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. 1996 Mar;8(3):529–537. doi: 10.1105/tpc.8.3.529

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.

F J Quintero 1, B Garciadeblás 1, A Rodríguez-Navarro 1
PMCID: PMC161118  PMID: 8721754

Abstract

A cDNA library in a yeast expression vector was prepared from roots of Arabidopsis exposed to salt and was used to select Li(+)-tolerant yeast transformants. The cDNA SAL1 isolated from one of these transformants encodes a polypeptide of 353 amino acid residues. This protein is homologous to the HAL2 and CysQ phosphatases of yeast and Escherichia coli, respectively. Partial cDNA sequences in the data bases indicate that rice produces a phosphatase highly homologous to SAL1 and that a second gene homologous to SAL1 exists in Arabidopsis. The SAL1 protein expressed in E. coli showed 3'(2'),5'-bisphosphate nucleotidase and inositol polyphosphate 1-phosphatase activities. In yeast, SAL1 restored the ability of a hal2/met22 mutant to grow on sulfate as a sole sulfur source, increased the intracellular Li+ tolerance, and modified Na+ and Li+ effluxes. We propose that the product of SAL1 participates in the sulfur assimilation pathway as well as in the phosphoinositide signaling pathway and that changes in the latter may affect Na+ and Li+ fluxes.

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Selected References

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  1. Alijo R., Ramos J. Several routes of activation of the potassium uptake system of yeast. Biochim Biophys Acta. 1993 Nov 7;1179(2):224–228. doi: 10.1016/0167-4889(93)90145-f. [DOI] [PubMed] [Google Scholar]
  2. Bronner C., Wiggins C., Monté D., Märki F., Capron A., Landry Y., Franson R. C. Compound 48/80 is a potent inhibitor of phospholipase C and a dual modulator of phospholipase A2 from human platelet. Biochim Biophys Acta. 1987 Aug 15;920(3):301–305. doi: 10.1016/0005-2760(87)90108-1. [DOI] [PubMed] [Google Scholar]
  3. Cho M. H., Shears S. B., Boss W. F. Changes in phosphatidylinositol metabolism in response to hyperosmotic stress in Daucus carota L. cells grown in suspension culture. Plant Physiol. 1993 Oct;103(2):637–647. doi: 10.1104/pp.103.2.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Claes B., Dekeyser R., Villarroel R., Van den Bulcke M., Bauw G., Van Montagu M., Caplan A. Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell. 1990 Jan;2(1):19–27. doi: 10.1105/tpc.2.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Diehl R. E., Whiting P., Potter J., Gee N., Ragan C. I., Linemeyer D., Schoepfer R., Bennett C., Dixon R. A. Cloning and expression of bovine brain inositol monophosphatase. J Biol Chem. 1990 Apr 15;265(11):5946–5949. [PubMed] [Google Scholar]
  7. Ecker J. R., Davis R. W. Plant defense genes are regulated by ethylene. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5202–5206. doi: 10.1073/pnas.84.15.5202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Garciadeblas B., Rubio F., Quintero F. J., Bañuelos M. A., Haro R., Rodríguez-Navarro A. Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol Gen Genet. 1993 Jan;236(2-3):363–368. doi: 10.1007/BF00277134. [DOI] [PubMed] [Google Scholar]
  10. Gaxiola R., de Larrinoa I. F., Villalba J. M., Serrano R. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 1992 Sep;11(9):3157–3164. doi: 10.1002/j.1460-2075.1992.tb05392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Geever R. F., Huiet L., Baum J. A., Tyler B. M., Patel V. B., Rutledge B. J., Case M. E., Giles N. H. DNA sequence, organization and regulation of the qa gene cluster of Neurospora crassa. J Mol Biol. 1989 May 5;207(1):15–34. doi: 10.1016/0022-2836(89)90438-5. [DOI] [PubMed] [Google Scholar]
  12. Gläser H. U., Thomas D., Gaxiola R., Montrichard F., Surdin-Kerjan Y., Serrano R. Salt tolerance and methionine biosynthesis in Saccharomyces cerevisiae involve a putative phosphatase gene. EMBO J. 1993 Aug;12(8):3105–3110. doi: 10.1002/j.1460-2075.1993.tb05979.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hallcher L. M., Sherman W. R. The effects of lithium ion and other agents on the activity of myo-inositol-1-phosphatase from bovine brain. J Biol Chem. 1980 Nov 25;255(22):10896–10901. [PubMed] [Google Scholar]
  14. Hirayama T., Ohto C., Mizoguchi T., Shinozaki K. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3903–3907. doi: 10.1073/pnas.92.9.3903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Inhorn R. C., Majerus P. W. Inositol polyphosphate 1-phosphatase from calf brain. Purification and inhibition by Li+, Ca2+, and Mn2+. J Biol Chem. 1987 Nov 25;262(33):15946–15952. [PubMed] [Google Scholar]
  16. Lamb H. K., Hawkins A. R., Smith M., Harvey I. J., Brown J., Turner G., Roberts C. F. Spatial and biological characterisation of the complete quinic acid utilisation gene cluster in Aspergillus nidulans. Mol Gen Genet. 1990 Aug;223(1):17–23. doi: 10.1007/BF00315792. [DOI] [PubMed] [Google Scholar]
  17. Majerus P. W. Inositol phosphate biochemistry. Annu Rev Biochem. 1992;61:225–250. doi: 10.1146/annurev.bi.61.070192.001301. [DOI] [PubMed] [Google Scholar]
  18. Mendoza I., Rubio F., Rodriguez-Navarro A., Pardo J. M. The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem. 1994 Mar 25;269(12):8792–8796. [PubMed] [Google Scholar]
  19. Murguía J. R., Bellés J. M., Serrano R. A salt-sensitive 3'(2'),5'-bisphosphate nucleotidase involved in sulfate activation. Science. 1995 Jan 13;267(5195):232–234. doi: 10.1126/science.7809627. [DOI] [PubMed] [Google Scholar]
  20. Neuwald A. F., Krishnan B. R., Brikun I., Kulakauskas S., Suziedelis K., Tomcsanyi T., Leyh T. S., Berg D. E. cysQ, a gene needed for cysteine synthesis in Escherichia coli K-12 only during aerobic growth. J Bacteriol. 1992 Jan;174(2):415–425. doi: 10.1128/jb.174.2.415-425.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Neuwald A. F., York J. D., Majerus P. W. Diverse proteins homologous to inositol monophosphatase. FEBS Lett. 1991 Dec 2;294(1-2):16–18. doi: 10.1016/0014-5793(91)81332-3. [DOI] [PubMed] [Google Scholar]
  22. Okorokov L. A., Lichko L. P., Kulaev I. S. Vacuoles: main compartments of potassium, magnesium, and phosphate ions in Saccharomyces carlsbergenis cells. J Bacteriol. 1980 Nov;144(2):661–665. doi: 10.1128/jb.144.2.661-665.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Posas F., Camps M., Ariño J. The PPZ protein phosphatases are important determinants of salt tolerance in yeast cells. J Biol Chem. 1995 Jun 2;270(22):13036–13041. doi: 10.1074/jbc.270.22.13036. [DOI] [PubMed] [Google Scholar]
  24. Ramaswamy S. G., Jakoby W. B. (2')3',5'-Bisphosphate nucleotidase. J Biol Chem. 1987 Jul 25;262(21):10044–10047. [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Thomas D., Barbey R., Henry D., Surdin-Kerjan Y. Physiological analysis of mutants of Saccharomyces cerevisiae impaired in sulphate assimilation. J Gen Microbiol. 1992 Oct;138(10):2021–2028. doi: 10.1099/00221287-138-10-2021. [DOI] [PubMed] [Google Scholar]
  27. Welters P., Takegawa K., Emr S. D., Chrispeels M. J. AtVPS34, a phosphatidylinositol 3-kinase of Arabidopsis thaliana, is an essential protein with homology to a calcium-dependent lipid binding domain. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11398–11402. doi: 10.1073/pnas.91.24.11398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yano R., Nagai H., Shiba K., Yura T. A mutation that enhances synthesis of sigma 32 and suppresses temperature-sensitive growth of the rpoH15 mutant of Escherichia coli. J Bacteriol. 1990 Apr;172(4):2124–2130. doi: 10.1128/jb.172.4.2124-2130.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yocum R. R., Hanley S., West R., Jr, Ptashne M. Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Oct;4(10):1985–1998. doi: 10.1128/mcb.4.10.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. York J. D., Majerus P. W. Isolation and heterologous expression of a cDNA encoding bovine inositol polyphosphate 1-phosphatase. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9548–9552. doi: 10.1073/pnas.87.24.9548. [DOI] [PMC free article] [PubMed] [Google Scholar]

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