Cell wall composition and biomass recalcitrance differences within a genotypically diverse set of Brachypodium distachyon inbred lines

Cass, Cynthia L.; Lavell, Anastasiya A.; Santoro, Nicholas; Foster, Cliff E.; Karlen, Steven D.; Smith, Rebecca A.; Ralph, John; Garvin, David F.; Sedbrook, John C.

doi:10.3389/fpls.2016.00708

Title: Cell wall composition and biomass recalcitrance differences within a genotypically diverse set of Brachypodium distachyon inbred lines

Journal Article · 26 May 2016 · Frontiers in Plant Science

DOI: https://doi.org/10.3389/fpls.2016.00708 · OSTI ID:1285953

Cass, Cynthia L. ^[1]; Lavell, Anastasiya A. ^[2]; Santoro, Nicholas ^[3]; Foster, Cliff E. ^[3]; Karlen, Steven D. ^[4]; Smith, Rebecca A. ^[4]; Ralph, John ^[5]; Garvin, David F. ^[2]; Sedbrook, John C. ^[6]

Illinois State Univ., Normal, IL (United States). School of Biological Science; Univ. of Wisconsin-Madison, Madison, WI (United States). U.S. Dept. of Energy Great Lakes Bioenergy Research Center
Univ. of Minnesota, St. Paul, MN (United States). Dept. of Agronomy and Plant Genetics; United States Dept. of Agriculture, Agricultural Research Service, St. Paul, MN (United States). Plant Science Research Unit
Michigan State Univ., East Lansing, MI (United States). U.S. Dept. of Energy Great Lakes Bioenergy Research Center
Univ. of Wisconsin-Madison, Madison, WI (United States). U.S. Dept. of Energy Great Lakes Bioenergy Research Center
Univ. of Wisconsin-Madison, Madison, WI (United States). U.S. Dept. of Energy Great Lakes Bioenergy Research Center; Dept. of Biochemistry
Illinois State Univ., Normal, IL (United States). School of Biological Sciences; Univ. of Wisconsin-Madison, Madison, WI (United States). U.S. Dept. of Energy Great Lakes Bioenergy Research Center

Brachypodium distachyon (Brachypodium) has emerged as a useful model system for studying traits unique to graminaceous species including bioenergy crop grasses owing to its amenability to laboratory experimentation and the availability of extensive genetic and germplasm resources. Considerable natural variation has been uncovered for a variety of traits including flowering time, vernalization responsiveness, and above-ground growth characteristics. However, cell wall composition differences remain underexplored. Therefore, we assessed cell wall-related traits relevant to biomass conversion to biofuels in seven Brachypodium inbred lines that were chosen based on their high level of genotypic diversity as well as available genome sequences and recombinant inbred line (RIL) populations. Senesced stems plus leaf sheaths from these lines exhibited significant differences in acetyl bromide soluble lignin (ABSL), cell wall polysaccharide-derived sugars, hydroxycinnamates content, and syringyl:guaiacyl:p-hydroxyphenyl (S:G:H) lignin ratios. Free glucose, sucrose, and starch content also differed significantly in senesced stems, as did the amounts of sugars released from cell wall polysaccharides (digestibility) upon exposure to a panel of thermochemical pretreatments followed by hydrolytic enzymatic digestion. Correlations were identified between inbred line lignin compositions and plant growth characteristics such as biomass accumulation and heading date (HD), and between amounts of cell wall polysaccharides and biomass digestibility. Finally, stem cell wall p-coumarate and ferulate contents and free-sugars content changed significantly with increased duration of vernalization for some inbred lines. Taken together, these results show that Brachypodium displays substantial phenotypic variation with respect to cell wall composition and biomass digestibility, with some compositional differences correlating with growth characteristics. Moreover, besides influencing HD and biomass accumulation, vernalization was found to affect cell wall composition and free sugars accumulation in some Brachypodium inbred lines, suggesting genetic differences in how vernalization affects carbon flux to polysaccharides. Lastly, the availability of related RIL populations will allow for the genetic and molecular dissection of this natural variation, the knowledge of which may inform ways to genetically improve bioenergy crop grasses.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1285953

Journal Information:: Frontiers in Plant Science, Vol. 7; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 12 works

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Brachypodium distachyon line Bd3-1 resistance is elicited by the barley stripe mosaic virus triple gene block 1 movement protein Lee, Mi Yeon; Yan, Lijie; Gorter, Florien A. Journal of General Virology, Vol. 93, Issue 12 https://doi.org/10.1099/vir.0.045880-0	journal	December 2012
Biological conversion assay using Clostridium phytofermentans to estimate plant feedstock quality Lee, Scott J.; Warnick, Thomas A.; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-5	journal	January 2012
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PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon Woods, Daniel P.; Ream, Thomas S.; Minevich, Gregory Genetics, Vol. 198, Issue 1 https://doi.org/10.1534/genetics.114.166785	journal	July 2014
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EST sequencing and phylogenetic analysis of the model grass Brachypodium distachyon Vogel, John P.; Gu, Yong Qiang; Twigg, Paul Theoretical and Applied Genetics, Vol. 113, Issue 2, p. 186-195 https://doi.org/10.1007/s00122-006-0285-3	journal	May 2006
High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3 Vogel, John; Hill, Theresa Plant Cell Reports, Vol. 27, Issue 3 https://doi.org/10.1007/s00299-007-0472-y	journal	November 2007
Natural Variation of Flowering Time and Vernalization Responsiveness in Brachypodium distachyon Schwartz, Christopher J.; Doyle, Mark R.; Manzaneda, Antonio J. BioEnergy Research, Vol. 3, Issue 1 https://doi.org/10.1007/s12155-009-9069-3	journal	February 2010
A High-Throughput Platform for Screening Milligram Quantities of Plant Biomass for Lignocellulose Digestibility Santoro, Nicholas; Cantu, Shane L.; Tornqvist, Carl-Erik BioEnergy Research, Vol. 3, Issue 1 https://doi.org/10.1007/s12155-009-9074-6	journal	January 2010
The role of pectin in plant morphogenesis Palin, Robert; Geitmann, Anja Biosystems, Vol. 109, Issue 3 https://doi.org/10.1016/j.biosystems.2012.04.006	journal	September 2012
The structure, function, and biosynthesis of plant cell wall pectic polysaccharides Caffall, Kerry Hosmer; Mohnen, Debra Carbohydrate Research, Vol. 344, Issue 14 https://doi.org/10.1016/j.carres.2009.05.021	journal	September 2009
Designing the deconstruction of plant cell walls Mccann, M.; Carpita, N. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.04.001	journal	June 2008
Pathway of p-Coumaric Acid Incorporation into Maize Lignin As Revealed by NMR Ralph, John; Hatfield, Ronald D.; Quideau, Stephane Journal of the American Chemical Society, Vol. 116, Issue 21, p. 9448-9456 https://doi.org/10.1021/ja00100a006	journal	October 1994
Extraction and Isolation of Lignin for Utilization as a Standard to Determine Lignin Concentration Using the Acetyl Bromide Spectrophotometric Method Fukushima, Romualdo S.; Hatfield, Ronald D. Journal of Agricultural and Food Chemistry, Vol. 49, Issue 7 https://doi.org/10.1021/jf010449r	journal	July 2001
Comparison of the Acetyl Bromide Spectrophotometric Method with Other Analytical Lignin Methods for Determining Lignin Concentration in Forage Samples Fukushima, Romualdo S.; Hatfield, Ronald D. Journal of Agricultural and Food Chemistry, Vol. 52, Issue 12, p. 3713-3720 https://doi.org/10.1021/jf035497l	journal	June 2004
Supramolecular Interactions in Secondary Plant Cell Walls: Effect of Lignin Chemical Composition Revealed with the Molecular Theory of Solvation Silveira, Rodrigo L.; Stoyanov, Stanislav R.; Gusarov, Sergey The Journal of Physical Chemistry Letters, Vol. 6, Issue 1 https://doi.org/10.1021/jz502298q	journal	December 2014
Genome sequencing and analysis of the model grass Brachypodium distachyon Nature, Vol. 463, Issue 7282, p. 763-768 https://doi.org/10.1038/nature08747	journal	February 2010
Range of cell-wall alterations enhance saccharification in Brachypodium distachyon mutants Marriott, Poppy E.; Sibout, Richard; Lapierre, Catherine Proceedings of the National Academy of Sciences, Vol. 111, Issue 40 https://doi.org/10.1073/pnas.1414020111	journal	September 2014
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
Effects of PHENYLALANINE AMMONIA LYASE ( PAL ) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium Cass, Cynthia L.; Peraldi, Antoine; Dowd, Patrick F. Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv269	journal	June 2015
Brachypodium distachyon line Bd3-1 resistance is elicited by the barley stripe mosaic virus triple gene block 1 movement protein Lee, Mi Yeon; Yan, Lijie; Gorter, Florien A. Journal of General Virology, Vol. 93, Issue 12 https://doi.org/10.1099/vir.0.045880-0	journal	December 2012
Brachypodium as a Model for the Grasses: Today and the Future Brkljacic, Jelena; Grotewold, Erich; Scholl, Randy Plant Physiology, Vol. 157, Issue 1 https://doi.org/10.1104/pp.111.179531	journal	July 2011
Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon Ream, Thomas S.; Woods, Daniel P.; Schwartz, Christopher J. Plant Physiology, Vol. 164, Issue 2 https://doi.org/10.1104/pp.113.232678	journal	December 2013
Genetic Determinants for Enzymatic Digestion of Lignocellulosic Biomass Are Independent of Those for Lignin Abundance in a Maize Recombinant Inbred Population Penning, Bryan W.; Sykes, Robert W.; Babcock, Nicholas C. Plant Physiology, Vol. 165, Issue 4 https://doi.org/10.1104/pp.114.242446	journal	June 2014
Natural variation of drought response in Brachypodium distachyon Luo, Na; Liu, Jianxiu; Yu, Xiaoqing Physiologia Plantarum, Vol. 141, Issue 1 https://doi.org/10.1111/j.1399-3054.2010.01413.x	journal	October 2010
Exploiting the Brachypodium Tool Box in cereal and grass research Mur, Luis A. J.; Allainguillaume, Joel; Catalán, Pilar New Phytologist, Vol. 191, Issue 2 https://doi.org/10.1111/j.1469-8137.2011.03748.x	journal	May 2011
CGR2 and CGR3 have critical overlapping roles in pectin methylesterification and plant growth in Arabidopsis thaliana Kim, Sang-Jin; Held, Michael A.; Zemelis, Starla The Plant Journal, Vol. 82, Issue 2 https://doi.org/10.1111/tpj.12802	journal	March 2015
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
The Biology of Arabinogalactan Proteins Seifert, Georg J.; Roberts, Keith Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103801	journal	June 2007
Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines Tyler, Ludmila; Fangel, Jonatan U.; Fagerström, Alexandra BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2229-14-25	journal	January 2014
Analysis of saccharification in Brachypodium distachyon stems under mild conditions of hydrolysis Gomez, Leonardo D.; Bristow, Jennifer K.; Statham, Emily R. Biotechnology for Biofuels, Vol. 1, Issue 1 https://doi.org/10.1186/1754-6834-1-15	journal	January 2008
Biological conversion assay using Clostridium phytofermentans to estimate plant feedstock quality Lee, Scott J.; Warnick, Thomas A.; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-5	journal	January 2012
Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique Biotechnology for Biofuels, Vol. 6, Article No. 46 https://doi.org/10.1186/1754-6834-6-46	journal	January 2013
Fine Mapping of the Bsr1 Barley Stripe Mosaic Virus Resistance Gene in the Model Grass Brachypodium distachyon Cui, Yu; Lee, Mi Yeon; Huo, Naxin PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0038333	journal	June 2012
Generation and Characterization of the Western Regional Research Center Brachypodium T-DNA Insertional Mutant Collection Bragg, Jennifer N.; Wu, Jiajie; Gordon, Sean P. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0041916	journal	September 2012
PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon Woods, Daniel P.; Ream, Thomas S.; Minevich, Gregory Genetics, Vol. 198, Issue 1 https://doi.org/10.1534/genetics.114.166785	journal	July 2014
Development of Genetic and Genomic Research Resources for , a New Model System for Grass Crop Research Garvin, David F.; Gu, Yong-Qiang; Hasterok, Robert Crop Science, Vol. 48, Issue Supplement_1 https://doi.org/10.2135/cropsci2007.06.0332tpg	journal	January 2008
Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans Tan, Li; Showalter, Allan M.; Egelund, Jack Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00140	journal	January 2012
Cell wall composition throughout development for the model grass Brachypodium distachyon Rancour, David M.; Marita, Jane M.; Hatfield, Ronald D. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00266	journal	January 2012
Roles of pectin in biomass yield and processing for biofuels Xiao, Chaowen; Anderson, Charles T. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00067	journal	January 2013
Memory of the vernalized state in plants including the model grass Brachypodium distachyon Woods, Daniel P.; Ream, Thomas S.; Amasino, Richard M. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00099	journal	March 2014
Pushing the boundaries of resistance: insights from Brachypodium-rust interactions Figueroa, Melania; Castell-Miller, Claudia V.; Li, Feng Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00558	journal	July 2015
Comprehensive Compositional Analysis of Plant Cell Walls (Lignocellulosic biomass) Part II: Carbohydrates Foster, Cliff E.; Martin, Tina M.; Pauly, Markus Journal of Visualized Experiments, Issue 37 https://doi.org/10.3791/1837-v	journal	March 2010

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Genetic and Quantitative Trait Locus Analysis of Cell Wall Components and Forage Digestibility in the Zheng58 × HD568 Maize RIL Population at Anthesis Stage Li, Kun; Wang, Hongwu; Hu, Xiaojiao Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01472	journal	August 2017
Never the Two Shall Mix: Robust Indel Markers to Ensure the Fidelity of Two Pivotal and Closely-Related Accessions of Brachypodium distachyon Brew-Appiah, Rhoda A. T.; Peracchi, Luigi M.; Sanguinet, Karen A. Plants, Vol. 8, Issue 6 https://doi.org/10.3390/plants8060153	journal	June 2019
Lignin Degradation by Fungal Pretreatment: A Review M., Madadi; A., Abbas Journal of Plant Pathology & Microbiology, Vol. 08, Issue 02 https://doi.org/10.4172/2157-7471.1000398	journal	January 2017

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Related Subjects

09 BIOMASS FUELS
bioenergy
grass
polysaccharide
hemicellulose
lignin
digestibility
vernalization
Pooideae
bromide spectrophotometric method
arabidopsis-thaliana
lignin concentration
natural variation
flowering time
model system
saccharification
conversion
quality