Identification of developmental stage and anatomical fraction contributions to cell wall recalcitrance in switchgrass

Crowe, Jacob D.; Feringa, Nicholas; Pattathil, Sivakumar; Merritt, Brian; Foster, Cliff; Dines, Dayna; Ong, Rebecca G.; Hodge, David B.

doi:10.1186/s13068-017-0870-5

Title: Identification of developmental stage and anatomical fraction contributions to cell wall recalcitrance in switchgrass

Journal Article · 01 December 2017 · Biotechnology for Biofuels

DOI: https://doi.org/10.1186/s13068-017-0870-5 · OSTI ID:1618683

Crowe, Jacob D. ^[1]; Feringa, Nicholas ^[1]; Pattathil, Sivakumar ^[2]; Merritt, Brian ^[3]; Foster, Cliff ^[4]; Dines, Dayna ^[4]; Ong, Rebecca G. ^[5]; Hodge, David B. ^[6]

Michigan State Univ., East Lansing, MI (United States). Dept. of Chemical Engineering and Materials Science
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)
Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
Michigan State Univ., East Lansing, MI (United States). DOE-Great Lakes Bioenergy Research Center
Michigan Technological Univ., Houghton, MI (United States). Dept. of Chemical Engineering
Michigan State Univ., East Lansing, MI (United States). Dept. of Chemical Engineering and Materials Science; Michigan State Univ., East Lansing, MI (United States). DOE-Great Lakes Bioenergy Research Center, and Dept. of Biosystems & Agricultural Engineering; Luleå Univ. of Technology, Luleå (Sweden). Dept. of Civil, Environmental and Natural Resources Engineering

Background: Heterogeneity within herbaceous biomass can present important challenges for processing feedstocks to cellulosic biofuels. Alterations to cell wall composition and organization during plant growth represent major contributions to heterogeneity within a single species or cultivar. To address this challenge, the focus of this study was to characterize the relationship between composition and properties of the plant cell wall and cell wall response to deconstruction by NaOH pretreatment and enzymatic hydrolysis for anatomical fractions (stem internodes, leaf sheaths, and leaf blades) within switchgrass at various tissue maturities as assessed by differing internode. Results: Substantial differences in both cell wall composition and response to deconstruction were observed as a function of anatomical fraction and tissue maturity. Notably, lignin content increased with tissue maturity concurrently with decreasing ferulate content across all three anatomical fractions. Stem internodes exhibited the highest lignin content as well as the lowest hydrolysis yields, which were inversely correlated to lignin content. Confocal microscopy was used to demonstrate that removal of cell wall aromatics (i.e., lignins and hydroxycinnamates) by NaOH pretreatment was non-uniform across diverse cell types. Non-cellulosic polysaccharides were linked to differences in cell wall response to deconstruction in lower lignin fractions. Specifically, leaf sheath and leaf blade were found to have higher contents of substituted glucuronoarabinoxylans and pectic polysaccharides. Glycome profiling demonstrated that xylan and pectic polysaccharide extractability varied with stem internode maturity, with more mature internodes requiring harsher chemical extractions to remove comparable glycan abundances relative to less mature internodes. While enzymatic hydrolysis was performed on extractives-free biomass, extractible sugars (i.e., starch and sucrose) comprised a significant portion of total dry weight particularly in stem internodes, and may provide an opportunity for recovery during processing. Conclusions: Cell wall structural differences within a single plant can play a significant role in feedstock properties and have the potential to be exploited for improving biomass processability during a biorefining process. The results from this work demonstrate that cell wall lignin content, while generally exhibiting a negative correlation with enzymatic hydrolysis yields, is not the sole contributor to cell wall recalcitrance across diverse anatomical fractions within switchgrass.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

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

Grant/Contract Number:: FC02-07ER64494; CBET 1336622; AC05-00OR22725

OSTI ID:: 1618683

Alternate ID(s):: OSTI ID: 1418505

Journal Information:: Biotechnology for Biofuels, Vol. 10, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 22 works

Citation information provided by
Web of Science

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Autofluorescence: Biological functions and technical applications García-Plazaola, José Ignacio; Fernández-Marín, Beatriz; Duke, Stephen O. Plant Science, Vol. 236 https://doi.org/10.1016/j.plantsci.2015.03.010	journal	July 2015
Compositional Analysis of Lignocellulosic Feedstocks. 1. Review and Description of Methods Sluiter, Justin B.; Ruiz, Raymond O.; Scarlata, Christopher J. Journal of Agricultural and Food Chemistry, Vol. 58, Issue 16, p. 9043-9053 https://doi.org/10.1021/jf1008023	journal	August 2010
Growth of the plant cell wall Cosgrove, Daniel J. Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11, p. 850-861 https://doi.org/10.1038/nrm1746	journal	November 2005
Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion Lionetti, V.; Francocci, F.; Ferrari, S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 2 https://doi.org/10.1073/pnas.0907549107	journal	December 2009
Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass Chuck, G. S.; Tobias, C.; Sun, L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 42, p. 17550-17555 https://doi.org/10.1073/pnas.1113971108	journal	October 2011
Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy Hutzler, P.; Fischbach, R.; Heller, W. Journal of Experimental Botany, Vol. 49, Issue 323 https://doi.org/10.1093/jxb/49.323.953	journal	June 1998
Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production Slewinski, T. L. Journal of Experimental Botany, Vol. 63, Issue 13 https://doi.org/10.1093/jxb/ers124	journal	June 2012
Cell-wall properties contributing to improved deconstruction by alkaline pre-treatment and enzymatic hydrolysis in diverse maize ( Zea mays L.) lines Li, Muyang; Heckwolf, Marlies; Crowe, Jacob D. Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv016	journal	February 2015
Highly Substituted Glucuronoarabinoxylans (hsGAXs) and Low-Branched Xylans Show a Distinct Localization Pattern in the Tissues of Zea mays L. Suzuki, Kiyoshi; Kitamura, Shinichi; Kato, Yoji Plant and Cell Physiology, Vol. 41, Issue 8 https://doi.org/10.1093/pcp/pcd019	journal	August 2000
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
A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific Endoglucanases Park, Yong Bum; Cosgrove, Daniel J. Plant Physiology, Vol. 158, Issue 4 https://doi.org/10.1104/pp.111.192880	journal	February 2012
A cell wall reference profile for Miscanthus bioenergy crops highlights compositional and structural variations associated with development and organ origin da Costa, Ricardo M. F.; Pattathil, Sivakumar; Avci, Utku New Phytologist, Vol. 213, Issue 4 https://doi.org/10.1111/nph.14306	journal	November 2016
Visualization of plant cell wall lignification using fluorescence-tagged monolignols Tobimatsu, Yuki; Wagner, Armin; Donaldson, Lloyd The Plant Journal, Vol. 76, Issue 3 https://doi.org/10.1111/tpj.12299	journal	August 2013
Feedstocks for Lignocellulosic Biofuels Somerville, Cris; Youngs, Heather; Taylor, Caroline Science, Vol. 329, Issue 5993, p. 790-792 https://doi.org/10.1126/science.1189268	journal	August 2010
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
Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone Wilkerson, C. G.; Mansfield, S. D.; Lu, F. Science, Vol. 344, Issue 6179, p. 90-93 https://doi.org/10.1126/science.1250161	journal	April 2014
Hemicelluloses Scheller, Henrik Vibe; Ulvskov, Peter Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112315	journal	June 2010
Softwood and Hardwood Lignin Fluorescence Spectra of Wood Cell Walls in Different Mounting Media Donaldson, Lloyd IAWA Journal, Vol. 34, Issue 1 https://doi.org/10.1163/22941932-00000002	journal	January 2013
Optimizing harvest of corn stover fractions based on overall sugar yields following ammonia fiber expansion pretreatment and enzymatic hydrolysis Garlock, Rebecca J.; Chundawat, Shishir PS; Balan, Venkatesh Biotechnology for Biofuels, Vol. 2, Issue 1 https://doi.org/10.1186/1754-6834-2-29	journal	January 2009
Structural characterization of alkaline hydrogen peroxide pretreated grasses exhibiting diverse lignin phenotypes Li, Muyang; Foster, Cliff; Kelkar, Shantanu Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-38	journal	January 2012
Enzyme affinity to cell types in wheat straw (Triticum aestivum L.) before and after hydrothermal pretreatment Hansen, Mads AT; Hidayat, Budi J.; Mogensen, Kit K. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-54	journal	January 2013
Tissue-specific distribution of hemicelluloses in six different sugarcane hybrids as related to cell wall recalcitrance Costa, Thales H. F.; Vega-Sánchez, Miguel E.; Milagres, Adriane M. F. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0513-2	journal	May 2016
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Inhibition of microbial biofuel production in drought-stressed switchgrass hydrolysate [Supplemental Data] Ong, Rebecca; Higbee, Alan; Bottoms, Scott figshare-Supplementary information for journal article at DOI: 10.1186/s13068-016-0657-0, 1 PDF file (188.87 kB); 1 CSV file (846.59 kB) https://doi.org/10.6084/m9.figshare.c.3629897.v1	dataset	November 2016

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Evaluating the Role of Ultrasonication-Assisted Alkali Pretreatment and Enzymatic Hydrolysis on Cellwall Polysaccharides of Pennisetum Grass Varieties as Potential Biofuel Feedstock Mohapatra, Sonali; Mishra, Chinmaya; Merritt, Brian B. ChemistrySelect, Vol. 4, Issue 3 https://doi.org/10.1002/slct.201802187	journal	January 2019
Modified expression of ZmMYB167 in Brachypodium distachyon and Zea mays leads to increased cell wall lignin and phenolic content Bhatia, Rakesh; Dalton, Sue; Roberts, Luned A. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-45225-9	journal	June 2019
Nutrient and drought stress: implications for phenology and biomass quality in miscanthus da Costa, Ricardo M. F.; Simister, Rachael; Roberts, Luned A. Annals of Botany, Vol. 124, Issue 4 https://doi.org/10.1093/aob/mcy155	journal	August 2018
Desirable plant cell wall traits for higher-quality miscanthus lignocellulosic biomass da Costa, Ricardo M. F.; Pattathil, Sivakumar; Avci, Utku Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1426-7	journal	April 2019
Lignin-Based Polyurethanes: Opportunities for Bio-Based Foams, Elastomers, Coatings and Adhesives Alinejad, Mona; Henry, Christián; Nikafshar, Saeid Polymers, Vol. 11, Issue 7 https://doi.org/10.3390/polym11071202	journal	July 2019
Desirable plant cell wall traits for higher-quality miscanthus lignocellulosic biomass da Costa, Ricardo M. F.; Pattathil, Sivakumar; Avci, Utku Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1426-7	journal	April 2019
Lignin-Based Polyurethanes: Opportunities for Bio-Based Foams, Elastomers, Coatings and Adhesives Alinejad, Mona; Henry, Christián; Nikafshar, Saeid Polymers, Vol. 11, Issue 7 https://doi.org/10.3390/polym11071202	journal	July 2019

Linked Research (4)

Figures / Tables (9)

black–red–bright yellow color scheme representing from no binding to strongest binding. The amount of carbohydrate material recovered per gram of AIR is depicted in the bar graphs (green) above the heat maps. The panel on the right-hand side of the heat map shows the groups of mAbs based on the class of cell wall glycan they each recognize" data-ostiid="1618683">

Fig. 7(p. 10) Fig. 7

Fig. 8(p. 12)

Fig. 9(p. 13)

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Related Subjects

09 BIOMASS FUELS
Switchgrass
Recalcitrance
Cell wall glycans
Alkaline pretreatment

Identification of developmental stage and anatomical fraction contributions to cell wall recalcitrance in switchgrass [Supplemental Data] Crowe, Jacob; Feringa, Nicholas; Pattathil, Sivakumar https://doi.org/10.6084/m9.figshare.c.3827599 The current record is supplemented by this figure	figure	July 2017
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MOESM1 of Identification of developmental stage and anatomical fraction contributions to cell wall recalcitrance in switchgrass Crowe, Jacob; Feringa, Nicholas; Pattathil, Sivakumar https://doi.org/10.6084/m9.figshare.c.3827599_d1 The current record is supplemented by this figure	figure	July 2017
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