complementation of xylan biosynthesis mutants
journal, January 2012

  • Petersen, Pia Damm; Lau, Jane; Ebert, Berit
  • Biotechnology for Biofuels, Vol. 5, Issue 1, Article No. 84
  • DOI: 10.1186/1754-6834-5-84

Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007

  • Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
  • Science, Vol. 315, Issue 5813, p. 804-807
  • DOI: 10.1126/science.1137016

The irregular xylem9 Mutant is Deficient in Xylan Xylosyltransferase Activity
journal, September 2007

  • Lee, C.; O'Neill, M. A.; Tsumuraya, Y.
  • Plant and Cell Physiology, Vol. 48, Issue 11
  • DOI: 10.1093/pcp/pcm135

Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence
journal, July 2013

  • Gatlin, Delbert M.; Santander, Javier; Loh, Amanda
  • Microbiology, Vol. 159, Issue 7
  • DOI: 10.1099/mic.0.066639-0

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

How biotech can transform biofuels
journal, February 2008

  • Lynd, Lee R.; Laser, Mark S.; Bransby, David
  • Nature Biotechnology, Vol. 26, Issue 2, p. 169-172
  • DOI: 10.1038/nbt0208-169

Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis
journal, December 2007

Comparison of four glycosyl residue composition methods for effectiveness in detecting sugars from cell walls of dicot and grass tissues
journal, July 2017

Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7
journal, August 2003

How could forest trees play an important role as feedstock for bioenergy production?
journal, March 2011

High-Throughput Screening Techniques for Biomass Conversion
journal, October 2009

Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance
journal, June 2015

  • Wang, Tuo; Park, Yong Bum; Cosgrove, Daniel J.
  • Plant Physiology, Vol. 168, Issue 3
  • DOI: 10.1104/pp.15.00665

Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014

  • Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
  • Science, Vol. 344, Issue 6185, p. 1246843-1246843
  • DOI: 10.1126/science.1246843

The structure of Cryptococcus neoformans galactoxylomannan contains β-d-glucuronic acid
journal, May 2009

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
  • DOI: 10.1104/pp.104.055087

A Synthetic Glycan Microarray Enables Epitope Mapping of Plant Cell Wall Glycan-Directed Antibodies
journal, September 2017

  • Ruprecht, Colin; Bartetzko, Max P.; Senf, Deborah
  • Plant Physiology, Vol. 175, Issue 3
  • DOI: 10.1104/pp.17.00737

Arabidopsis thaliana T-DNA Mutants Implicate GAUT Genes in the Biosynthesis of Pectin and Xylan in Cell Walls and Seed Testa
journal, September 2009

  • Caffall, Kerry H.; Pattathil, Sivakumar; Phillips, Sarah E.
  • Molecular Plant, Vol. 2, Issue 5
  • DOI: 10.1093/mp/ssp062

Molecular characterization of the pyrolysis of biomass
journal, March 1987

Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics
journal, June 2005

  • Brown, David M.; Zeef, Leo A. H.; Ellis, Joanne
  • The Plant Cell, Vol. 17, Issue 8
  • DOI: 10.1105/tpc.105.031542

Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex
journal, November 2011

  • Atmodjo, M. A.; Sakuragi, Y.; Zhu, X.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
  • DOI: 10.1073/pnas.1112816108

The Arabidopsis irregular xylem8 Mutant Is Deficient in Glucuronoxylan and Homogalacturonan, Which Are Essential for Secondary Cell Wall Integrity
journal, January 2007

  • Persson, Staffan; Caffall, Kerry Hosmer; Freshour, Glenn
  • The Plant Cell, Vol. 19, Issue 1
  • DOI: 10.1105/tpc.106.047720

An Arabidopsis Cell Wall Proteoglycan Consists of Pectin and Arabinoxylan Covalently Linked to an Arabinogalactan Protein
journal, January 2013

  • Tan, Li; Eberhard, Stefan; Pattathil, Sivakumar
  • The Plant Cell, Vol. 25, Issue 1
  • DOI: 10.1105/tpc.112.107334

MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

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

Molecular Characterization of PoGT8D and PoGT43B, Two Secondary Wall-Associated Glycosyltransferases in Poplar
journal, March 2007

  • Zhou, G. -K.; Zhong, R.; Himmelsbach, D. S.
  • Plant and Cell Physiology, Vol. 48, Issue 5
  • DOI: 10.1093/pcp/pcm037

Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase
journal, March 2006

  • Sterling, J. D.; Atmodjo, M. A.; Inwood, S. E.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 13, p. 5236-5241
  • DOI: 10.1073/pnas.0600120103

Plant Physiology.
journal, January 1980

  • Davis, Robert F.; Bidwell, R. G. S.
  • Bulletin of the Torrey Botanical Club, Vol. 107, Issue 1
  • DOI: 10.2307/2484859

Cellulose factories: advancing bioenergy production from forest trees
journal, November 2011

Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets
journal, June 2005

  • Persson, S.; Wei, H.; Milne, J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 24
  • DOI: 10.1073/pnas.0503392102

Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties
journal, June 2008

    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

    Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
    journal, April 2019

    • Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David
    • New Phytologist, Vol. 223, Issue 1
    • DOI: 10.1111/nph.15777

    Rhamnogalacturonan‐I is a determinant of cell–cell adhesion in poplar wood
    journal, October 2019

    • Yang, Haibing; Benatti, Matheus R.; Karve, Rucha A.
    • Plant Biotechnology Journal, Vol. 18, Issue 4
    • DOI: 10.1111/pbi.13271

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

    A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex
    journal, October 2018

    • Amos, Robert A.; Pattathil, Sivakumar; Yang, Jeong-Yeh
    • Journal of Biological Chemistry, Vol. 293, Issue 49
    • DOI: 10.1074/jbc.ra118.004463
      Sort by:
      [ × clear filter / sort ]

      Similar Records in DOE PAGES and OSTI.GOV collections:

      Other research related to this record: