Understanding the Remodelling of Cell Walls during Brachypodium distachyon Grain Development through a Sub-Cellular Quantitative Proteomic Approach

Brachypodium distachyon is a suitable plant model for studying temperate cereal crops, such as wheat, barley or rice, and helpful in the study of the grain cell wall. Indeed, the most abundant hemicelluloses that are in the B. distachyon cell wall of grain are (1-3)(1-4)-β-glucans and arabinoxylans, in a ratio similar to those of cereals such as barley or oat. Conversely, these cell walls contain few pectins and xyloglucans. Cell walls play an important role in grain physiology. The modifications of cell wall polysaccharides that occur during grain development and filling are key in the determination of the size and weight of the cereal grains. The mechanisms required for cell wall assembly and remodelling are poorly understood, especially in cereals. To provide a better understanding of these processes, we purified the cell wall at three developmental stages of the B. distachyon grain. The proteins were then extracted, and a quantitative and comparative LC-MS/MS analysis was performed to investigate the protein profile changes during grain development. Over 466 cell wall proteins (CWPs) were identified and classified according to their predicted functions. This work highlights the different proteome profiles that we could relate to the main phases of grain development and to the reorganization of cell wall polysaccharides that occurs during these different developmental stages. These results provide a good springboard to pursue functional validation to better understand the role of CWPs in the assembly and remodelling of the grain cell wall of cereals.

[1]  A. Ding,et al.  Expansins: roles in plant growth and potential applications in crop improvement , 2016, Plant Cell Reports.

[2]  C. Dunand,et al.  Arabidopsis thaliana root cell wall proteomics: Increasing the proteome coverage using a combinatorial peptide ligand library and description of unexpected Hyp in peroxidase amino acid sequences , 2016, Proteomics.

[3]  H. San Clemente,et al.  Cell wall proteome of sugarcane stems: comparison of a destructive and a non-destructive extraction method showed differences in glycoside hydrolases and peroxidases , 2016, BMC Plant Biology.

[4]  Jérôme Collemare,et al.  The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant–pathogen interactions , 2015, Front. Plant Sci..

[5]  H. Rogniaux,et al.  Cell wall proteomic of Brachypodium distachyon grains: A focus on cell wall remodeling proteins , 2015, Proteomics.

[6]  C. Dunand,et al.  Roles of cell wall peroxidases in plant development. , 2015, Phytochemistry.

[7]  B. Bouchet,et al.  Endomembrane proteomics reveals putative enzymes involved in cell wall metabolism in wheat grain outer layers , 2015, Journal of experimental botany.

[8]  D. Lv,et al.  N-linked glycoproteome profiling of seedling leaf in Brachypodium distachyon L. , 2015, Journal of proteome research.

[9]  H. San Clemente,et al.  WallProtDB, a database resource for plant cell wall proteomics , 2015, Plant Methods.

[10]  Wei Wang,et al.  Over-expression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. , 2015, Journal of plant physiology.

[11]  P. Shewry,et al.  Comparative in situ analyses of cell wall matrix polysaccharide dynamics in developing rice and wheat grain , 2014, Planta.

[12]  T. Girin,et al.  Brachypodium: a promising hub between model species and cereals. , 2014, Journal of experimental botany.

[13]  C. Albenne,et al.  Plant Cell Wall Proteins: A Large Body of Data, but What about Runaways? , 2014, Proteomes.

[14]  C. T. Anderson,et al.  POLYGALACTURONASE INVOLVED IN EXPANSION1 Functions in Cell Elongation and Flower Development in Arabidopsis[C][W] , 2014, Plant Cell.

[15]  B. Bakan,et al.  The Wheat Grain Contains Pectic Domains Exhibiting Specific Spatial and Development-Associated Distribution , 2014, PloS one.

[16]  Matthew R. Tucker,et al.  Grain development in Brachypodium and other grasses: possible interactions between cell expansion, starch deposition, and cell-wall synthesis. , 2013, Journal of experimental botany.

[17]  L. Franková,et al.  Biochemistry and physiological roles of enzymes that 'cut and paste' plant cell-wall polysaccharides. , 2013, Journal of experimental botany.

[18]  H. Clemente,et al.  Brachypodium distachyon as a model plant toward improved biofuel crops: Search for secreted proteins involved in biogenesis and disassembly of cell wall polymers , 2013, Proteomics.

[19]  C. Albenne,et al.  Plant cell wall proteomics: the leadership of Arabidopsis thaliana , 2013, Front. Plant Sci..

[20]  D. Tessier,et al.  Identification of glycosyltransferases involved in cell wall synthesis of wheat endosperm. , 2013, Journal of proteomics.

[21]  F. Guillon,et al.  Cell wall deposition and metabolism in wheat grain , 2012 .

[22]  Sebastian Wolf,et al.  Growth control by cell wall pectins , 2012, Protoplasma.

[23]  Xiaohong Yu,et al.  Acetylesterase-Mediated Deacetylation of Pectin Impairs Cell Elongation, Pollen Germination, and Plant Reproduction[C][W] , 2012, Plant Cell.

[24]  H. Rogniaux,et al.  A comprehensive overview of grain development in Brachypodium distachyon variety Bd21 , 2011, Journal of experimental botany.

[25]  Olivier Langella,et al.  MassChroQ: A versatile tool for mass spectrometry quantification , 2011, Proteomics.

[26]  C. Albenne,et al.  Combining various strategies to increase the coverage of the plant cell wall glycoproteome. , 2011, Phytochemistry.

[27]  S. A. Bokhari,et al.  Comparative Proteomics Analysis of the Root Apoplasts of Rice Seedlings in Response to Hydrogen Peroxide , 2011, PloS one.

[28]  J. Doonan,et al.  Endosperm development in Brachypodium distachyon , 2010, Journal of experimental botany.

[29]  G. Tuskan,et al.  Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon , 2010, BMC Genomics.

[30]  F. Guillon,et al.  Brachypodium distachyon grain: identification and subcellular localization of storage proteins , 2010, Journal of experimental botany.

[31]  Sai Guna Ranjan Gurazada,et al.  Genome sequencing and analysis of the model grass Brachypodium distachyon , 2010, Nature.

[32]  X. C. Lizana,et al.  Expansins expression is associated with grain size dynamics in wheat (Triticum aestivum L.) , 2010, Journal of experimental botany.

[33]  B. Bouchet,et al.  Wheat endosperm cell walls: Spatial heterogeneity of polysaccharide structure and composition using micro-scale enzymatic fingerprinting and FT-IR microspectroscopy , 2009 .

[34]  W. Van den Ende,et al.  Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. , 2009, Journal of experimental botany.

[35]  H. Clemente,et al.  Bioinformatics as a Tool for Assessing the Quality of Sub-Cellular Proteomic Strategies and Inferring Functions of Proteins: Plant Cell Wall Proteomics as a Test Case , 2009, Bioinformatics and biology insights.

[36]  M. Irshad,et al.  A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: Confirmed actors and newcomers , 2008, BMC Plant Biology.

[37]  J. Vogel Unique aspects of the grass cell wall. , 2008, Current opinion in plant biology.

[38]  J. Knox Revealing the structural and functional diversity of plant cell walls. , 2008, Current opinion in plant biology.

[39]  Z. Minić Physiological roles of plant glycoside hydrolases , 2008, Planta.

[40]  J. Rose,et al.  The biochemistry and biology of extracellular plant lipid‐transfer proteins (LTPs) , 2008, Protein science : a publication of the Protein Society.

[41]  C. Albenne,et al.  Recent advances in plant cell wall proteomics , 2008, Proteomics.

[42]  Jian-feng Zhang,et al.  A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis , 2007, Planta.

[43]  A. Carvalho,et al.  Role of plant lipid transfer proteins in plant cell physiology—A concise review , 2007, Peptides.

[44]  G. Fincher,et al.  A Barley Xyloglucan Xyloglucosyl Transferase Covalently Links Xyloglucan, Cellulosic Substrates, and (1,3;1,4)-β-D-Glucans* , 2007, Journal of Biological Chemistry.

[45]  M. Irshad,et al.  Evaluation of cell wall preparations for proteomics: a new procedure for purifying cell walls from Arabidopsis hypocotyls , 2006, Plant Methods.

[46]  D. Cosgrove Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[47]  M. Pauly,et al.  XTH acts at the microfibril-matrix interface during cell elongation. , 2005, Journal of experimental botany.

[48]  Jürgen Pleiss,et al.  Molecular modeling of family GH16 glycoside hydrolases: Potential roles for xyloglucan transglucosylases/hydrolases in cell wall modification in the poaceae , 2004, Protein science : a publication of the Protein Society.

[49]  C. Dunand,et al.  Performing the paradoxical: how plant peroxidases modify the cell wall. , 2004, Trends in plant science.

[50]  S. Fry Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. , 2004, The New phytologist.

[51]  Makoto Takano,et al.  Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. , 2002, Plant & cell physiology.

[52]  J. Draper,et al.  Brachypodium distachyon. A new model system for functional genomics in grasses. , 2001, Plant physiology.

[53]  R. Burton,et al.  Barley arabinoxylan arabinofuranohydrolases: purification, characterization and determination of primary structures from cDNA clones. , 2001, The Biochemical journal.

[54]  B. Bouchet,et al.  Brachypodium distachyon grain: characterization of endosperm cell walls. , 2011, Journal of experimental botany.

[55]  H. Scheller,et al.  Characterization of the primary cell walls of seedlings of Brachypodium distachyon--a potential model plant for temperate grasses. , 2010, Phytochemistry.

[56]  U. Sonnewald,et al.  Functional characterisation of Nicotiana tabacum xyloglucan endotransglycosylase (NtXET-1): generation of transgenic tobacco plants and changes in cell wall xyloglucan , 2001, Planta.