PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms.

Many plants increase in freezing tolerance upon exposure to low nonfreezing temperatures, a phenomenon known as cold acclimation. In this review, recent advances in determining the nature and function of genes with roles in freezing tolerance and the mechanisms involved in low temperature gene regulation and signal transduction are described. One of the important conclusions to emerge from these studies is that cold acclimation includes the expression of certain cold-induced genes that function to stabilize membranes against freeze-induced injury. In addition, a family of Arabidopsis transcription factors, the CBF/DREB1 proteins, have been identified that control the expression of a regulon of cold-induced genes that increase plant freezing tolerance. These results along with many of the others summarized here further our understanding of the basic mechanisms that plants have evolved to survive freezing temperatures. In addition, the findings have potential practical applications as freezing temperatures are a major factor limiting the geographical locations suitable for growing crop and horticultural plants and periodically account for significant losses in plant productivity.

[1]  A. Cutler,et al.  A 5.3-Kilobase Genomic Fragment from Arabidopsis thaliana Containing kin1 and cor6.6 , 1994, Plant Physiology.

[2]  W. Larcher,et al.  Frost Survival of Plants: Responses and Adaptation to Freezing Stress , 1987 .

[3]  R. Teutonico,et al.  Isolation of Mutations Affecting the Development of Freezing Tolerance in Arabidopsis thaliana (L.) Heynh , 1996, Plant physiology.

[4]  H. Nam,et al.  Identification of a Receptor-Like Protein Kinase Gene Rapidly Induced by Abscisic Acid, Dehydration, High Salt, and Cold Treatments in Arabidopsis thaliana , 1997, Plant physiology.

[5]  K. Yamaguchi-Shinozaki,et al.  An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. , 1998, Biochemical and biophysical research communications.

[6]  J. Duman Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. , 1994, Biochimica et biophysica acta.

[7]  D. Fowler,et al.  Genetic Control of Cold Hardiness and Vernalization Requirement in Winter Wheat , 1988 .

[8]  L. Dure A repeating 11-mer amino acid motif and plant desiccation. , 1993, The Plant journal : for cell and molecular biology.

[9]  S. Bowley,et al.  Active Oxygen and Freezing Tolerance in Transgenic Plants , 1997 .

[10]  M. Uemura,et al.  Effect of Cold Acclimation on Membrane Lipid Composition and Freeze-Induced Membrane Destablization , 1997 .

[11]  A S Rudolph,et al.  Membrane stabilization during freezing: the role of two natural cryoprotectants, trehalose and proline. , 1985, Cryobiology.

[12]  C. Guy,et al.  Changes in freezing tolerance and polypeptide content of spinach and citrus at 5 °C☆☆☆ , 1988 .

[13]  C. J. Weiser,et al.  An Excised Leaflet Test for Evaluating Potato Frost Tolerance1 , 1972, HortScience.

[14]  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.

[15]  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.

[16]  M. Ishitani,et al.  HOS1, a Genetic Locus Involved in Cold-Responsive Gene Expression in Arabidopsis , 1998, Plant Cell.

[17]  C. Guy,et al.  Structural Organization of the Spinach Endoplasmic Reticulum-Luminal 70-Kilodalton Heat-Shock Cognate Gene and Expression of 70-Kilodalton Heat-Shock Genes during Cold Acclimation , 1994, Plant physiology.

[18]  G. Warren,et al.  Cold responses of Arabidopsis mutants impaired in freezing tolerance , 1996 .

[19]  G. Coupland,et al.  A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. , 1996, The Plant cell.

[20]  C. R. Olien,et al.  Ice adhesions in relation to freeze stress. , 1977, Plant physiology.

[21]  C. Guy,et al.  Association of Proteins with the Stress 70 Molecular Chaperones at Low Temperature: Evidence for the Existence of Cold Labile Proteins in Spinach☆ , 1998 .

[22]  S. J. Gilmour,et al.  Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. B. Fowler,et al.  Selection for Winterhardiness in Wheat. I. Identification of Genotypic Variability1 , 1979 .

[24]  M. Thomashow,et al.  Regulation of Arabidopsis thaliana L. (Heyn) cor78 in Response to Low Temperature , 1993, Plant physiology.

[25]  B. Sundberg,et al.  Alterations in Water Status, Endogenous Abscisic Acid Content, and Expression of rab18 Gene during the Development of Freezing Tolerance in Arabidopsis thaliana , 1994, Plant physiology.

[26]  G. Öquist,et al.  Energy balance and acclimation to light and cold , 1998 .

[27]  E. Meyerowitz,et al.  The AP2/EREBP family of plant transcription factors. , 1998, Biological chemistry.

[28]  F. Sarhan,et al.  Chromosome mapping of low-temperature induced Wcs120 family genes and regulation of cold-tolerance expression in wheat , 1997, Molecular and General Genetics MGG.

[29]  S. J. Gilmour,et al.  Cold Acclimation in Arabidopsis thaliana. , 1988, Plant physiology.

[30]  M. Van Montagu,et al.  Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. , 1994, The Plant cell.

[31]  Dale Haskell,et al.  Detection of polypeptides associated with the cold acclimation process in spinach , 1988, Electrophoresis.

[32]  M. Thomashow,et al.  DNA Sequence Analysis of a Complementary DNA for Cold-Regulated Arabidopsis Gene cor 15 and Characterization of the COR 15 Polypeptidel , 2022 .

[33]  K. Shinozaki,et al.  ATMPKs: a gene family of plant MAP kinases in Arabidopsis thaliana , 1993, FEBS letters.

[34]  C. Guy,et al.  Altered gene expression during cold acclimation of spinach. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[35]  P. Kramer,et al.  Responses of Plants to Environmental Stresses , 1973 .

[36]  H. Hirt,et al.  Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Ohme-Takagi,et al.  Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. , 1995, The Plant cell.

[38]  R. Dhindsa,et al.  Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold‐inactivation , 1998 .

[39]  E. Grill,et al.  A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. , 1994, Science.

[40]  P. Lillford,et al.  A carrot leucine-rich-repeat protein that inhibits ice recrystallization. , 1998, Science.

[41]  M. Thomashow Molecular Genetics of Cold Acclimation in Higher Plants , 1990 .

[42]  J. Giraudat,et al.  Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. , 1994, Science.

[43]  K. Shepherd,et al.  Use of isozymes as chromosome markers in the isolation and characterization of wheat-barley chromosome addition lines , 1980 .

[44]  C. Somerville,et al.  Cloning of a Temperature-Regulated Gene Encoding a Chloroplast [omega]-3 Desaturase from Arabidopsis thaliana , 1994, Plant physiology.

[45]  W. Keller,et al.  Induction of Freezing Tolerance in an Embryogenic Cell Suspension Culture of Brassica napus by Abscisic Acid at Room Temperature , 1986 .

[46]  A. Pugsley A genetic analysis of the spring-winter habit of growth in wheat , 1971 .

[47]  The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. , 1996, The Plant cell.

[48]  J. Ingram,et al.  THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[49]  J. Braam,et al.  Cold-Shock Regulation of the Arabidopsis TCH Genes and the Effects of Modulating Intracellular Calcium Levels , 1996, Plant physiology.

[50]  K. Dörffling,et al.  Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties , 1985 .

[51]  J. Snape,et al.  Chromosome variation for loci controlling ear emergence time on chromosome 5A of wheat , 1976, Heredity.

[52]  K. Shinozaki,et al.  Stress‐responsive expression of genes for two‐component response regulator‐like proteins in Arabidopsis thaliana , 1998, FEBS letters.

[53]  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.

[54]  M. Brenner,et al.  Involvement of abscisic Acid in potato cold acclimation. , 1983, Plant physiology.

[55]  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.

[56]  Y. Shai,et al.  Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides , 1995, Biopolymers.

[57]  H. Hauser,et al.  Stabilization of lipid bilayer vesicles by sucrose during freezing. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Carpenter,et al.  Cryoprotection of phosphofructokinase with organic solutes: characterization of enhanced protection in the presence of divalent cations. , 1986, Archives of biochemistry and biophysics.

[59]  K. Irie,et al.  A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[60]  F. Sarhan,et al.  The wheat wcs120 gene family. A useful model to understand the molecular genetics of freezing tolerance in cereals , 1997 .

[61]  M. Griffith,et al.  Antifreeze protein accumulation in freezing-tolerant cereals , 1997 .

[62]  M. Dunn,et al.  The molecular biology of plant acclimation to low temperature , 1996 .

[63]  A. Robertson,et al.  Effect of Temperature, Light, Nutrients and Dehardening on Abscisic Acid Induced Cold Hardiness in Bromus inermis Leyss Suspension Cultured Cells , 1990 .

[64]  R. Hill,et al.  Characterization of a gene family encoding abscisic acid- and environmental stress-inducible proteins of alfalfa. , 1992, The Journal of biological chemistry.

[65]  R S Quatrano,et al.  A plant leucine zipper protein that recognizes an abscisic acid response element. , 1990, Science.

[66]  P. Steponkus Role of the Plasma Membrane in Freezing Injury and Cold Acclimation , 1984 .

[67]  L. Vézina,et al.  A New Cold-Induced Alfalfa Gene Is Associated with Enhanced Hardening at Subzero Temperature , 1993, Plant physiology.

[68]  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.

[69]  D. Livingston,et al.  Apoplastic Sugars, Fructans, Fructan Exohydrolase, and Invertase in Winter Oat: Responses to Second-Phase Cold Hardening , 1998 .

[70]  R. Dhindsa,et al.  Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 degrees C. , 1995, The Plant cell.

[71]  Charles L. Guy,et al.  Cold Acclimation and Freezing Stress Tolerance: Role of Protein Metabolism , 1990 .

[72]  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.

[73]  E. T. Palva,et al.  Role of Abscisic Acid in Drought-Induced Freezing Tolerance, Cold Acclimation, and Accumulation of LT178 and RAB18 Proteins in Arabidopsis thaliana , 1995, Plant physiology.

[74]  H. Kalbitzer,et al.  The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. , 1996, Biological chemistry.

[75]  M. Uemura,et al.  Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions) , 1995, Plant physiology.

[76]  P. Hugueney,et al.  Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. , 1996, The EMBO journal.

[77]  A S Rudolph,et al.  Modes of interaction of cryoprotectants with membrane phospholipids during freezing. , 1987, Cryobiology.

[78]  T. Close Dehydrins: A commonalty in the response of plants to dehydration and low temperature , 1997 .

[79]  R. Dhindsa,et al.  The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium , 1997, Planta.

[80]  M. Ishitani,et al.  Genetic analysis of osmotic and cold stress signal transduction in Arabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways. , 1997, The Plant cell.

[81]  J. Ding,et al.  Modulation of mechanosensitive calcium-selective cation channels by temperature. , 1993, The Plant journal : for cell and molecular biology.

[82]  R. Allan,et al.  Effect of the Vrn1‐Fr1 Interval on Cold Hardiness Levels in Near‐Isogenic Wheat Lines , 1998 .

[83]  D. Sparrow,et al.  Isolation and characterization of euplasmic wheat-barley chromosome addition lines , 1981, Heredity.

[84]  D. Hincha,et al.  Purification and Characterization of a Cryoprotective Protein (Cryoprotectin) from the Leaves of Cold-Acclimated Cabbage , 1996, Plant physiology.

[85]  K. Pihakaski-Maunsbach,et al.  Antifreeze proteins in winter rye , 1997 .

[86]  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.

[87]  F. Sarhan,et al.  Engineering cold-tolerant crops—throwing the master switch , 1998 .

[88]  D. Laurie,et al.  RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter x spring barley (Hordeum vulgare L.) cross. , 1995, Genome.

[89]  S. Hill,et al.  Cold-Induced Accumulation of hsp90 Transcripts in Brassica napus , 1995, Plant physiology.

[90]  M. Koornneef,et al.  The genetic and molecular dissection of abscisic acid biosynthesis and signal transduction in Arabidopsis. , 1998 .

[91]  C. Guy,et al.  Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. , 1998, Plant physiology.

[92]  R. Foster,et al.  Plant bZIP proteins gather at ACGT elements , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[93]  S. J. Gilmour,et al.  Molecular Cloning and Expression of cor (Cold-Regulated) Genes in Arabidopsis thaliana. , 1990, Plant physiology.

[94]  P. Hayes,et al.  Quantitative trait loci on barley (Hordeum vulgare L.) chromosome 7 associated with components of winterhardiness. , 1993, Genome.

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

[96]  M. Uemura,et al.  Membrane destabilization during freeze-induced dehydration , 1993 .

[97]  F. Sarhan,et al.  Cold-Induced Changes in Freezing Tolerance, Protein Phosphorylation, and Gene Expression (Evidence for a Role of Calcium) , 1993, Plant physiology.

[98]  F. Sarhan,et al.  Low temperature-stimulated phosphorylation regulates the binding of nuclear factors to the promoter of Wcs120, a cold-specific gene in wheat , 1998, Molecular and General Genetics MGG.

[99]  C. Guy,et al.  Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation induced proteins. , 1987, Plant physiology.

[100]  M. Thomashow,et al.  DNA Sequence Analysis of a Complementary DNA for Cold-Regulated Arabidopsis Gene cor15 and Characterization of the COR 15 Polypeptide. , 1992, Plant physiology.

[101]  C. Guy,et al.  The Organization and Evolution of the Spinach Stress 70 Molecular Chaperone Gene Family , 1998, Plant Cell.

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

[103]  T. Close,et al.  Cold-Specific Induction of a Dehydrin Gene Family Member in Barley , 1995, Plant physiology.