Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis

Biswal, Ajaya K.; Atmodjo, Melani A.; Li, Mi; Baxter, Holly L.; Yoo, Chang Geun; Pu, Yunqiao; Lee, Yi-Ching; Mazarei, Mitra; Black, Ian M.; Zhang, Ji-Yi; Ramanna, Hema; Bray, Adam L.; King, Zachary R.; LaFayette, Peter R.; Pattathil, Sivakumar; Donohoe, Bryon S.; Mohanty, Sushree S.; Ryno, David; Yee, Kelsey; Thompson, Olivia A.; Rodriguez, Miguel; Dumitrache, Alexandru; Natzke, Jace; Winkeler, Kim; Collins, Cassandra; Yang, Xiaohan; Tan, Li; Sykes, Robert W.; Gjersing, Erica L.; Ziebell, Angela; Turner, Geoffrey B.; Decker, Stephen R.; Hahn, Michael G.; Davison, Brian H.; Udvardi, Michael K.; Mielenz, Jonathan R.; Davis, Mark F.; Nelson, Richard S.; Parrott, Wayne A.; Ragauskas, Arthur J.; Neal Stewart, C.; Mohnen, Debra

doi:10.1038/nbt.4067

Title: Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis

Journal Article · Mon Feb 12 00:00:00 EST 2018 · Nature Biotechnology

DOI:https://doi.org/10.1038/nbt.4067· OSTI ID:1460184

Biswal, Ajaya K. ^[1];

^[1];

^[2]; Baxter, Holly L. ^[3]; Yoo, Chang Geun ^[2];

^[2]; Lee, Yi-Ching ^[4]; Mazarei, Mitra ^[3]; Black, Ian M. ^[5]; Zhang, Ji-Yi ^[4]; Ramanna, Hema ^[4]; Bray, Adam L. ^[6]; King, Zachary R. ^[6]; LaFayette, Peter R. ^[6]; Pattathil, Sivakumar ^[1];

^[7]; Mohanty, Sushree S. ^[1]; Ryno, David ^[1]; Yee, Kelsey ^[8]; Thompson, Olivia A. ^[8] more »

Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC). Biosciences Division; UT-ORNL Joint Inst. for Biological Sciences, Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Plant Sciences
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); Noble Research Inst., Ardmore, OK (United States)
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); Univ. of Georgia, Athens, GA (United States). Inst. of Plant Breeding, Genetics and Genomics
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC). Biosciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); ArborGen, Inc., Ridgeville, SC (United States)
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center. Dept. of Plant Biology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC). Biosciences Division; UT-ORNL Joint Inst. for Biological Sciences, Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering. Dept. of Forestry, Wildlife, and Fisheries

Cell walls in crops and trees have been engineered for production of biofuels and commodity chemicals, but engineered varieties often fail multi-year field trials and are not commercialized. In this paper, we engineered reduced expression of a pectin biosynthesis gene (Galacturonosyltransferase 4, GAUT4) in switchgrass and poplar, and find that this improves biomass yields and sugar release from biomass processing. Both traits were maintained in a 3-year field trial of GAUT4-knockdown switchgrass, with up to sevenfold increased saccharification and ethanol production and sixfold increased biomass yield compared with control plants. We show that GAUT4 is an α-1,4-galacturonosyltransferase that synthesizes homogalacturonan (HG). Downregulation of GAUT4 reduces HG and rhamnogalacturonan II (RGII), reduces wall calcium and boron, and increases extractability of cell wall sugars. Finally, decreased recalcitrance in biomass processing and increased growth are likely due to reduced HG and RGII cross-linking in the cell wall.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)

Grant/Contract Number:: AC05-00OR22725; SC0015662; DBI-0421683; IOS-0923992

OSTI ID:: 1460184

Journal Information:: Nature Biotechnology, Vol. 36, Issue 3; ISSN 1087-0156

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 102 works

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Expression profiles of cell-wall related genes vary broadly between two common maize inbreds during stem development Penning, Bryan W.; Shiga, Tânia M.; Klimek, John F. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6117-z	journal	October 2019
Overexpression of a rice BAHD acyltransferase gene in switchgrass (Panicum virgatum L.) enhances saccharification Li, Guotian; Jones, Kyle C.; Eudes, Aymerick BMC Biotechnology, Vol. 18, Issue 1 https://doi.org/10.1186/s12896-018-0464-8	journal	September 2018
Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus Biswal, Ajaya K.; Atmodjo, Melani A.; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-017-1002-y	journal	January 2018
Switchgrass (Panicum virgatum L.) promoters for green tissue-specific expression of the MYB4 transcription factor for reduced-recalcitrance transgenic switchgrass Liu, Wusheng; Mazarei, Mitra; Ye, Rongjian Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1119-7	journal	April 2018
Desirable plant cell wall traits for higher-quality miscanthus lignocellulosic biomass da Costa, Ricardo M. F.; Pattathil, Sivakumar; Avci, Utku Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1426-7	journal	April 2019
Embryogenic cell suspensions for high-capacity genetic transformation and regeneration of switchgrass (Panicum virgatum L.) Ondzighi-Assoume, Christine A.; Willis, Jonathan D.; Ouma, Wilson K. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1632-3	journal	December 2019
Use of the lignocellulose-degrading bacterium Caldicellulosiruptor bescii to assess recalcitrance and conversion of wild-type and transgenic poplar Straub, Christopher T.; Bing, Ryan G.; Wang, Jack P. Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01675-2	journal	March 2020
High Throughput Screening Technologies in Biomass Characterization Decker, Stephen R.; Harman-Ware, Anne E.; Happs, Renee M. Frontiers in Energy Research, Vol. 6 https://doi.org/10.3389/fenrg.2018.00120	journal	November 2018
Functional Analysis of Cellulose Synthase CesA4 and CesA6 Genes in Switchgrass (Panicum virgatum) by Overexpression and RNAi-Mediated Gene Silencing Mazarei, Mitra; Baxter, Holly L.; Li, Mi Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01114	journal	August 2018
Engineering Non-cellulosic Polysaccharides of Wood for the Biorefinery Donev, Evgeniy; Gandla, Madhavi Latha; Jönsson, Leif J. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01537	journal	October 2018
Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression Amos, Robert A.; Mohnen, Debra Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00915	journal	July 2019
Analytical Enzymatic Saccharification of Lignocellulosic Biomass for Conversion to Biofuels and Bio-Based Chemicals Gandla, Madhavi; Martín, Carlos; Jönsson, Leif Energies, Vol. 11, Issue 11 https://doi.org/10.3390/en11112936	journal	October 2018
The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs) Wormit, Alexandra; Usadel, Björn International Journal of Molecular Sciences, Vol. 19, Issue 10 https://doi.org/10.3390/ijms19102878	journal	September 2018
Rhamnogalacturonan‐I is a determinant of cell–cell adhesion in poplar wood Yang, Haibing; Benatti, Matheus R.; Karve, Rucha A. Plant Biotechnology Journal, Vol. 18, Issue 4 https://doi.org/10.1111/pbi.13271	journal	October 2019
The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs) Wormit, Alexandra; Usadel, Björn RWTH Aachen University https://doi.org/10.18154/rwth-2018-230481	text	January 2018
Brassinosteroid overproduction improves lignocellulose quantity and quality to maximize bioethanol yield under green-like biomass process in transgenic poplar Fan, Chunfen; Yu, Hua; Qin, Shifei Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-1652-z	journal	January 2020
Co-evolution of Enzymes Involved in Plant Cell Wall Metabolism in the Grasses Bulone, Vincent; Schwerdt, Julian G.; Fincher, Geoffrey B. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01009	journal	August 2019
Engineering of Bioenergy Crops: Dominant Genetic Approaches to Improve Polysaccharide Properties and Composition in Biomass Brandon, Andrew G.; Scheller, Henrik V. Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00282	journal	March 2020

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Related Subjects

09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
biofuels
field trials
molecular engineering in plants