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

Ajaya K. Biswal, Melani A. Atmodjo, Mi Li, Holly L. Baxter, Chang Geun Yoo, Yunqiao Pu, Yi Ching Lee, Mitra Mazarei, Ian M. Black, Ji Yi Zhang, Hema Ramanna, Adam L. Bray, Zachary R. King, Peter R. Lafayette, Sivakumar Pattathil, Bryon S. Donohoe, Sushree S. Mohanty, David Ryno, Kelsey Yee, Olivia A. Thompson & 22 others Miguel Rodriguez, Alexandru Dumitrache, Jace Natzke, Kim Winkeler, Cassandra Collins, Xiaohan Yang, Li Tan, Robert W. Sykes, Erica L. Gjersing, Angela Ziebell, Geoffrey B. Turner, Stephen R. Decker, Michael G. Hahn, Brian H. Davison, Michael K. Udvardi, Jonathan R. Mielenz, Mark F. Davis, Richard S. Nelson, Wayne A. Parrott, Arthur J. Ragauskas, C. Neal Stewart, Debra Mohnen

Research output: Contribution to journalArticleResearchpeer-review

25 Citations (Scopus)

Abstract

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. 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. Decreased recalcitrance in biomass processing and increased growth are likely due to reduced HG and RGII cross-linking in the cell wall.

Original languageEnglish
Pages (from-to)249-257
Number of pages9
JournalNature Biotechnology
Volume36
Issue number3
DOIs
Publication statusPublished - 1 Mar 2018
Externally publishedYes

Cite this

Biswal, A. K., Atmodjo, M. A., Li, M., Baxter, H. L., Yoo, C. G., Pu, Y., ... Mohnen, D. (2018). Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nature Biotechnology, 36(3), 249-257. https://doi.org/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. In: Nature Biotechnology. 2018 ; Vol. 36, No. 3. pp. 249-257.
@article{fb7aa38aa18746d9b73de8ea317db8f4,
title = "Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis",
abstract = "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. 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. Decreased recalcitrance in biomass processing and increased growth are likely due to reduced HG and RGII cross-linking in the cell wall.",
author = "Biswal, {Ajaya K.} and Atmodjo, {Melani A.} and Mi Li and Baxter, {Holly L.} and Yoo, {Chang Geun} and Yunqiao Pu and Lee, {Yi Ching} and Mitra Mazarei and Black, {Ian M.} and Zhang, {Ji Yi} and Hema Ramanna and Bray, {Adam L.} and King, {Zachary R.} and Lafayette, {Peter R.} and Sivakumar Pattathil and Donohoe, {Bryon S.} and Mohanty, {Sushree S.} and David Ryno and Kelsey Yee and Thompson, {Olivia A.} and Miguel Rodriguez and Alexandru Dumitrache and Jace Natzke and Kim Winkeler and Cassandra Collins and Xiaohan Yang and Li Tan and Sykes, {Robert W.} and Gjersing, {Erica L.} and Angela Ziebell 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 Debra Mohnen",
year = "2018",
month = "3",
day = "1",
doi = "10.1038/nbt.4067",
language = "English",
volume = "36",
pages = "249--257",
journal = "Nature Biotechnology",
issn = "1087-0156",
publisher = "Nature Publishing Group",
number = "3",

}

Biswal, AK, Atmodjo, MA, Li, M, Baxter, HL, Yoo, CG, Pu, Y, Lee, YC, Mazarei, M, Black, IM, Zhang, JY, Ramanna, H, Bray, AL, King, ZR, Lafayette, PR, Pattathil, S, Donohoe, BS, Mohanty, SS, Ryno, D, Yee, K, Thompson, OA, Rodriguez, M, Dumitrache, A, Natzke, J, Winkeler, K, Collins, C, Yang, X, Tan, L, Sykes, RW, Gjersing, EL, Ziebell, A, Turner, GB, Decker, SR, Hahn, MG, Davison, BH, Udvardi, MK, Mielenz, JR, Davis, MF, Nelson, RS, Parrott, WA, Ragauskas, AJ, Neal Stewart, C & Mohnen, D 2018, 'Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis', Nature Biotechnology, vol. 36, no. 3, pp. 249-257. https://doi.org/10.1038/nbt.4067

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.

In: Nature Biotechnology, Vol. 36, No. 3, 01.03.2018, p. 249-257.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis

AU - Biswal, Ajaya K.

AU - Atmodjo, Melani A.

AU - Li, Mi

AU - Baxter, Holly L.

AU - Yoo, Chang Geun

AU - Pu, Yunqiao

AU - Lee, Yi Ching

AU - Mazarei, Mitra

AU - Black, Ian M.

AU - Zhang, Ji Yi

AU - Ramanna, Hema

AU - Bray, Adam L.

AU - King, Zachary R.

AU - Lafayette, Peter R.

AU - Pattathil, Sivakumar

AU - Donohoe, Bryon S.

AU - Mohanty, Sushree S.

AU - Ryno, David

AU - Yee, Kelsey

AU - Thompson, Olivia A.

AU - Rodriguez, Miguel

AU - Dumitrache, Alexandru

AU - Natzke, Jace

AU - Winkeler, Kim

AU - Collins, Cassandra

AU - Yang, Xiaohan

AU - Tan, Li

AU - Sykes, Robert W.

AU - Gjersing, Erica L.

AU - Ziebell, Angela

AU - Turner, Geoffrey B.

AU - Decker, Stephen R.

AU - Hahn, Michael G.

AU - Davison, Brian H.

AU - Udvardi, Michael K.

AU - Mielenz, Jonathan R.

AU - Davis, Mark F.

AU - Nelson, Richard S.

AU - Parrott, Wayne A.

AU - Ragauskas, Arthur J.

AU - Neal Stewart, C.

AU - Mohnen, Debra

PY - 2018/3/1

Y1 - 2018/3/1

N2 - 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. 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. Decreased recalcitrance in biomass processing and increased growth are likely due to reduced HG and RGII cross-linking in the cell wall.

AB - 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. 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. Decreased recalcitrance in biomass processing and increased growth are likely due to reduced HG and RGII cross-linking in the cell wall.

UR - http://www.scopus.com/inward/record.url?scp=85042920324&partnerID=8YFLogxK

U2 - 10.1038/nbt.4067

DO - 10.1038/nbt.4067

M3 - Article

VL - 36

SP - 249

EP - 257

JO - Nature Biotechnology

JF - Nature Biotechnology

SN - 1087-0156

IS - 3

ER -