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

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.
Authors:
 [1] ; ORCiD logo [1] ; ORCiD logo [2] ;  [3] ;  [2] ; ORCiD logo [2] ;  [4] ;  [3] ;  [5] ;  [4] ;  [4] ;  [6] ;  [6] ;  [6] ;  [1] ; ORCiD logo [7] ;  [1] ;  [1] ;  [8] ;  [8] more »;  [8] ;  [8] ;  [8] ;  [9] ;  [9] ; ORCiD logo [8] ;  [1] ;  [7] ;  [7] ;  [7] ;  [7] ; ORCiD logo [7] ; ORCiD logo [10] ;  [8] ;  [4] ;  [8] ; ORCiD logo [7] ;  [4] ;  [6] ;  [11] ;  [3] ;  [1] « less
  1. 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)
  2. 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)
  3. 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
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); Noble Research Inst., Ardmore, OK (United States)
  5. Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  6. 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
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States)
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC). Biosciences Division
  9. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). DOE-BioEnergy Science Center (BESC); ArborGen, Inc., Ridgeville, SC (United States)
  10. 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)
  11. 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
Publication Date:
Grant/Contract Number:
AC05-00OR22725; SC0015662; DBI-0421683; IOS-0923992
Type:
Accepted Manuscript
Journal Name:
Nature Biotechnology
Additional Journal Information:
Journal Volume: 36; Journal Issue: 3; Journal ID: ISSN 1087-0156
Publisher:
Springer Nature
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Georgia, Athens, GA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF)
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; biofuels; field trials; molecular engineering in plants
OSTI Identifier:
1460184

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., and Mohnen, Debra. Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. United States: N. p., Web. doi:10.1038/nbt.4067.
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. Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. United States. doi:10.1038/nbt.4067.
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., and Mohnen, Debra. 2018. "Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis". United States. doi:10.1038/nbt.4067.
@article{osti_1460184,
title = {Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis},
author = {Biswal, Ajaya K. and Atmodjo, Melani A. and Li, Mi and Baxter, Holly L. and Yoo, Chang Geun and Pu, Yunqiao and Lee, Yi-Ching and Mazarei, Mitra and Black, Ian M. and Zhang, Ji-Yi and Ramanna, Hema and Bray, Adam L. and King, Zachary R. and LaFayette, Peter R. and Pattathil, Sivakumar and Donohoe, Bryon S. and Mohanty, Sushree S. and Ryno, David and Yee, Kelsey and Thompson, Olivia A. and Rodriguez, Miguel and Dumitrache, Alexandru and Natzke, Jace and Winkeler, Kim and Collins, Cassandra and Yang, Xiaohan and Tan, Li and Sykes, Robert W. and Gjersing, Erica L. and Ziebell, Angela and Turner, Geoffrey B. and Decker, Stephen R. and Hahn, Michael G. and Davison, Brian H. and Udvardi, Michael K. and Mielenz, Jonathan R. and Davis, Mark F. and Nelson, Richard S. and Parrott, Wayne A. and Ragauskas, Arthur J. and Neal Stewart, C. and Mohnen, Debra},
abstractNote = {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.},
doi = {10.1038/nbt.4067},
journal = {Nature Biotechnology},
number = 3,
volume = 36,
place = {United States},
year = {2018},
month = {2}
}

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