Transcriptional regulation network of cold-responsive genes in higher plants

Abstract CBF (DREB1) genes act as nodes of regulatory network in Arabidopsis response to cold stress, which are conserved in many plants. Combined use of genetic and molecular approaches, a series of regulatory genes involved in CBF cold response pathway have been isolated and analyzed. Among them, some gene products are thought to function directly in transcription. HOS1 is a negative regulator of CBFs, whereas FRY2 acts as a transcriptional repressor and LOS2 as a positive regulator in the pathway. ICE1, the regulator of the CBF3 may be regulated by HOS1. Arabidopsis transcriptome profiling studies suggest multiplicity and complexity of the cold-responsive pathways. It is underestimated that 1000 genes are cold-responsive in the entire Arabidosis genome, some of which are transient or up-regulated and others of which are long lived or down-regulated. In addition, the data indicate that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold-responsive pathway. Two transcription factors, RAV1 and ZAT12 probably operate in pathways that are parallel to those of the CBFs. By contrast, two AP2 domain proteins, RAP2.6 and RAP2.1 might be targets of the CBF activators. Moreover, the latest results show that the expression of CBFs in Arabidopsis is also regulated by ABA, light and the circadian clock. It is suggested that there exist extensive crosstalks between the CBF cold response pathway and the non-temperature signaling transduction pathways.

[1]  K. Shinozaki,et al.  OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. , 2003, The Plant journal : for cell and molecular biology.

[2]  K. Shinozaki,et al.  Molecular responses to drought and cold stress. , 1996, Current opinion in biotechnology.

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

[4]  T. Close,et al.  Barley Cbf3 Gene Identification, Expression Pattern, and Map Location1 , 2002, Plant Physiology.

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

[6]  J. Oliveros,et al.  A freezing-sensitive mutant of Arabidopsis, frs1, is a new aba3 allele , 2000, Planta.

[7]  E. Stockinger,et al.  Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. , 1998, The Plant journal : for cell and molecular biology.

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

[9]  J. Browse,et al.  Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Piero Carninci,et al.  Monitoring the Expression Pattern of 1300 Arabidopsis Genes under Drought and Cold Stresses by Using a Full-Length cDNA Microarray , 2001, Plant Cell.

[11]  A. Michael,et al.  Isolation and characterisation of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs , 1997, Plant Molecular Biology.

[12]  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.

[13]  Michael F. Thomashow,et al.  Low Temperature Induction of Arabidopsis CBF1, 2, and 3 Is Gated by the Circadian Clock1 , 2005, Plant Physiology.

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

[15]  J. Browse,et al.  Cold comfort farm: the acclimation of plants to freezing temperatures. , 2000 .

[16]  M. Chan,et al.  Heterology Expression of the ArabidopsisC-Repeat/Dehydration Response Element Binding Factor 1 Gene Confers Elevated Tolerance to Chilling and Oxidative Stresses in Transgenic Tomato1 , 2002, Plant Physiology.

[17]  T. Zhu Global analysis of gene expression using GeneChip microarrays. , 2003, Current opinion in plant biology.

[18]  P. Hayes,et al.  Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map , 2004, Theoretical and Applied Genetics.

[19]  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.

[20]  G. Xue The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. , 2003, The Plant journal : for cell and molecular biology.

[21]  Ghislaine Allard,et al.  Regulation and characterization of four CBF transcription factors from Brassica napus , 2002, Plant Molecular Biology.

[22]  M. Van Montagu,et al.  The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G. Coupland,et al.  GIGANTEA: a circadian clock‐controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane‐spanning domains , 1999, The EMBO journal.

[24]  S. J. Gilmour,et al.  Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. , 2000, Plant physiology.

[25]  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.

[26]  M. Thomashow,et al.  CBF1 Orthologs in Sour Cherry and Strawberry and the Heterologous Expression of CBF1 in Strawberry , 2002 .

[27]  Transcription Factor CBF4 Is a Regulator of Drought Adaptation in Arabidopsis1 , 2002, Plant Physiology.

[28]  Bin Han,et al.  Gene Expression Phenotypes of Arabidopsis Associated with Sensitivity to Low Temperatures[w] , 2003, Plant Physiology.

[29]  S. J. Gilmour,et al.  Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[31]  J. Dubcovsky,et al.  The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A , 2003, Molecular Genetics and Genomics.

[32]  M. Thomashow,et al.  Cold Induction of Arabidopsis CBF Genes Involves Multiple ICE (Inducer of CBF Expression) Promoter Elements and a Cold-Regulatory Circuit That Is Desensitized by Low Temperature1 , 2003, Plant Physiology.

[33]  M. Thomashow,et al.  Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. , 2001, Plant physiology.

[34]  K. Shinozaki,et al.  Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. , 2000, Current opinion in plant biology.

[35]  K. Shinozaki,et al.  DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. , 2002, Biochemical and biophysical research communications.

[36]  Jian-Kang Zhu,et al.  Cell Signaling during Cold, Drought, and Salt Stress Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000596. , 2002, The Plant Cell Online.

[37]  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.

[38]  M. Ishitani,et al.  Cold-regulated gene expression and freezing tolerance in an Arabidopsis thaliana mutant. , 1999, The Plant journal : for cell and molecular biology.

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

[40]  Hur-Song Chang,et al.  Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis1,212 , 2002, Plant Physiology.

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

[42]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[43]  R. Bressan,et al.  Repression of stress-responsive genes by FIERY2, a novel transcriptional regulator in Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Thomashow Role of cold-responsive genes in plant freezing tolerance. , 1998, Plant physiology.

[45]  M. Thomashow,et al.  Abscisic Acid Induces CBF Gene Transcription and Subsequent Induction of Cold-Regulated Genes via the CRT Promoter Element1 , 2004, Plant Physiology.

[46]  J.-S. Zhang,et al.  An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress , 2003, Theoretical and Applied Genetics.

[47]  K. Shinozaki,et al.  Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis , 1998, Plant Cell.

[48]  M. Ishitani,et al.  The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo--cytoplasmic partitioning. , 2001, Genes & development.

[49]  S. Chen,et al.  Characterization of a DRE-binding transcription factor from a halophyte Atriplex hortensis , 2003, Theoretical and Applied Genetics.

[50]  L. Xiong,et al.  A single amino acid substitution in the Arabidopsis FIERY1/HOS2 protein confers cold signaling specificity and lithium tolerance. , 2004, The Plant journal : for cell and molecular biology.

[51]  K. Ohmiya,et al.  RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. , 1999, Nucleic acids research.

[52]  Kazuo Shinozaki,et al.  Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor , 1999, Nature Biotechnology.

[53]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[54]  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.

[55]  Kil-Jae Lee,et al.  Acquired tolerance to temperature extremes. , 2003, Trends in plant science.

[56]  D. E. Somers,et al.  Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. , 1999, Science.

[57]  Heather Knight,et al.  The sfr6 Mutation in Arabidopsis Suppresses Low-Temperature Induction of Genes Dependent on the CRT/DRE Sequence Motif , 1999, Plant Cell.

[58]  K. Shinozaki,et al.  Regulatory network of gene expression in the drought and cold stress responses. , 2003, Current opinion in plant biology.

[59]  O. Schabenberger,et al.  Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. , 1998, Science.

[60]  S. H. Lee,et al.  A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. , 2001, The Plant journal : for cell and molecular biology.