Identification of Cold-Induced Genes in Cereal Crops and Arabidopsis Through Comparative Analysis of Multiple EST Sets

Freezing tolerance in plants is obtained during a period of low nonfreezing temperatures before the winter sets on, through a biological process known as cold acclimation. Cold is one of the major stress factors that limits the growth, productivity and distribution of plants, and understanding the mechanism of cold tolerance is therefore important for crop improvement. Expressed sequence tags (EST) analysis is a powerful, economical and time-efficient way of assembling information on the transcriptome. To date, several EST sets have been generated from cold-induced cDNA libraries from several different plant species. In this study we utilize the variation in the frequency of ESTs sampled from different cold-stressed plant libraries, in order to identify genes preferentially expressed in cold in comparison to a number of control sets. The species included in the comparative study are oat (Avena sativa), barley (Hordeum vulgare), wheat (Triticum aestivum), rice (Oryza sativa) and Arabidopsis thaliana. However, in order to get comparable gene expression estimates across multiple species and data sets, we choose to compare the expression of tentative ortholog groups (TOGs) instead of single genes, as in the normal procedure. We consider TOGs as preferentially expressed if they are detected as differentially expressed by a test statistic and up-regulated in comparison to all control sets, and/or uniquely expressed during cold stress, i.e., not present in any of the control sets. The result of this analysis revealed a diverse representation of genes in the different species. In addition, the derived TOGs mainly represent genes that are long-term highly or moderately expressed in response to cold and/or other stresses.

[1]  H. Paulsen,et al.  The N‐terminal domain of the light‐harvesting chlorophyll a/b‐binding protein complex (LHCII) is essential for its acclimative proteolysis , 2000, FEBS letters.

[2]  J. Claverie,et al.  The significance of digital gene expression profiles. , 1997, Genome research.

[3]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[4]  Ji-yeon Lee,et al.  Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress , 2003, Plant Molecular Biology.

[5]  D. J. Widgery,et al.  From laboratory to field , 2003 .

[6]  Jing Li,et al.  The WRKY family of transcription factors in rice and Arabidopsis and their origins. , 2005, DNA research : an international journal for rapid publication of reports on genes and genomes.

[7]  D. Bowles,et al.  Plants in a cold climate. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[9]  J. Claverie Computational methods for the identification of differential and coordinated gene expression. , 1999, Human molecular genetics.

[10]  C. Guy,et al.  Coordinate and non-coordinate expression of the stress 70 family and other molecular chaperones at high and low temperature in spinach and tomato , 2004, Plant Molecular Biology.

[11]  M. Thomashow,et al.  Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[12]  G. Pertea,et al.  Cross-referencing eukaryotic genomes: TIGR Orthologous Gene Alignments (TOGA). , 2002, Genome research.

[13]  A. Halpern,et al.  Massive parallelism, randomness and genomic advances , 2003, Nature Genetics.

[14]  D. Stekel,et al.  The comparison of gene expression from multiple cDNA libraries. , 2000, Genome research.

[15]  K H Buetow,et al.  In silico analysis of cancer through the Cancer Genome Anatomy Project. , 2001, Trends in cell biology.

[16]  J. Browse,et al.  Temperature sensing and cold acclimation. , 2001, Current opinion in plant biology.

[17]  John Quackenbush,et al.  The TIGR Gene Indices: reconstruction and representation of expressed gene sequences , 2000, Nucleic Acids Res..

[18]  Matthew A Hannah,et al.  A Global Survey of Gene Regulation during Cold Acclimation in Arabidopsis thaliana , 2005, PLoS genetics.

[19]  K. Akiyama,et al.  Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. , 2002, The Plant journal : for cell and molecular biology.

[20]  S. Bortoluzzi,et al.  Detecting differentially expressed genes in multiple tag sampling experiments: comparative evaluation of statistical tests. , 2001, Human molecular genetics.

[21]  J. Forster,et al.  Gene expression and genetic mapping analyses of a perennial ryegrass glycine-rich RNA-binding protein gene suggest a role in cold adaptation , 2006, Zeitschrift für Induktive Abstammungs- und Vererbungslehre.

[22]  Renu Deswal,et al.  The molecular biology of the low‐temperature response in plants , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[23]  Hur-Song Chang,et al.  Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses , 2002, The Plant Cell Online.

[24]  M. Thomashow,et al.  Arabidopsis Transcriptome Profiling Indicates That Multiple Regulatory Pathways Are Activated during Cold Acclimation in Addition to the CBF Cold Response Pathway Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1 , 2002, The Plant Cell Online.

[25]  Hur-Song Chang,et al.  Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress1,212 , 2002, Plant Physiology.

[26]  Mark Stitt,et al.  A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. , 2002, Current opinion in plant biology.

[27]  R. Creelman,et al.  From Laboratory to Field. Using Information from Arabidopsis to Engineer Salt, Cold, and Drought Tolerance in Crops1 , 2004, Plant Physiology.

[28]  C. Pilarsky,et al.  Exhaustive mining of EST libraries for genes differentially expressed in normal and tumour tissues. , 1999, Nucleic acids research.

[29]  Jin-Young Park,et al.  Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[30]  E. Stockinger,et al.  Structural, Functional, and Phylogenetic Characterization of a Large CBF Gene Family in Barley , 2005, Plant Molecular Biology.

[31]  S. Rudd Expressed sequence tags: alternative or complement to whole genome sequences? , 2003, Trends in plant science.

[32]  E. Rassart,et al.  Differential expression of a gene encoding an acidic dehydrin in chilling sensitive and freezing tolerant gramineae species , 1994, FEBS letters.

[33]  A. Böck,et al.  Ribosomal mutation in Escherichia coli affecting membrane stability , 2004, Molecular and General Genetics MGG.

[34]  Jian-Kang Zhu,et al.  ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. , 2003, Genes & development.

[35]  Mark L. Blaxter,et al.  Making sense of EST sequences by CLOBBing them , 2002, BMC Bioinformatics.

[36]  S. -. Park,et al.  Improvement of salt tolerance in transgenic potato plants by glyceraldehyde-3 phosphate dehydrogenase gene transfer. , 2001, Molecules and cells.

[37]  A. Leyva,et al.  Low Temperature Induces the Accumulation of Alcohol Dehydrogenase mRNA in Arabidopsis thaliana, a Chilling-Tolerant Plant , 1993, Plant physiology.

[38]  H. Teramoto,et al.  The level of mRNA transcribed from psaL, which encodes a subunit of photosystem I, is increased by cytokinin in darkness in etiolated cotyledons of cucumber. , 1996, Plant & cell physiology.

[39]  Seppänen,et al.  Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. , 2000, Plant science : an international journal of experimental plant biology.

[40]  Angelica Lindlöf Gene identification through large-scale EST sequence processing. , 2003, Applied bioinformatics.

[41]  Zhangjun Fei,et al.  Comprehensive EST analysis of tomato and comparative genomics of fruit ripening. , 2004, The Plant journal : for cell and molecular biology.

[42]  Xiao-Lin Wu,et al.  Census of orthologous genes and self-organizing maps of biologically relevant transcriptional patterns in chickens (Gallus gallus). , 2004, Gene.

[43]  M. Thomashow So what's new in the field of plant cold acclimation? Lots! , 2001, Plant physiology.

[44]  B. Olsson,et al.  Generation and analysis of 9792 EST sequences from cold acclimated oat, Avena sativa , 2005, BMC Plant Biology.

[45]  X. Huang,et al.  CAP3: A DNA sequence assembly program. , 1999, Genome research.

[46]  H. Mewes,et al.  How can we deliver the large plant genomes? Strategies and perspectives. , 2002, Current opinion in plant biology.

[47]  C. Bogdan Nitric oxide and the regulation of gene expression. , 2001, Trends in cell biology.

[48]  F. Sarhan,et al.  Transcriptome comparison of winter and spring wheat responding to low temperature. , 2005, Genome.

[49]  V. Walbot,et al.  Low-temperature accumulation of alcohol dehydrogenase-1 mRNA and protein activity in maize and rice seedlings. , 1991, Plant physiology.