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Title: OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice

Abstract

Genetic modification of plant cell walls has been posed to reduce lignocellulose recalcitrance for enhancing biomass saccharification. Several dozen CESA mutants have been reported since cellulose synthase (CESA) gene was first identified, but almost all mutants exhibit the defective phenotypes in plant growth and development. Here, the rice (Oryza sativa) Osfc16 mutant with substitutions (W481C, P482S) at P-CR conserved site in CESA9 shows a slightly affected plant growth and higher biomass yield by 25%–41% compared with wild type (Nipponbare, a japonica variety). Chemical and ultrastructural analyses indicate that Osfc16 has a significantly reduced cellulose crystallinity (CrI) and thinner secondary cell walls compared with wild type. CESA co-IP detection, together with implementations of a proteasome inhibitor (MG132) and two distinct cellulose inhibitors (Calcofluor, CGA), shows that CESA9 mutation could affect integrity of CESA4/7/9 complexes, which may lead to rapid CESA proteasome degradation for low-DP cellulose biosynthesis. These may reduce cellulose CrI, which improves plant lodging resistance, a major and integrated agronomic trait on plant growth and grain production, and enhances biomass enzymatic saccharification by up to 2.3-fold and ethanol productivity by 34%–42%. Our study has for the first time reported a direct modification for the low-DP cellulose production that has broadmore » applications in biomass industries.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2]; ORCiD logo [2];  [1]
  1. Huazhong Agricultural Univ. Wuhan (China)
  2. Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1376598
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Plant Biotechnology Journal
Additional Journal Information:
Journal Volume: 15; Journal Issue: 9; Journal ID: ISSN 1467-7644
Publisher:
Society for Experimental Biology; Association of Applied Biology
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; biomass saccharification; cellulose; CESA; lodging resistance; rice

Citation Formats

Li, Fengcheng, Xie, Guosheng, Huang, Jiangfeng, Zhang, Ran, Li, Yu, Zhang, Miaomiao, Wang, Yanting, Li, Ao, Li, Xukai, Xia, Tao, Qu, Chengcheng, Hu, Fan, Ragauskas, Arthur J., and Peng, Liangcai. OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice. United States: N. p., 2017. Web. doi:10.1111/pbi.12700.
Li, Fengcheng, Xie, Guosheng, Huang, Jiangfeng, Zhang, Ran, Li, Yu, Zhang, Miaomiao, Wang, Yanting, Li, Ao, Li, Xukai, Xia, Tao, Qu, Chengcheng, Hu, Fan, Ragauskas, Arthur J., & Peng, Liangcai. OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice. United States. https://doi.org/10.1111/pbi.12700
Li, Fengcheng, Xie, Guosheng, Huang, Jiangfeng, Zhang, Ran, Li, Yu, Zhang, Miaomiao, Wang, Yanting, Li, Ao, Li, Xukai, Xia, Tao, Qu, Chengcheng, Hu, Fan, Ragauskas, Arthur J., and Peng, Liangcai. 2017. "OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice". United States. https://doi.org/10.1111/pbi.12700. https://www.osti.gov/servlets/purl/1376598.
@article{osti_1376598,
title = {OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice},
author = {Li, Fengcheng and Xie, Guosheng and Huang, Jiangfeng and Zhang, Ran and Li, Yu and Zhang, Miaomiao and Wang, Yanting and Li, Ao and Li, Xukai and Xia, Tao and Qu, Chengcheng and Hu, Fan and Ragauskas, Arthur J. and Peng, Liangcai},
abstractNote = {Genetic modification of plant cell walls has been posed to reduce lignocellulose recalcitrance for enhancing biomass saccharification. Several dozen CESA mutants have been reported since cellulose synthase (CESA) gene was first identified, but almost all mutants exhibit the defective phenotypes in plant growth and development. Here, the rice (Oryza sativa) Osfc16 mutant with substitutions (W481C, P482S) at P-CR conserved site in CESA9 shows a slightly affected plant growth and higher biomass yield by 25%–41% compared with wild type (Nipponbare, a japonica variety). Chemical and ultrastructural analyses indicate that Osfc16 has a significantly reduced cellulose crystallinity (CrI) and thinner secondary cell walls compared with wild type. CESA co-IP detection, together with implementations of a proteasome inhibitor (MG132) and two distinct cellulose inhibitors (Calcofluor, CGA), shows that CESA9 mutation could affect integrity of CESA4/7/9 complexes, which may lead to rapid CESA proteasome degradation for low-DP cellulose biosynthesis. These may reduce cellulose CrI, which improves plant lodging resistance, a major and integrated agronomic trait on plant growth and grain production, and enhances biomass enzymatic saccharification by up to 2.3-fold and ethanol productivity by 34%–42%. Our study has for the first time reported a direct modification for the low-DP cellulose production that has broad applications in biomass industries.},
doi = {10.1111/pbi.12700},
url = {https://www.osti.gov/biblio/1376598}, journal = {Plant Biotechnology Journal},
issn = {1467-7644},
number = 9,
volume = 15,
place = {United States},
year = {Wed Mar 15 00:00:00 EDT 2017},
month = {Wed Mar 15 00:00:00 EDT 2017}
}

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Works referenced in this record:

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Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone
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Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
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Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains
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Brittle Culm1, a COBRA-Like Protein, Functions in Cellulose Assembly through Binding Cellulose Microfibrils
journal, August 2013


Expression profiling and integrative analysis of the CESA/CSL superfamily in rice
journal, January 2010


Plant cell wall engineering: applications in biofuel production and improved human health
journal, April 2014


XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan
journal, October 2012


DWARF3 Participates in an SCF Complex and Associates with DWARF14 to Suppress Rice Shoot Branching
journal, April 2014


Disruption of Secondary Wall Cellulose Biosynthesis Alters Cadmium Translocation and Tolerance in Rice Plants
journal, November 2013


Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies
journal, September 2009


Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014


Loosening lignin's grip on biofuel production
journal, July 2007


Interactions among three distinct CesA proteins essential for cellulose synthesis
journal, January 2003


Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1A903V and CESA3T942I of cellulose synthase
journal, February 2012


Tertiary model of a plant cellulose synthase
journal, April 2013


New hope for old dreams: evidence that plant cellulose synthase genes have finally been identified.
journal, October 1996


Disruption of Secondary Wall Cellulose Biosynthesis Alters Cadmium Translocation and Tolerance in Rice Plants
journal, November 2013


DWARF3 Participates in an SCF Complex and Associates with DWARF14 to Suppress Rice Shoot Branching
journal, April 2014


Three Distinct Rice Cellulose Synthase Catalytic Subunit Genes Required for Cellulose Synthesis in the Secondary Wall
journal, August 2003


Pausing of Golgi Bodies on Microtubules Regulates Secretion of Cellulose Synthase Complexes in Arabidopsis
journal, April 2009


A Gibberellin-Mediated DELLA-NAC Signaling Cascade Regulates Cellulose Synthesis in Rice
journal, May 2015


Cell-wall carbohydrates and their modification as a resource for biofuels
journal, May 2008


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


How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility?
journal, November 2012


Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone
journal, April 2014


Calcofluor white ST Alters the in vivo assembly of cellulose microfibrils
journal, November 1980


The Ubiquitin 26s Proteasome Proteolytic Pathway
journal, June 2004


Cellulose Synthesis in Higher Plants
journal, November 2006


Expression profiling and integrative analysis of the CESA/CSL superfamily in rice
journal, January 2010


Works referencing / citing this record:

Flax tubulin and CesA superfamilies represent attractive and challenging targets for a variety of genome- and base-editing applications
journal, March 2019


Survey of wheat straw stem characteristics for enhanced resistance to lodging
journal, January 2020


Stalk Bending Strength is Strongly Associated with Maize Stalk Lodging Incidence Across Multiple Environments
journal, April 2020


Cellulose Synthase Mutants Distinctively Affect Cell Growth and Cell Wall Integrity for Plant Biomass Production in Arabidopsis
journal, March 2018


Three AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis
journal, October 2017


AtCSLD3 and GhCSLD3 mediate root growth and cell elongation downstream of the ethylene response pathway in Arabidopsis
journal, December 2017


Three AtCesA6-like members enhance biomass production by distinctively promoting cell growth in Arabidopsis
journal, October 2017