Two Classes of Plant cDNA Clones Differentially Complement Yeast Calcineurin Mutants and Increase Salt Tolerance of Wild-type Yeast*

The salt-sensitive phenotype of yeast cells deficient in the phosphoprotein phosphatase, calcineurin, was used to identify genes from the higher plant Arabidopsis thaliana that complement this phenotype. cDNA clones corresponding to two different sequences, designated STO (salt tolerance) and STZ (salt tolerance zinc finger), were found to increased tolerance of calcineurin mutants and of wild-type yeast to both Li+ and Na+ ions. STZ is related to Cys2/His2-type zinc-finger proteins found in higher plants, and STO is similar to the Arabidopsis CONSTANS protein in regions that may also be zinc fingers. Although neither protein has sequence similarity to any protein phosphatase, STO was able to at least partially compensate for all tested additional phenotypic effects of calcineurin deficiency, and STZ compensated for a subset of these effects. Salt tolerance produced by STZ appeared to be partially dependent on ENA1/PMR2, a P-type ATPase required for Li+ and Na+ efflux in yeast, whereas the effect of STO on salt tolerance was independent of ENA1/PMR2. STZ and STO were found to be expressed in Arabidopsis roots and leaves, whereas only STO message was detectable in flowers. An apparent increase in the level of STZ mRNA was observed in response NaCl exposure in Arabidopsis seedlings, but the level of STO mRNA was not altered by this treatment.

[1]  A. Rodríguez-Navarro,et al.  The SAL1 gene of Arabidopsis, encoding an enzyme with 3'(2'),5'-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities, increases salt tolerance in yeast. , 1996, The Plant cell.

[2]  G. Fink,et al.  Regulation of cation transport in Saccharomyces cerevisiae by the salt tolerance gene HAL3 , 1995, Molecular and cellular biology.

[3]  Z. Hong,et al.  Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants , 1995, Plant physiology.

[4]  F. Posas,et al.  The PPZ Protein Phosphatases Are Important Determinants of Salt Tolerance in Yeast Cells (*) , 1995, The Journal of Biological Chemistry.

[5]  Y. Anraku,et al.  Cooperation of Calcineurin and Vacuolar H+-ATPase in Intracellular Ca2+Homeostasis of Yeast Cells * , 1995, The Journal of Biological Chemistry.

[6]  B. Law,et al.  Identification of Soluble Protein Phosphatases That Dephosphorylate Voltage-sensitive Sodium Channels in Rat Brain (*) , 1995, The Journal of Biological Chemistry.

[7]  R. Simon,et al.  The CONSTANS gene of arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors , 1995, Cell.

[8]  R. Serrano,et al.  A salt-sensitive 3'(2'),5'-bisphosphate nucleotidase involved in sulfate activation , 1995, Science.

[9]  T. Rabbitts,et al.  The LIM domain: a new structural motif found in zinc-finger-like proteins. , 1994, Trends in genetics : TIG.

[10]  H. Takatsuji,et al.  A new family of zinc finger proteins in petunia: structure, DNA sequence recognition, and floral organ-specific expression. , 1994, The Plant Cell.

[11]  J. Heitman,et al.  Calcineurin is essential in cyclosporin A- and FK506-sensitive yeast strains. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  I. Módy,et al.  Regulation of NMDA channel function by endogenous Ca2+-dependent phosphatase , 1994, Nature.

[13]  F. Rubio,et al.  The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. , 1994, The Journal of biological chemistry.

[14]  C. Gasser,et al.  Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana. , 1994, The Journal of biological chemistry.

[15]  G. Fink,et al.  Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases , 1994, The Journal of cell biology.

[16]  R. Serrano,et al.  Microbial Models and Salt Stress Tolerance in Plants , 1994 .

[17]  S. Rossie,et al.  Identification of the sites of selective phosphorylation and dephosphorylation of the rat brain Na+ channel alpha subunit by cAMP-dependent protein kinase and phosphoprotein phosphatases. , 1993, The Journal of biological chemistry.

[18]  Y. Liu,et al.  Protein phosphatase type 2B (calcineurin)‐mediated, FK506‐sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. , 1993, The EMBO journal.

[19]  A. Sakamoto,et al.  The putative zinc-finger protein WZF1 interacts with a cis-acting element of wheat histone genes. , 1993, European journal of biochemistry.

[20]  M. Mumby,et al.  Protein serine/threonine phosphatases: structure, regulation, and functions in cell growth. , 1993, Physiological reviews.

[21]  Y. Surdin-Kerjan,et al.  Salt tolerance and methionine biosynthesis in Saccharomyces cerevisiae involve a putative phosphatase gene. , 1993, The EMBO journal.

[22]  S. Schreiber,et al.  Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[23]  H. Bohnert,et al.  Stress Protection of Transgenic Tobacco by Production of the Osmolyte Mannitol , 1993, Science.

[24]  Jacobs Gh.  Determination of the base recognition positions of zinc fingers from sequence analysis. , 1992 .

[25]  R. Serrano,et al.  A novel and conserved salt‐induced protein is an important determinant of salt tolerance in yeast. , 1992, The EMBO journal.

[26]  M. Cyert,et al.  Regulatory subunit (CNB1 gene product) of yeast Ca2+/calmodulin-dependent phosphoprotein phosphatases is required for adaptation to pheromone , 1992, Molecular and cellular biology.

[27]  R. Elble.  A simple and efficient procedure for transformation of yeasts. , 1992, BioTechniques.

[28]  R. Schiestl,et al.  Improved method for high efficiency transformation of intact yeast cells. , 1992, Nucleic acids research.

[29]  K. R. Wendt,et al.  Enhancement of NaCl tolerance in Arabidopsis thaliana by exogenous L‐asparagine and D‐asparagine , 1992 .

[30]  P. Benfey,et al.  Characterization of a zinc finger DNA‐binding protein expressed specifically in Petunia petals and seedlings. , 1992, The EMBO journal.

[31]  L. C. Robinson,et al.  Yeast casein kinase I homologues: an essential gene pair. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Rodríguez-Navarro,et al.  A novel P‐type ATPase from yeast involved in sodium transport , 1991, FEBS letters.

[33]  M. Cyert,et al.  Yeast has homologs (CNA1 and CNA2 gene products) of mammalian calcineurin, a calmodulin-regulated phosphoprotein phosphatase. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Aigle,et al.  The open reading frame YCR101 located on chromosome III from Saccharomyces cerevisiae is a putative protein kinase , 1991, Yeast.

[35]  N. Pavletich,et al.  Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A , 1991, Science.

[36]  R. W. Davis,et al.  Lambda YES: a multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[37]  R. Vierstra,et al.  Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. , 1990, The Journal of biological chemistry.

[38]  J. Berg.  Zinc finger domains: hypotheses and current knowledge. , 1990, Annual review of biophysics and biophysical chemistry.

[39]  G. Fink,et al.  The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family , 1989, Cell.

[40]  R. Sikorski,et al.  A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. , 1989, Genetics.

[41]  D. Armstrong.  Calcium channel regulation by calcineurin, a Ca2+-activated phosphatase in mammalian brain , 1989, Trends in Neurosciences.

[42]  M. Van Montagu,et al.  Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[43]  G. Fink,et al.  TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae , 1988, Molecular and cellular biology.

[44]  D. Shah,et al.  Structure, expression, and evolution of the 5-enolpyruvylshikimate-3-phosphate synthase genes of petunia and tomato. , 1988, The Journal of biological chemistry.

[45]  R. Evans,et al.  Zinc fingers: Gilt by association , 1988, Cell.

[46]  Nancy Kleckner,et al.  A Method for Gene Disruption That Allows Repeated Use of URA3 Selection in the Construction of Multiply Disrupted Yeast Strains , 1987, Genetics.

[47]  J. Vieira,et al.  Production of single-stranded plasmid DNA. , 1987, Methods in enzymology.

[48]  D. Shah,et al.  The structure and expression of maize genes encoding the major heat shock protein, hsp70 , 1986, The EMBO journal.

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

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

[51]  H. Lehrach,et al.  An integrated and simplified approach to cloning into plasmids and single-stranded phages. , 1983, Methods in enzymology.

[52]  G. Borst-Pauwels.  Ion transport in yeast. , 1981, Biochimica et biophysica acta.

[53]  G. Fink,et al.  Methods in yeast genetics , 1979 .

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