Analysis of Global Gene Expression in Brachypodium distachyon Reveals Extensive Network Plasticity in Response to Abiotic Stress

Brachypodium distachyon is a close relative of many important cereal crops. Abiotic stress tolerance has a significant impact on productivity of agriculturally important food and feedstock crops. Analysis of the transcriptome of Brachypodium after chilling, high-salinity, drought, and heat stresses revealed diverse differential expression of many transcripts. Weighted Gene Co-Expression Network Analysis revealed 22 distinct gene modules with specific profiles of expression under each stress. Promoter analysis implicated short DNA sequences directly upstream of module members in the regulation of 21 of 22 modules. Functional analysis of module members revealed enrichment in functional terms for 10 of 22 network modules. Analysis of condition-specific correlations between differentially expressed gene pairs revealed extensive plasticity in the expression relationships of gene pairs. Photosynthesis, cell cycle, and cell wall expression modules were down-regulated by all abiotic stresses. Modules which were up-regulated by each abiotic stress fell into diverse and unique gene ontology GO categories. This study provides genomics resources and improves our understanding of abiotic stress responses of Brachypodium.

[1]  Haiyan Wu,et al.  Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array , 2008, BMC Genomics.

[2]  Justin N. Vaughn,et al.  Reference genome sequence of the model plant Setaria , 2012, Nature Biotechnology.

[3]  Chungui Lu,et al.  Plant responses to cold: Transcriptome analysis of wheat. , 2010, Plant biotechnology journal.

[4]  Zhou Du,et al.  agriGO: a GO analysis toolkit for the agricultural community , 2010, Nucleic Acids Res..

[5]  Shoshi Kikuchi,et al.  Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. , 2004, Physiological genomics.

[6]  Rolf Apweiler,et al.  InterProScan - an integration platform for the signature-recognition methods in InterPro , 2001, Bioinform..

[7]  Henry D. Priest,et al.  Genome-wide mapping of alternative splicing in Arabidopsis thaliana. , 2010, Genome research.

[8]  Samuel E. Fox,et al.  Comparative analyses reveal potential uses of Brachypodium distachyon as a model for cold stress responses in temperate grasses , 2012, BMC Plant Biology.

[9]  A. D. Cullmann,et al.  Linking the Salt Transcriptome with Physiological Responses of a Salt-Resistant Populus Species as a Strategy to Identify Genes Important for Stress Acclimation1[W][OA] , 2010, Plant Physiology.

[10]  Jian-bo Wang,et al.  DNA-methylation changes induced by salt stress in wheat Triticum aestivum , 2009 .

[11]  W. Lopushinsky.  Stomatal Closure in Conifer Seedlings in Response to Leaf Moisture Stress , 1969, Botanical Gazette.

[12]  T. Sakurai,et al.  Genome sequence of the palaeopolyploid soybean , 2010, Nature.

[13]  F. Turano,et al.  Characterization of two glutamate decarboxylase cDNA clones from Arabidopsis. , 1998, Plant physiology.

[14]  Peter Langfelder,et al.  Fast R Functions for Robust Correlations and Hierarchical Clustering. , 2012, Journal of statistical software.

[15]  Hongtao Liu,et al.  Calmodulin Is Involved in Heat Shock Signal Transduction in Wheat1 , 2003, Plant Physiology.

[16]  Masakazu Satou,et al.  Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. , 2008, Plant & cell physiology.

[17]  John A. Hamilton,et al.  The TIGR Rice Genome Annotation Resource: improvements and new features , 2006, Nucleic Acids Res..

[18]  T. Hahn,et al.  Altered expression of pyrophosphate: Fructose-6-phosphate 1-phosphotransferase affects the growth of transgenic Arabidopsis plants , 2009, Molecules and cells.

[19]  J. Flexas,et al.  Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. , 2007, Plant, cell & environment.

[20]  J. Zhu,et al.  Cell signaling under salt, water and cold stresses. , 2001, Current opinion in plant biology.

[21]  C. Abdelly,et al.  Calcium Signaling via Phospholipase C Is Essential for Proline Accumulation upon Ionic But Not Nonionic Hyperosmotic Stresses in Arabidopsis1 , 2007, Plant Physiology.

[22]  J. J. Grant,et al.  CBL1, a Calcium Sensor That Differentially Regulates Salt, Drought, and Cold Responses in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012393. , 2003, The Plant Cell Online.

[23]  S. Reader,et al.  Breeding for abiotic stresses for sustainable agriculture , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[25]  Rafael A Irizarry,et al.  Exploration, normalization, and summaries of high density oligonucleotide array probe level data. , 2003, Biostatistics.

[26]  Colleen J. Doherty,et al.  Roles for Arabidopsis CAMTA Transcription Factors in Cold-Regulated Gene Expression and Freezing Tolerance[W][OA] , 2009, The Plant Cell Online.

[27]  A. Portis,et al.  Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. , 2005, Plant & cell physiology.

[28]  Birgit Kersten,et al.  PlnTFDB: updated content and new features of the plant transcription factor database , 2009, Nucleic Acids Res..

[29]  A. Trewavas,et al.  Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. , 1996, The Plant cell.

[30]  A. Altman,et al.  Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance , 2003, Planta.

[31]  Kris Freeman,et al.  Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle , 2007, Plant Molecular Biology.

[32]  Yeon-Ki Kim,et al.  Coexpression network analysis associated with call of rice seedlings for encountering heat stress , 2013, Plant Molecular Biology.

[33]  L. Tippett.  Statistical Tables: For Biological, Agricultural and Medical Research , 1954 .

[34]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[35]  R. A. Fisher,et al.  Statistical Tables for Biological, Agricultural and Medical Research , 1956 .

[36]  E. Stockinger,et al.  Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Alexandre V Morozov,et al.  Gene regulation by nucleosome positioning. , 2010, Trends in genetics : TIG.

[38]  R. Tibshirani,et al.  Significance analysis of microarrays applied to the ionizing radiation response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Araus,et al.  Plant breeding and drought in C3 cereals: what should we breed for? , 2002, Annals of botany.

[40]  K. Shinozaki,et al.  A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. , 1994, The Plant cell.

[41]  J. Peñuelas,et al.  Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. , 2005, Plant Ecology.

[42]  Narendra Tuteja,et al.  Mechanisms of high salinity tolerance in plants. , 2007, Methods in enzymology.

[43]  Trey Ideker,et al.  Cytoscape 2.8: new features for data integration and network visualization , 2010, Bioinform..

[44]  Kathleen Marchal,et al.  PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences , 2002, Nucleic Acids Res..

[45]  Stephen P. Ficklin,et al.  Maximizing capture of gene co-expression relationships through pre-clustering of input expression samples: an Arabidopsis case study , 2013, BMC Systems Biology.

[46]  K. Shinozaki,et al.  ABA-mediated transcriptional regulation in response to osmotic stress in plants , 2011, Journal of Plant Research.

[47]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[48]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[49]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[50]  Christoph Benning,et al.  Freezing Tolerance in Plants Requires Lipid Remodeling at the Outer Chloroplast Membrane , 2010, Science.

[51]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools , 2011, Nucleic Acids Res..

[52]  Connor W. McEntee,et al.  Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules , 2007, PLoS genetics.

[53]  Kazuo Shinozaki,et al.  Global Landscape of a Co-Expressed Gene Network in Barley and its Application to Gene Discovery in Triticeae Crops , 2011, Plant & cell physiology.

[54]  Kazuo Shinozaki,et al.  Research on plant abiotic stress responses in the post-genome era: past, present and future. , 2010, The Plant journal : for cell and molecular biology.

[55]  T. Demura,et al.  Mutations in MYB3R1 and MYB3R4 Cause Pleiotropic Developmental Defects and Preferential Down-Regulation of Multiple G2/M-Specific Genes in Arabidopsis1[C][W] , 2011, Plant Physiology.

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

[57]  D. Roby,et al.  Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence , 2013, Nature Communications.

[58]  Mihaela M. Martis,et al.  The Sorghum bicolor genome and the diversification of grasses , 2009, Nature.

[59]  G. Erice,et al.  Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.) , 2010, Journal of experimental botany.

[60]  Yin Hoon Chew,et al.  A stress-free walk from Arabidopsis to crops. , 2011, Current opinion in biotechnology.

[61]  Jinfang Tan,et al.  Role of calcium ion in protection against heat and high irradiance stress-induced oxidative damage to photosynthesis of wheat leaves , 2005, Photosynthetica.

[62]  David M. Goodstein,et al.  Phytozome: a comparative platform for green plant genomics , 2011, Nucleic Acids Res..

[63]  T. Mockler,et al.  Plant abiotic stress: insights from the genomics era , 2011 .

[64]  E. Vierling,et al.  Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. , 2001, Plant physiology.

[65]  S. Sopory,et al.  Stress-mediated alterations in chromatin architecture correlate with down-regulation of a gene encoding 60S rpL32 in rice. , 2013, Plant & cell physiology.

[66]  N. Tuteja,et al.  Cold, salinity and drought stresses: an overview. , 2005, Archives of biochemistry and biophysics.

[67]  M. Ashraf,et al.  Artemisia L. species recognized by the local community of the northern areas of Pakistan as folk therapeutic plants , 2010 .

[68]  Gunnar Rätsch,et al.  Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. , 2009, The Plant journal : for cell and molecular biology.

[69]  E. Bornberg-Bauer,et al.  The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. , 2007, The Plant journal : for cell and molecular biology.

[70]  M. Lauria,et al.  Epigenetic control of gene regulation in plants. , 2011, Biochimica et biophysica acta.

[71]  Søren Lindemose,et al.  Structure, Function and Networks of Transcription Factors Involved in Abiotic Stress Responses , 2013, International journal of molecular sciences.