Cell Wall Composition and Candidate Biosynthesis Gene Expression During Rice Development

Lin, Fan; Manisseri, Chithra; Fagerström, Alexandra; Peck, Matthew L.; Vega-Sánchez, Miguel E.; Williams, Brian; Chiniquy, Dawn M.; Saha, Prasenjit; Pattathil, Sivakumar; Conlin, Brian; Zhu, Lan; Hahn, Michael G.; Willats, William G. T.; Scheller, Henrik V.; Ronald, Pamela C.; Bartley, Laura E.

doi:10.1093/pcp/pcw125

Title: Cell Wall Composition and Candidate Biosynthesis Gene Expression During Rice Development

Journal Article · Mon Aug 01 00:00:00 EDT 2016 · Plant and Cell Physiology

DOI:https://doi.org/10.1093/pcp/pcw125· OSTI ID:1379223

Lin, Fan; Manisseri, Chithra; Fagerström, Alexandra; Peck, Matthew L.; Vega-Sánchez, Miguel E.; Williams, Brian; Chiniquy, Dawn M.; Saha, Prasenjit; Pattathil, Sivakumar; Conlin, Brian; Zhu, Lan; Hahn, Michael G.; Willats, William G. T.; Scheller, Henrik V.; Ronald, Pamela C.; Bartley, Laura E.

Cell walls of grasses, including cereal crops and biofuel grasses, comprise the majority of plant biomass and intimately influence plant growth, development and physiology. However, the functions of many cell wall synthesis genes, and the relationships among and the functions of cell wall components remain obscure. To better understand the patterns of cell wall accumulation and identify genes that act in grass cell wall biosynthesis, we characterized 30 samples from aerial organs of rice (Oryza sativa cv. Kitaake) at 10 developmental time points, 3-100 d post-germination. Within these samples, we measured 15 cell wall chemical components, enzymatic digestibility and 18 cell wall polysaccharide epitopes/ligands. We also used quantitative reverse transcription-PCR to measure expression of 50 glycosyltransferases, 15 acyltransferases and eight phenylpropanoid genes, many of which had previously been identified as being highly expressed in rice. Most cell wall components vary significantly during development, and correlations among them support current understanding of cell walls. We identified 92 significant correlations between cell wall components and gene expression and establish nine strong hypotheses for genes that synthesize xylans, mixed linkage glucan and pectin components. This work provides an extensive analysis of cell wall composition throughout rice development, identifies genes likely to synthesize grass cell walls, and provides a framework for development of genetically improved grasses for use in lignocellulosic biofuel production and agriculture.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

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

DOE Contract Number:: AC02-05CH11231

OSTI ID:: 1379223

Journal Information:: Plant and Cell Physiology, Vol. 57, Issue 10; ISSN 0032-0781

Publisher:: Japanese Society of Plant Physiologists

Country of Publication:: United States

Language:: English

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Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases Rennie, Emilie A.; Hansen, Sara Fasmer; Baidoo, Edward E. K. Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.200964	journal	June 2012
Xylan biosynthesis Rennie, Emilie A.; Scheller, Henrik Vibe Current Opinion in Biotechnology, Vol. 26 https://doi.org/10.1016/j.copbio.2013.11.013	journal	April 2014
Tensile Properties of Arabidopsis Cell Walls Depend on Both a Xyloglucan Cross-Linked Microfibrillar Network and Rhamnogalacturonan II-Borate Complexes Ryden, Peter; Sugimoto-Shirasu, Keiko; Smith, Andrew Charles Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.103.021873	journal	May 2003
Involvement of cell wall-bound phenolic acids in decrease in cell wall susceptibility to expansins during the cessation of rapid growth in internodes of floating rice Sasayama, Daisuke; Azuma, Tetsushi; Itoh, Kazuyuki Journal of Plant Physiology, Vol. 168, Issue 2 https://doi.org/10.1016/j.jplph.2010.06.010	journal	January 2011
Glycosyltransferases and cell wall biosynthesis: novel players and insights Scheible, Wolf-Rüdiger; Pauly, Markus Current Opinion in Plant Biology, Vol. 7, Issue 3 https://doi.org/10.1016/j.pbi.2004.03.006	journal	June 2004
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
Temporal and Spatial Variation in Switchgrass Biomass Composition and Theoretical Ethanol Yield Schmer, M. R.; Vogel, K. P.; Mitchell, R. B. Agronomy Journal, Vol. 104, Issue 1 https://doi.org/10.2134/agronj2011.0195	journal	January 2012
Structural Redesigning Arabidopsis Lignins into Alkali-Soluble Lignins through the Expression of p- Coumaroyl-CoA:Monolignol Transferase PMT Sibout, Richard; Le Bris, Philippe; Legée, Frédéric Plant Physiology, Vol. 170, Issue 3 https://doi.org/10.1104/pp.15.01877	journal	January 2016
Structural characterization of a mixed-linkage glucan deficient mutant reveals alteration in cellulose microfibril orientation in rice coleoptile mesophyll cell walls Smith-Moritz, Andreia M.; Hao, Zhao; Fernández-Niño, Susana G. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00628	journal	August 2015
Statistical significance for genomewide studies Storey, J. D.; Tibshirani, R. Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445 https://doi.org/10.1073/pnas.1530509100	journal	July 2003
Leaf shape and anatomy as indicators of phase change in the grasses: comparison of maize, rice, and bluegrass Sylvester, Anne W.; Parker-Clark, Vickie; Murray, Glen A. American Journal of Botany, Vol. 88, Issue 12 https://doi.org/10.2307/3558377	journal	December 2001
Digestibility of silages in relation to their hydroxycinnamic acid content and lignin composition Taboada, Alfredo; Novo-Uzal, Esther; Flores, Gonzalo Journal of the Science of Food and Agriculture, Vol. 90, Issue 7 https://doi.org/10.1002/jsfa.3933	journal	May 2010
An Arabidopsis Cell Wall Proteoglycan Consists of Pectin and Arabinoxylan Covalently Linked to an Arabinogalactan Protein Tan, Li; Eberhard, Stefan; Pattathil, Sivakumar The Plant Cell, Vol. 25, Issue 1 https://doi.org/10.1105/tpc.112.107334	journal	January 2013
Cell Wall Composition and Bioenergy Potential of Rice Straw Tissues Are Influenced by Environment, Tissue Type, and Genotype Tanger, Paul; Vega-Sánchez, Miguel E.; Fleming, Margaret BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-014-9573-y	journal	January 2015
A beta-(14)-xylosyltransferase involved in the synthesis of arabinoxylans in developing barley endosperms Urahara, Takeshi; Tsuchiya, Kouji; Kotake, Toshihisa Physiologia Plantarum, Vol. 122, Issue 2 https://doi.org/10.1111/j.0031-9317.2004.00390.x	journal	October 2004
Two Arabidopsis proteins synthesize acetylated xylan in vitro Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A. The Plant Journal, Vol. 80, Issue 2 https://doi.org/10.1111/tpj.12643	journal	September 2014
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
Engineering temporal accumulation of a low recalcitrance polysaccharide leads to increased C6 sugar content in plant cell walls Vega-Sánchez, Miguel E.; Loqué, Dominique; Lao, Jeemeng Plant Biotechnology Journal, Vol. 13, Issue 7 https://doi.org/10.1111/pbi.12326	journal	January 2015
Loss of Cellulose Synthase - Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice Vega-Sánchez, Miguel E.; Verhertbruggen, Yves; Christensen, Ulla Plant Physiology, Vol. 159, Issue 1 https://doi.org/10.1104/pp.112.195495	journal	March 2012
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
Investigation of cell wall composition related to stem lodging resistance in wheat ( Triticum aestivum L.) by FTIR spectroscopy Wang, Jian; Zhu, Jinmao; Huang, RuZhu Plant Signaling & Behavior, Vol. 7, Issue 7 https://doi.org/10.4161/psb.20468	journal	July 2012
Determining the Subcellular Location of Synthesis and Assembly of the Cell Wall Polysaccharide (1,3; 1,4)-β-d-Glucan in Grasses Wilson, Sarah M.; Ho, Yin Ying; Lampugnani, Edwin R. The Plant Cell, Vol. 27, Issue 3 https://doi.org/10.1105/tpc.114.135970	journal	March 2015
Identification of Grass-specific Enzyme That Acylates Monolignols with p-Coumarate Withers, Saunia; Lu, Fachuang; Kim, Hoon Journal of Biological Chemistry, Vol. 287, Issue 11, p. 8347-8355 https://doi.org/10.1074/jbc.M111.284497	journal	January 2012
Overexpression of AtLOV1 in Switchgrass Alters Plant Architecture, Lignin Content, and Flowering Time Xu, Bin; Sathitsuksanoh, Noppadon; Tang, Yuhong PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0047399	journal	December 2012
Evolution of mixed-linkage (1 → 3, 1 → 4)-β-d-glucan (MLG) and xyloglucan in Equisetum (horsetails) and other monilophytes Xue, Xinxin; Fry, Stephen C. Annals of Botany, Vol. 109, Issue 5 https://doi.org/10.1093/aob/mcs018	journal	February 2012
A Transporter Regulating Silicon Distribution in Rice Shoots Yamaji, Naoki; Mitatni, Namiki; Ma, Jian Feng The Plant Cell, Vol. 20, Issue 5 https://doi.org/10.1105/tpc.108.059311	journal	May 2008
Comprehensive Flavonol Profiling and Transcriptome Coexpression Analysis Leading to Decoding Gene–Metabolite Correlations in Arabidopsis Yonekura-Sakakibara, Keiko; Tohge, Takayuki; Matsuda, Fumio The Plant Cell, Vol. 20, Issue 8 https://doi.org/10.1105/tpc.108.058040	journal	August 2008
Biochemical control of xylan biosynthesis — which end is up? York, W.; Oneill, M. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.02.007	journal	June 2008
A Glucurono(arabino)xylan Synthase Complex from Wheat Contains Members of the GT43, GT47, and GT75 Families and Functions Cooperatively Zeng, Wei; Jiang, Nan; Nadella, Ramya Plant Physiology, Vol. 154, Issue 1 https://doi.org/10.1104/pp.110.159749	journal	July 2010
GOLD HULL AND INTERNODE2 Encodes a Primarily Multifunctional Cinnamyl-Alcohol Dehydrogenase in Rice Zhang, Kewei; Qian, Qian; Huang, Zejun Plant Physiology, Vol. 140, Issue 3 https://doi.org/10.1104/pp.105.073007	journal	January 2006
Altering the Cell Wall and Its Impact on Plant Disease: From Forage to Bioenergy Zhao, Qiao; Dixon, Richard A. Annual Review of Phytopathology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-phyto-082712-102237	journal	August 2014

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