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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 Laboratory (NREL), Golden, CO (United States); Oak Ridge National Laboratory (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.
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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
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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.
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@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 = {Wed Jan 17 00:00:00 EST 2018},
month = {Wed Jan 17 00:00:00 EST 2018}
}
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The structure of Cryptococcus neoformans galactoxylomannan contains β-d-glucuronic acid
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How could forest trees play an important role as feedstock for bioenergy production?
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Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties
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Molecular characterization of the pyrolysis of biomass
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How biotech can transform biofuels
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Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase
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Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing
journal, January 2017

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  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 5
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A transcriptional roadmap to wood formation
journal, November 2001

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  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 25
  • DOI: 10.1073/pnas.261293398

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

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  • Journal of Experimental Botany, Vol. 67, Issue 2
  • DOI: 10.1093/jxb/erv416

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
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Molecular Dissection of Xylan Biosynthesis during Wood Formation in Poplar
journal, July 2011

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

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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

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

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

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

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

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

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

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

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

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

    Xylan in the Middle: Understanding Xylan Biosynthesis and Its Metabolic Dependencies Toward Improving Wood Fiber for Industrial Processing
    journal, February 2019

    • Wierzbicki, Martin P.; Maloney, Victoria; Mizrachi, Eshchar
    • Frontiers in Plant Science, Vol. 10
    • DOI: 10.3389/fpls.2019.00176
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