Comparing genomic expression patterns across plant species reveals highly diverged transcriptional dynamics in response to salt stress

BackgroundRice and barley are both members of Poaceae (grass family) but have a marked difference in salt tolerance. The molecular mechanism underlying this difference was previously unexplored. This study employs a comparative genomics approach to identify analogous and contrasting gene expression patterns between rice and barley.ResultsA hierarchical clustering approach identified several interesting expression trajectories among rice and barley genotypes. There were no major conserved expression patterns between the two species in response to salt stress. A wheat salt-stress dataset was queried for comparison with rice and barley. Roughly one-third of the salt-stress responses of barley were conserved with wheat while overlap between wheat and rice was minimal. These results demonstrate that, at transcriptome level, rice is strikingly different compared to the more closely related barley and wheat. This apparent lack of analogous transcriptional programs in response to salt stress is further highlighted through close examination of genes associated with root growth and development.ConclusionThe analysis provides support for the hypothesis that conservation of transcriptional signatures in response to environmental cues depends on the genetic similarity among the genotypes within a species, and on the phylogenetic distance between the species.

[1]  G. Ólafsdóttir,et al.  The oleate-stimulated phospholipase D, PLDdelta, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. , 2003, The Plant cell.

[2]  Xing Wang Deng,et al.  Conservation and Divergence of Light-Regulated Genome Expression Patterns during Seedling Development in Rice and Arabidopsis[W] , 2005, The Plant Cell Online.

[3]  D. Hartl,et al.  Population genetic variation in genome-wide gene expression. , 2003, Molecular biology and evolution.

[4]  Hong Wang,et al.  Gene Expression Profiles during the Initial Phase of Salt Stress in Rice , 2001, Plant Cell.

[5]  B. Forster Mutation genetics of salt tolerance in barley: An assessment of Golden Promise and other semi-dwarf mutants , 2004, Euphytica.

[6]  J. Bennetzen,et al.  Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. , 2002, Genetics.

[7]  D. Galbraith,et al.  Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley , 2004, Plant Molecular Biology.

[8]  Matthew A. Zapala,et al.  Elevated gene expression levels distinguish human from non-human primate brains , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[9]  H. Bohnert,et al.  Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[10]  D. Crawford,et al.  Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus , 2005, Nature Genetics.

[11]  A. Whitehead,et al.  Variation in tissue-specific gene expression among natural populations , 2005, Genome Biology.

[12]  Jian Wang,et al.  A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. , 2005, Genome research.

[13]  J. Dvorak,et al.  RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines , 2002 .

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

[15]  Magnus Holm,et al.  Arabidopsis CONSTANS-LIKE3 Is a Positive Regulator of Red Light Signaling and Root Growth[W] , 2005, The Plant Cell Online.

[16]  L. Kruglyak,et al.  Genetic Dissection of Transcriptional Regulation in Budding Yeast , 2002, Science.

[17]  Pascal Condamine,et al.  Array-based genotyping and expression analysis of barley cv. Maythorpe and Golden Promise , 2007, BMC Genomics.

[18]  E. Lombi,et al.  Salinity induced differences in growth, ion distribution and partitioning in barley between the cultivar Maythorpe and its derived mutant Golden Promise , 2004, Plant and Soil.

[19]  M. Ohta,et al.  LOS2, a genetic locus required for cold‐responsive gene transcription encodes a bi‐functional enolase , 2002, The EMBO journal.

[20]  Russell D. Wolfinger,et al.  The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster , 2001, Nature Genetics.

[21]  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.

[22]  Paulo A. S. Nuin,et al.  Transcriptional Profiling Implicates Novel Interactions between Abiotic Stress and Hormonal Responses in Thellungiella, a Close Relative of Arabidopsis1[W] , 2006, Plant Physiology.

[23]  L. Zeng,et al.  Salinity Effects on Seedling Growth and Yield Components of Rice , 2000 .

[24]  Daniel L. Mace,et al.  Cell Identity Mediates the Response of Arabidopsis Roots to Abiotic Stress , 2008, Science.

[25]  Pascal Condamine,et al.  Comparative Transcriptional Profiling of Two Contrasting Rice Genotypes under Salinity Stress during the Vegetative Growth Stage1[w] , 2005, Plant Physiology.

[26]  R. Wang,et al.  Comparative transcriptome analysis of salt-tolerant wheat germplasm lines using wheat genome arrays , 2007 .

[27]  E. Wurtele,et al.  An mRNA Putatively Coding for an O-Methyltransferase Accumulates Preferentially in Maize Roots and Is Located Predominantly in the Region of the Endodermis , 1993, Plant physiology.

[28]  T. Takabe,et al.  Comparative transcriptome analyses of barley and rice under salt stress , 2006, Theoretical and Applied Genetics.

[29]  Jake K. Byrnes,et al.  Whole genome transcriptome polymorphisms in Arabidopsis thaliana , 2008, Genome Biology.

[30]  T. Flowers,et al.  The Contribution of an Apoplastic Pathway to Sodium Uptake by Rice Roots in Saline Conditions , 1987 .

[31]  G. Ólafsdóttir,et al.  The Oleate-Stimulated Phospholipase D, PLDδ, and Phosphatidic Acid Decrease H2O2-Induced Cell Death in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/ 10.1105/tpc.013961. , 2003, The Plant Cell Online.

[32]  J. Salse,et al.  Identification and Characterization of Shared Duplications between Rice and Wheat Provide New Insight into Grass Genome Evolution[W] , 2008, The Plant Cell Online.