Characterization of cellulose structure of Populus plants modified in candidate cellulose biosynthesis genes
Abstract
Here, the recalcitrant nature of lignocellulosic biomass is a combined effect of several factors such as high crystallinity and high degree of polymerization of cellulose, lignin content and structure, and the available surface area for enzymatic degradation (i.e., accessibility). Genetic improvement of feedstock cell wall properties is a path to reducing recalcitrance of lignocellulosic biomass and improving conversion to various biofuels. An advanced understanding of the cellulose biosynthesis pathway is essential to precisely modify cellulose properties of plant cell walls. Here we report on the impact of modified expression of candidate cellulose biosynthesis pathway genes on the ultra-structure of cellulose, a key carbohydrate polymer of Populus cell wall using advanced nuclear magnetic resonance approaches. Noteworthy changes were observed in the cell wall characteristics of downregulated KORRIGAN 1 (KOR) and KOR 2 transgenic plants in comparison to the wild-type control. It was observed that all of the transgenic lines showed variation in cellulose ultrastructure, increase in cellulose crystallinity and decrease in the cellulose degree of polymerization. Additionally, the properties of cellulose allomorph abundance and accessibility were found to be variable. Application of such cellulose characterization techniques beyond the traditional measurement of cellulose abundance to comprehensive studies of cellulose properties in largermore »
- Authors:
-
[3]
- Georgia Inst. of Technology, Atlanta, GA (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Georgia Inst. of Technology, Atlanta, GA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1327717
- Alternate Identifier(s):
- OSTI ID: 1398027
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biomass and Bioenergy
- Additional Journal Information:
- Journal Volume: 94; Journal Issue: C; Journal ID: ISSN 0961-9534
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; cellulose biosynthesis; gene; crystallinity; micro-fibril; degree of polymerization
Citation Formats
Bali, Garima, Khunsupat, Ratayakorn, Akinosho, Hannah, Payyavula, Raja S., Samuel, Reichel, Tuskan, Gerald A., Kalluri, Udaya C., and Ragauskas, Arthur J. Characterization of cellulose structure of Populus plants modified in candidate cellulose biosynthesis genes. United States: N. p., 2016.
Web. doi:10.1016/j.biombioe.2016.08.013.
Bali, Garima, Khunsupat, Ratayakorn, Akinosho, Hannah, Payyavula, Raja S., Samuel, Reichel, Tuskan, Gerald A., Kalluri, Udaya C., & Ragauskas, Arthur J. Characterization of cellulose structure of Populus plants modified in candidate cellulose biosynthesis genes. United States. https://doi.org/10.1016/j.biombioe.2016.08.013
Bali, Garima, Khunsupat, Ratayakorn, Akinosho, Hannah, Payyavula, Raja S., Samuel, Reichel, Tuskan, Gerald A., Kalluri, Udaya C., and Ragauskas, Arthur J. Sat .
"Characterization of cellulose structure of Populus plants modified in candidate cellulose biosynthesis genes". United States. https://doi.org/10.1016/j.biombioe.2016.08.013. https://www.osti.gov/servlets/purl/1327717.
@article{osti_1327717,
title = {Characterization of cellulose structure of Populus plants modified in candidate cellulose biosynthesis genes},
author = {Bali, Garima and Khunsupat, Ratayakorn and Akinosho, Hannah and Payyavula, Raja S. and Samuel, Reichel and Tuskan, Gerald A. and Kalluri, Udaya C. and Ragauskas, Arthur J.},
abstractNote = {Here, the recalcitrant nature of lignocellulosic biomass is a combined effect of several factors such as high crystallinity and high degree of polymerization of cellulose, lignin content and structure, and the available surface area for enzymatic degradation (i.e., accessibility). Genetic improvement of feedstock cell wall properties is a path to reducing recalcitrance of lignocellulosic biomass and improving conversion to various biofuels. An advanced understanding of the cellulose biosynthesis pathway is essential to precisely modify cellulose properties of plant cell walls. Here we report on the impact of modified expression of candidate cellulose biosynthesis pathway genes on the ultra-structure of cellulose, a key carbohydrate polymer of Populus cell wall using advanced nuclear magnetic resonance approaches. Noteworthy changes were observed in the cell wall characteristics of downregulated KORRIGAN 1 (KOR) and KOR 2 transgenic plants in comparison to the wild-type control. It was observed that all of the transgenic lines showed variation in cellulose ultrastructure, increase in cellulose crystallinity and decrease in the cellulose degree of polymerization. Additionally, the properties of cellulose allomorph abundance and accessibility were found to be variable. Application of such cellulose characterization techniques beyond the traditional measurement of cellulose abundance to comprehensive studies of cellulose properties in larger transgenic and naturally variable populations is expected to provide deeper insights into the complex nature of lignocellulosic material, which can significantly contribute to the development of precisely tailored plants for enhanced biofuels production.},
doi = {10.1016/j.biombioe.2016.08.013},
journal = {Biomass and Bioenergy},
number = C,
volume = 94,
place = {United States},
year = {Sat Sep 10 00:00:00 EDT 2016},
month = {Sat Sep 10 00:00:00 EDT 2016}
}
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Works referenced in this record:
Plants to power: bioenergy to fuel the future
journal, August 2008
- Yuan, Joshua S.; Tiller, Kelly H.; Al-Ahmad, Hani
- Trends in Plant Science, Vol. 13, Issue 8
Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels
journal, July 2006
- Hill, J.; Nelson, E.; Tilman, D.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 30
Bioethanol
journal, April 2006
- Gray, Kevin A.; Zhao, Lishan; Emptage, Mark
- Current Opinion in Chemical Biology, Vol. 10, Issue 2, p. 141-146
The Path Forward for Biofuels and Biomaterials
journal, January 2006
- Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H.
- Science, Vol. 311, Issue 5760, p. 484-489
Cellulose crystallinity - a key predictor of the enzymatic hydrolysis rate: Cellulose crystallinity
journal, February 2010
- Hall, Mélanie; Bansal, Prabuddha; Lee, Jay H.
- FEBS Journal, Vol. 277, Issue 6
Evolution and impact of cellulose architecture during enzymatic hydrolysis by fungal cellulases
journal, January 2013
- Chauve, Marie; Barre, Loic; Tapin-Lingua, Sandra
- Advances in Bioscience and Biotechnology, Vol. 04, Issue 12
Organosolv Ethanol Lignin from Hybrid Poplar as a Radical Scavenger: Relationship between Lignin Structure, Extraction Conditions, and Antioxidant Activity
journal, August 2006
- Pan, Xuejun; Kadla, John F.; Ehara, Katsunobu
- Journal of Agricultural and Food Chemistry, Vol. 54, Issue 16
Coordinated development of leading biomass pretreatment technologies
journal, December 2005
- Wyman, Charles E.; Dale, Bruce E.; Elander, Richard T.
- Bioresource Technology, Vol. 96, Issue 18, p. 1959-1966
Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies
journal, September 2009
- Kumar, Rajeev; Mago, Gaurav; Balan, Venkatesh
- Bioresource Technology, Vol. 100, Issue 17
Transgenics are imperative for biofuel crops
journal, March 2008
- Gressel, Jonathan
- Plant Science, Vol. 174, Issue 3
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass
journal, February 2011
- Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808
The endo-1,4-β-glucanase Korrigan exhibits functional conservation between gymnosperms and angiosperms and is required for proper cell wall formation in gymnosperms
journal, December 2011
- Maloney, Victoria J.; Samuels, A. Lacey; Mansfield, Shawn D.
- New Phytologist, Vol. 193, Issue 4
Effect of Modification of the O-Methyltransferase Activity on Cell Wall Composition, Ultrastructure and Degradability of Transgenic Tobacco
journal, November 1996
- Vailhé, Marie Andrée Bernard; Migné, Carole; Cornu, Agnès
- Journal of the Science of Food and Agriculture, Vol. 72, Issue 3
Downregulation of Caffeic Acid 3- O -Methyltransferase and Caffeoyl CoA 3- O -Methyltransferase in Transgenic Alfalfa: Impacts on Lignin Structure and Implications for the Biosynthesis of G and S Lignin
journal, January 2001
- Guo, Dianjing; Chen, Fang; Inoue, Kentaro
- The Plant Cell, Vol. 13, Issue 1
Chemical, ultrastructural and supramolecular analysis of tension wood in Populus tremula x alba as a model substrate for reduced recalcitrance
journal, January 2011
- Foston, Marcus; Hubbell, Christopher A.; Samuel, Reichel
- Energy & Environmental Science, Vol. 4, Issue 12
Cellulose Synthesis in Higher Plants
journal, November 2006
- Somerville, Chris
- Annual Review of Cell and Developmental Biology, Vol. 22, Issue 1
Role of the Putative Membrane-Bound Endo-1,4-β-Glucanase KORRIGAN in Cell Elongation and Cellulose Synthesis in Arabidopsis thaliana
journal, March 2001
- Sato, Shigeru; Kato, Tomohiko; Kakegawa, Koichi
- Plant and Cell Physiology, Vol. 42, Issue 3
The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning
journal, October 1999
- Sturm, Arnd; Tang, Guo-Qing
- Trends in Plant Science, Vol. 4, Issue 10
CELLULOSE BIOSYNTHESIS: Exciting Times for A Difficult Field of Study
journal, June 1999
- Delmer, Deborah P.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1
Sitosterol-beta -glucoside as Primer for Cellulose Synthesis in Plants
journal, January 2002
- Peng, L.
- Science, Vol. 295, Issue 5552
Characterization and varied expression of a membrane-bound endo-β-1,4-glucanase in hybrid poplar
journal, April 2010
- Maloney, Victoria J.; Mansfield, Shawn D.
- Plant Biotechnology Journal, Vol. 8, Issue 3
Towards Understanding the Role of Membrane-bound Endo-β-1,4-glucanases in Cellulose Biosynthesis
journal, December 2002
- Mølhøj, Michael; Pagant, Silvère; Höfte, Herman
- Plant and Cell Physiology, Vol. 43, Issue 12
Changes in lignocellulosic supramolecular and ultrastructure during dilute acid pretreatment of Populus and switchgrass
journal, December 2010
- Foston, Marcus; Ragauskas, Art J.
- Biomass and Bioenergy, Vol. 34, Issue 12
Down-Regulation of KORRIGAN-Like Endo-β-1,4-Glucanase Genes Impacts Carbon Partitioning, Mycorrhizal Colonization and Biomass Production in Populus
journal, October 2016
- Kalluri, Udaya C.; Payyavula, Raja S.; Labbé, Jessy L.
- Frontiers in Plant Science, Vol. 7
Comparison of laboratory delignification methods, their selectivity, and impacts on physiochemical characteristics of cellulosic biomass
journal, February 2013
- Kumar, Rajeev; Hu, Fan; Hubbell, Christopher A.
- Bioresource Technology, Vol. 130
The effect of precipitation on the molecular weight distribution of cellulose tricarbanilate
journal, August 1986
- Wood, Barry F.; Conner, Anthony H.; Hill, Charles G.
- Journal of Applied Polymer Science, Vol. 32, Issue 2
Structural characterization of hemicelluloses fractionated by graded ethanol precipitation from Pinus yunnanensis
journal, May 2012
- Xue, Bai-Liang; Wen, Jia-Long; Xu, Feng
- Carbohydrate Research, Vol. 352
Isolation of Cellulolytic Enzyme Lignin from Wood Preswollen/Dissolved in Dimethyl Sulfoxide/ N -Methylimidazole
journal, March 2010
- Zhang, Aiping; Lu, Fachuang; Sun, Run-Cang
- Journal of Agricultural and Food Chemistry, Vol. 58, Issue 6
Inhibition of cellulase, xylanase and β-glucosidase activities by softwood lignin preparations
journal, September 2006
- Berlin, Alex; Balakshin, Mikhail; Gilkes, Neil
- Journal of Biotechnology, Vol. 125, Issue 2, p. 198-209
Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance
journal, January 2010
- Park, Sunkyu; Baker, John O.; Himmel, Michael E.
- Biotechnology for Biofuels, Vol. 3, Issue 1
Assignment of non-crystalline forms in cellulose I by CP/MAS 13C NMR spectroscopy
journal, November 1998
- Wickholm, Kristina; Larsson, Per Tomas; Iversen, Tommy
- Carbohydrate Research, Vol. 312, Issue 3
A CP/MAS13C NMR investigation of molecular ordering in celluloses
journal, July 1997
- Larsson, Per Tomas; Wickholm, Kristina; Iversen, Tommy
- Carbohydrate Research, Vol. 302, Issue 1-2
KORRIGAN1 and its Aspen Homolog PttCel9A1 Decrease Cellulose Crystallinity in Arabidopsis Stems
journal, April 2009
- Takahashi, Junko; Rudsander, Ulla J.; Hedenström, Mattias
- Plant and Cell Physiology, Vol. 50, Issue 6
Determination of cellulose Iα and Iβ in lignocellulosic materials
journal, August 1994
- Lennholm, Helena; Larsson, Tomas; Iversen, Tommy
- Carbohydrate Research, Vol. 261, Issue 1
Structural aspects in ultrathin cellulose microfibrils followed by 13C CP-MAS NMR
journal, October 1999
- Heux, L.; Dinand, E.; Vignon, M. R.
- Carbohydrate Polymers, Vol. 40, Issue 2
Effects of organosolv pretreatment and enzymatic hydrolysis on cellulose structure and crystallinity in Loblolly pine
journal, May 2010
- Sannigrahi, Poulomi; Miller, Stephen J.; Ragauskas, Arthur J.
- Carbohydrate Research, Vol. 345, Issue 7
CP/MAS 13C NMR analysis of cellulase treated bleached softwood kraft pulp
journal, April 2006
- Pu, Yunqiao; Ziemer, Cherie; Ragauskas, Arthur J.
- Carbohydrate Research, Vol. 341, Issue 5
Estimation of the lateral dimensions of cellulose crystallites using NMR signal strengths
journal, October 1999
- Newman, Roger H.
- Solid State Nuclear Magnetic Resonance, Vol. 15, Issue 1
Cellulose biosynthesis and deposition in higher plants
journal, April 2008
- Taylor, Neil G.
- New Phytologist, Vol. 178, Issue 2
The Maize Primary Cell Wall Microfibril: A New Model Derived from Direct Visualization
journal, February 2006
- Ding, Shi-You; Himmel, Michael E.
- Journal of Agricultural and Food Chemistry, Vol. 54, Issue 3
Toward an aggregated understanding of enzymatic hydrolysis of cellulose: Noncomplexed cellulase systems
journal, November 2004
- Zhang, Yi-Heng Percival; Lynd, Lee R.
- Biotechnology and Bioengineering, Vol. 88, Issue 7, p. 797-824
HSQC (heteronuclear single quantum coherence) 13C–1H correlation spectra of whole biomass in perdeuterated pyridinium chloride–DMSO system: An effective tool for evaluating pretreatment
journal, September 2011
- Samuel, Reichel; Foston, Marcus; Jaing, Nan
- Fuel, Vol. 90, Issue 9
NMR Characterization of C3H and HCT Down-Regulated Alfalfa Lignin
journal, October 2009
- Pu, Yunqiao; Chen, Fang; Ziebell, Angela
- BioEnergy Research, Vol. 2, Issue 4
Works referencing / citing this record:
The effect of liquid hot water pretreatment on the chemical–structural alteration and the reduced recalcitrance in poplar
journal, November 2017
- Li, Mi; Cao, Shilin; Meng, Xianzhi
- Biotechnology for Biofuels, Vol. 10, Issue 1
Functional Analysis of Cellulose Synthase CesA4 and CesA6 Genes in Switchgrass (Panicum virgatum) by Overexpression and RNAi-Mediated Gene Silencing
journal, August 2018
- Mazarei, Mitra; Baxter, Holly L.; Li, Mi
- Frontiers in Plant Science, Vol. 9
Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants
journal, June 2018
- Veach, Allison M.; Yip, Daniel; Engle, Nancy L.
- Plant and Soil, Vol. 429, Issue 1-2
The effect of liquid hot water pretreatment on the chemical–structural alteration and the reduced recalcitrance in poplar
text, January 2017
- Li, Mi; Cao, Shilin; Meng, Xianzhi
- (:null)
Progress in understanding and overcoming biomass recalcitrance: a BioEnergy Science Center (BESC) perspective
journal, November 2017
- Gilna, Paul; Lynd, Lee R.; Mohnen, Debra
- Biotechnology for Biofuels, Vol. 10, Issue 1