Two related low-temperature-inducible genes of Arabidopsis encode proteins showing high homology to 14-3-3 proteins, a family of putative kinase regulators

We have isolated two Rare Cold-Inducible (RCI1 and RCI2) cDNAs by screening a cDNA library prepared from cold-acclimated etiolated seedlings of Arabidopsis thaliana with a subtracted probe. RNA-blot hybridizations revealed that the expression of both RCI1 and RCI2 genes is induced by low temperature independently of the plant organ or the developmental stage considered. However, RCI1 mRNA accumulates faster and at higher levels than the RCI2 one indicating that these genes have differential responsiveness to cold stress. Additionally, when plants are returned to room temperature, RCI1 mRNA decreases faster than RCI2. In contrast to most of the cold-inducible plant genes characterized, the expression of RCI1 and RCI2 is not induced by ABA or water stress. The nucleotide sequences of RCI1 and RCI2 cDNAs predict two acidic polypeptides of 255 and 251 amino acids with molecular weights of 29 and 28 kDa respectively. The alignment of these polypeptides indicates that they have 181 identical amino acids suggesting that the corresponding genes have a common origin. Sequence comparisons reveal no similarities between the RCI proteins and any other cold-regulated plant protein so far described. Instead, they demonstrate that the RCI proteins are highly homologous to a family of proteins, known as 14-3-3 proteins, which are thought to be involved in the regulation of multifunctional protein kinases.

[1]  K. Hahlbrock,et al.  Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures. , 1990, The Journal of biological chemistry.

[2]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[3]  S. Kurkela,et al.  Cloning and characterization of a cold-and ABA-inducible Arabidopsis gene , 1990, Plant Molecular Biology.

[4]  D. Walton.  Biochemistry and physiology of abscisic acid. , 1980 .

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

[6]  K. Oono,et al.  Molecular cloning and characterization of genes related to chilling tolerance in rice. , 1992, Plant physiology.

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

[8]  R. Dhindsa,et al.  Abscisic Acid-regulated gene expression in relation to freezing tolerance in alfalfa. , 1988, Plant physiology.

[9]  P. Heino,et al.  Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. , 1991, Plant Molecular Biology.

[10]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[11]  A. Aitken,et al.  14-3-3 proteins : a highly conserved widespread family of eukaryotic proteins , 2003 .

[12]  E. T. Palva,et al.  The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh , 1992, Plant Molecular Biology.

[13]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[14]  E. Krebs,et al.  Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. , 1991, The Journal of biological chemistry.

[15]  D. Siminovitch,et al.  Correlation between Cold- and Drought-Induced Frost Hardiness in Winter Wheat and Rye Varieties. , 1982, Plant physiology.

[16]  R. Kuwano,et al.  Widespread Distribution of the 14‐3‐3 Protein in Vertebrate Brains and Bovine Tissues: Correlation with the Distributions of Calcium‐Dependent Protein Kinases , 1991, Journal of neurochemistry.

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

[18]  K. Struhl,et al.  Current Protocols in Molecular Biology (New York: Greene Publishing Associates and Wiley-Interscience). Host-Range Shuttle System for Gene Insertion into the Chromosomes of Gram-negative Bacteria. , 1988 .

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

[20]  M. Dunn,et al.  Nucleotide sequence and molecular analysis of the low temperature induced cereal gene, BLT4 , 1991, Molecular and General Genetics MGG.

[21]  S. McKnight,et al.  Scissors-grip model for DNA recognition by a family of leucine zipper proteins. , 1989, Science.

[22]  B. Patterson,et al.  Responses of Plants to Low, Nonfreezing Temperatures: Proteins, Metabolism, and Acclimation , 1982 .

[23]  T. Isobe,et al.  Activation of protein kinase C by the 14‐3‐3 proteins homologous with Exol protein that stimulates calcium‐dependent exocytosis , 1992, FEBS letters.

[24]  M. Thomashow,et al.  Characterization of a Cold-Regulated Wheat Gene Related to Arabidopsis cor47. , 1992, Plant physiology.

[25]  L. Cattivelli,et al.  Modification of gene expression induced by ABA, in relation to drought and cold stress in barley shoots , 1992 .

[26]  E. Lagendijk,et al.  Characterization of the yeast BMH1 gene encoding a putative protein homologous to mammalian protein kinase II activators and protein kinase C inhibitors , 1992, FEBS letters.

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

[28]  A. Kato,et al.  Isolation and characterization of a rice cDNA similar to the bovine brain-specific 14-3-3 protein gene , 2004, Plant Molecular Biology.

[29]  N. de Vetten,et al.  A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. , 1992, The Plant cell.

[30]  E. T. Palva,et al.  Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh , 1993, Plant Molecular Biology.

[31]  R. Kuwano,et al.  Distinct forms of the protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. , 1991, Journal of molecular biology.

[32]  M. Ptashne,et al.  Transcription in yeast activated by a putative amphipathic alpha helix linked to a DNA binding unit. , 1987, Nature.

[33]  M. Dunn,et al.  The Effect of Temperature on Plant Growth and Development , 1990 .

[34]  R. Ferl,et al.  Brain proteins in plants: an Arabidopsis homolog to neurotransmitter pathway activators is part of a DNA binding complex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[35]  D. V. Lynch,et al.  Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation , 1989, Journal of bioenergetics and biomembranes.

[36]  J. Levitt,et al.  Responses of Plants to Environmental Stress, 2nd Edition, Volume 1: Chilling, Freezing, and High Temperature Stresses. , 1980 .

[37]  W. D. Cress,et al.  Critical structural elements of the VP16 transcriptional activation domain. , 1991, Science.

[38]  R. Dhindsa,et al.  cDNA Sequence, Expression, and Transcript Stability of a Cold Acclimation-Specific Gene, cas18, of Alfalfa (Medicago falcata) Cells , 1993, Plant physiology.

[39]  E. Rassart,et al.  Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. , 1992, Plant physiology.

[40]  L. Gusta,et al.  Abscisic Acid-induced freezing resistance in cultured plant cells. , 1983, Plant physiology.

[41]  S. J. Gilmour,et al.  cDNA sequence analysis and expression of two cold-regulated genes ofArabidopsis thaliana , 2004, Plant Molecular Biology.

[42]  M. Tesche.  BuchbesprechungA. Sakai, W. Larcher, Frost Survival of Plants. Responses and Adaptation to Freezing Stress., Springer-Verlag, Berlin-Heidelberg-New York-LondonParis-Tokyo (1987), Series Ecological Studies 62. 321 S . , 200 Abb., zahlr. Tab. , Preis : DM 198. , 1988 .

[43]  E. T. Palva,et al.  The expression of a rab-related gene, rab 18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh , 2004, Plant Molecular Biology.

[44]  D. Lipman,et al.  Improved tools for biological sequence comparison. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[45]  T. White,et al.  Characterization of Three Related Low-Temperature-Regulated cDNAs from Winter Brassica napus , 1993, Plant physiology.

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

[47]  S. Kurkela,et al.  Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana , 1992, Plant Molecular Biology.

[48]  Professor Dr. Walter Larcher,et al.  Frost Survival of Plants , 1987, Ecological Studies.

[49]  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 .

[50]  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.

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

[52]  L. Willmitzer,et al.  Improved method for the isolation of RNA from plant tissues. , 1987, Analytical biochemistry.

[53]  A. Toker,et al.  Kinase and neurotransmitters , 1990, Nature.

[54]  A. Aitken,et al.  A plant homologue to mammalian brain 14‐3‐3 protein and protein kinase C inhibitor , 1992, FEBS letters.

[55]  S. J. Gilmour,et al.  Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana , 1991, Plant Molecular Biology.

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

[57]  C. Somerville,et al.  Sulfonylurea-resistant mutants of Arabidopsis thaliana , 1986, Molecular and General Genetics MGG.

[58]  D. Higgins,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Clustal: Blockina Blockinpackage Blockinfor Blockinperforming Multiple Blockinsequence Blockinalignment Blockinon Blockina Minicomputer Article Blockin Blockinin Blockin , 2022 .

[59]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[60]  H. Thordal-Christensen,et al.  A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. , 1992, The Plant journal : for cell and molecular biology.