Insights into plant cell wall structure, architecture, and integrity using glycome profiling of native and AFEXTM -pre-treated biomass

Pattathil, Sivakumar; Hahn, Michael G.; Dale, Bruce E.; Chundawat, Shishir P.  S.

doi:10.1093/jxb/erv107

Title: Insights into plant cell wall structure, architecture, and integrity using glycome profiling of native and AFEX^TM -pre-treated biomass

Journal Article · 23 April 2015 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/erv107 · OSTI ID:1293995

Pattathil, Sivakumar ^[1]; Hahn, Michael G. ^[1]; Dale, Bruce E. ^[2]; Chundawat, Shishir P. S. ^[3]

Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Michigan State Univ., East Lansing, MI (United States). DOE Great Lakes Bioenergy Research Center, Dept. of Chemical Engineering
Michigan State Univ., East Lansing, MI (United States). DOE Great Lakes Bioenergy Research Center, Dept. of Chemical Engineering; Rutgers Univ., Piscataway, NJ (United States). Dept. of Chemical and Biochemical Engineering

We report that cell walls, which constitute the bulk of plant biomass, vary considerably in their structure, composition, and architecture. Studies on plant cell walls can be conducted on both native and pre-treated plant biomass samples, allowing an enhanced understanding of these structural and compositional variations. Here glycome profiling was employed to determine the relative abundance of matrix polysaccharides in several phylogenetically distinct native and pre-treated plant biomasses. Eight distinct biomass types belonging to four different subgroups (i.e. monocot grasses, woody dicots, herbaceous dicots, and softwoods) were subjected to various regimes of AFEX™ (ammonia fiber expansion) pre-treatment [AFEX is a trademark of MBI, Lansing (http://www.mbi.org]. This approach allowed detailed analysis of close to 200 cell wall glycan epitopes and their relative extractability using a high-throughput platform. In general, irrespective of the phylogenetic origin, AFEX™ pre-treatment appeared to cause loosening and improved accessibility of various xylan epitope subclasses in most plant biomass materials studied. For most biomass types analysed, such loosening was also evident for other major non-cellulosic components including subclasses of pectin and xyloglucan epitopes. The studies also demonstrate that AFEX™ pre-treatment significantly reduced cell wall recalcitrance among diverse phylogenies (except softwoods) by inducing structural modifications to polysaccharides that were not detectable by conventional gross composition analyses. Lastly, we found that monitoring changes in cell wall glycan compositions and their relative extractability for untreated and pre-treated plant biomass can provide an improved understanding of variations in structure and composition of plant cell walls and delineate the role(s) of matrix polysaccharides in cell wall recalcitrance.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; FC02-07ER64494; DBI-0421683; IOS-0923992

OSTI ID:: 1293995

Journal Information:: Journal of Experimental Botany, Vol. 66, Issue 14; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles Moller, Isabel; Marcus, Susan E.; Haeger, Ash Glycoconjugate Journal, Vol. 25, Issue 1 https://doi.org/10.1007/s10719-007-9059-7	journal	July 2007
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Process and economic analysis of pretreatment technologies Eggeman, Tim; Elander, Richard T. Bioresource Technology, Vol. 96, Issue 18, p. 2019-2025 https://doi.org/10.1016/j.biortech.2005.01.017	journal	December 2005
Multifaceted characterization of cell wall decomposition products formed during ammonia fiber expansion (AFEX) and dilute acid based pretreatments Chundawat, Shishir P. S.; Vismeh, Ramin; Sharma, Lekh N. Bioresource Technology, Vol. 101, Issue 21 https://doi.org/10.1016/j.biortech.2010.06.027	journal	November 2010
Evaluating the impact of ammonia fiber expansion (AFEX) pretreatment conditions on the cost of ethanol production Bals, Bryan; Wedding, Chris; Balan, Venkatesh Bioresource Technology, Vol. 102, Issue 2, p. 1277-1283 https://doi.org/10.1016/j.biortech.2010.08.058	journal	January 2011
Evolution and diversity of green plant cell walls Popper, Z. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.02.012	journal	June 2008
Revealing the structural and functional diversity of plant cell walls Knox, J. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.001	journal	June 2008
Unique aspects of the grass cell wall Vogel, J. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.002	journal	June 2008
Pectin structure and biosynthesis Mohnen, D. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.03.006	journal	June 2008
In Vitro Model Assemblies To Study the Impact of Lignin−Carbohydrate Interactions on the Enzymatic Conversion of Xylan Boukari, Imen; Putaux, Jean-Luc; Cathala, Bernard Biomacromolecules, Vol. 10, Issue 9 https://doi.org/10.1021/bm9004518	journal	September 2009
Restructuring the Crystalline Cellulose Hydrogen Bond Network Enhances Its Depolymerization Rate Chundawat, Shishir P. S.; Bellesia, Giovanni; Uppugundla, Nirmal Journal of the American Chemical Society, Vol. 133, Issue 29 https://doi.org/10.1021/ja2011115	journal	July 2011
3D Electron Tomography of Pretreated Biomass Informs Atomic Modeling of Cellulose Microfibrils Ciesielski, Peter N.; Matthews, James F.; Tucker, Melvin P. ACS Nano, Vol. 7, Issue 9 https://doi.org/10.1021/nn4031542	journal	August 2013
Loss of function of cinnamyl alcohol dehydrogenase 1 leads to unconventional lignin and a temperature-sensitive growth defect in Medicago truncatula Zhao, Q.; Tobimatsu, Y.; Zhou, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 33 https://doi.org/10.1073/pnas.1312234110	journal	July 2013
Efficient biomass pretreatment using ionic liquids derived from lignin and hemicellulose Socha, A. M.; Parthasarathi, R.; Shi, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1405685111	journal	August 2014
Feruloylation in Grasses: Current and Future Perspectives de O. Buanafina, Marcia M. Molecular Plant, Vol. 2, Issue 5 https://doi.org/10.1093/mp/ssp067	journal	September 2009
Covalent Cross-Links in the Cell Wall Iiyama, K.; Lam, Tbt.; Stone, B. A. Plant Physiology, Vol. 104, Issue 2 https://doi.org/10.1104/pp.104.2.315	journal	February 1994
A Comprehensive Toolkit of Plant Cell Wall Glycan-Directed Monoclonal Antibodies Pattathil, S.; Avci, U.; Baldwin, D. Plant Physiology, Vol. 153, Issue 2, p. 514-525 https://doi.org/10.1104/pp.109.151985	journal	April 2010
Developmental and Tissue-Specific Structural Alterations of the Cell-Wall Polysaccharides of Arabidopsis thaliana Roots Freshour, G.; Clay, R. P.; Fuller, M. S. Plant Physiology, Vol. 110, Issue 4 https://doi.org/10.1104/pp.110.4.1413	journal	April 1996
GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns Bromley, Jennifer R.; Busse-Wicher, Marta; Tryfona, Theodora The Plant Journal, Vol. 74, Issue 3 https://doi.org/10.1111/tpj.12135	journal	March 2013
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
How Does Plant Cell Wall Nanoscale Architecture Correlate with Enzymatic Digestibility? Ding, S. -Y.; Liu, Y. -S.; Zeng, Y. Science, Vol. 338, Issue 6110 https://doi.org/10.1126/science.1227491	journal	November 2012
Deconstruction of Lignocellulosic Biomass to Fuels and Chemicals Chundawat, Shishir P. S.; Beckham, Gregg T.; Himmel, Michael E. Annual Review of Chemical and Biomolecular Engineering, Vol. 2, Issue 1, p. 121-145 https://doi.org/10.1146/annurev-chembioeng-061010-114205	journal	July 2011
Enhanced characteristics of genetically modified switchgrass (Panicum virgatum L.) for high biofuel production Shen, Hui; Poovaiah, Charleson R.; Ziebell, Angela Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-71	journal	January 2013
Comparative analysis of the ability of Clostridium clariflavum strains and Clostridium thermocellumto utilize hemicellulose and unpretreated plant material Izquierdo, Javier A.; Pattathil, Sivakumar; Guseva, Anna Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0136-4	journal	November 2014
Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance Chung, Daehwan; Pattathil, Sivakumar; Biswal, Ajaya K. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0147-1	journal	October 2014
Supramolecular Self-Assembled Chaos: Polyphenolic Lignin’s Barrier to Cost-Effective Lignocellulosic Biofuels Achyuthan, Komandoor Elayavalli; Achyuthan, Ann Mary; Adams, Paul David Molecules, Vol. 15, Issue 12 https://doi.org/10.3390/molecules15118641	journal	November 2010
Multi-scale visualization and characterization of lignocellulosic plant cell wall deconstruction during thermochemical pretreatment Chundawat, Shishir P. S.; Donohoe, Bryon S.; Sousa, Leonardo Rutgers University https://doi.org/10.7282/t3j1062s	text	January 2011
Enzymatic digestibility and pretreatment degradation products of AFEX-treated hardwoods (Populus nigra) Balan, Venkatesh; da Costa Sousa, Leonardo; Dale, Bruce E. Rutgers University https://doi.org/10.7282/t3zp48dw	text	January 2009

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Probing the role of cation-π interaction in the thermotolerance and catalytic performance of endo-polygalacturonases Tu, Tao; Li, Yeqing; Su, Xiaoyun Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep38413	journal	December 2016
Determination of glycoside hydrolase specificities during hydrolysis of plant cell walls using glycome profiling Walker, Johnnie A.; Pattathil, Sivakumar; Bergeman, Lai F. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0703-6	journal	February 2017
Comprehensive characterization of non-cellulosic recalcitrant cell wall carbohydrates in unhydrolyzed solids from AFEX-pretreated corn stover Gunawan, Christa; Xue, Saisi; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0757-5	journal	March 2017
Xylan epitope profiling: an enhanced approach to study organ development-dependent changes in xylan structure, biosynthesis, and deposition in plant cell walls Peralta, Angelo G.; Venkatachalam, Sivasankari; Stone, Sydney C. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0935-5	journal	November 2017
Dynamic changes in transcriptome and cell wall composition underlying brassinosteroid-mediated lignification of switchgrass suspension cells Rao, Xiaolan; Shen, Hui; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0954-2	journal	November 2017
Conversion of lignocellulosic agave residues into liquid biofuels using an AFEX™-based biorefinery Flores-Gómez, Carlos A.; Escamilla Silva, Eleazar M.; Zhong, Cheng Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-017-0995-6	journal	January 2018
Catalysts of plant cell wall loosening Cosgrove, Daniel J. F1000Research, Vol. 5 https://doi.org/10.12688/f1000research.7180.1	journal	January 2016
Comparative genome analysis indicates high evolutionary potential of pathogenicity genes in Colletotrichum tanaceti Lelwala, Ruvini V.; Korhonen, Pasi K.; Young, Neil D. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0212248	journal	May 2019
Immunological Approaches to Biomass Characterization and Utilization Pattathil, Sivakumar; Avci, Utku; Zhang, Tiantian Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00173	journal	October 2015
Report on the Current Inventory of the Toolbox for Plant Cell Wall Analysis: Proteinaceous and Small Molecular Probes Rydahl, Maja G.; Hansen, Aleksander R.; Kračun, Stjepan K. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00581	journal	May 2018
Phytolith Formation in Plants: From Soil to Cell Nawaz, Muhammad Amjad; Zakharenko, Alexander Mikhailovich; Zemchenko, Ivan Vladimirovich Plants, Vol. 8, Issue 8 https://doi.org/10.3390/plants8080249	journal	July 2019

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59 BASIC BIOLOGICAL SCIENCES
09 BIOMASS FUELS
recalcitrance
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AFEX
biofuels
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Title: Insights into plant cell wall structure, architecture, and integrity using glycome profiling of native and AFEXTM -pre-treated biomass

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Title: Insights into plant cell wall structure, architecture, and integrity using glycome profiling of native and AFEX^TM -pre-treated biomass