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Plant Molecular Biology

, Volume 47, Issue 5, pp 571–579 | Cite as

A catalytic subunit of the sugar beet protein kinase CK2 is induced by salt stress and increases NaCl tolerance in Saccharomyces cerevisiae

  • Rodolphe Kanhonou
  • Ramon Serrano
  • Roc Ros Palau
Article

Abstract

Salinity is an important limiting factor in plant growth and development. We have cloned a catalytic subunit of the sugar beet protein kinase CK2 (BvCKA2) by functional expression in yeast of a NaCl-induced cDNA library. BvCKA2 was able to increase the yeast tolerance to NaCl and to functionally complement the cka1 cka2 yeast double mutant upon over-expression. Southern blot analysis indicated that, in sugar beet, the BCKA2 gene is a member of a multigene family. The mRNA levels of BvCKA2 were up-regulated in response to NaCl stress which suggests that protein kinase CK2 may be involved in the plant response to salt stress.

Beta vulgaris CK2 catalytic subunit NaCl stress Saccharomyces cerevisiae 

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References

  1. Allende, J.E. and Allende, C.C. 1995. Protein kinase CK2: an en-zyme with multiple substrates and a puzzling regulation. FASEB J. 9: 313–323.Google Scholar
  2. Apse, M.P., Ahoron, G.S., Sneddeb, W.A. and Blumwald E. 1999. Salt tolerance conferred by overexpression of a vacuolar Na +/H +antiport in Arabidopsis. Science 285: 1256–1258.Google Scholar
  3. BaÑuelos, M.A., Sychrov, H., Bleykasten-Grosshans, C., Souciet, J.L. and Potier S. 1998. The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144: 2749–2758.Google Scholar
  4. Bidwai, A.P., Reed, J.C. and Glover, C.V. 1995. Cloning and dis-ruption of CKB1, the gene encoding the 38-kDa β subunit of Saccharomyces cerevisiae casein kinase II (CKII). Deletion of CKII regulatory subunits elicits a salt-sensitive phenotype. J. Biol. Chem. 270: 10395–10404.Google Scholar
  5. Brunelli, J.P. and Pall, M.L. 1993. A series of yeast/Escherichia coli λ expression vectors designed for directional cloning of cDNAs and cre/lox-mediated plasmid excision. Yeast 9: 1309–1318.Google Scholar
  6. Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.Google Scholar
  7. Davies, L.G., Dibner, M.D. and Battey, J.F. 1986. Basic Methods in Molecular Biology. Elsevier, Amsterdam, pp. 143–146.Google Scholar
  8. Donald, R.G.K. and Cashmore, A.R. 1990. Mutation in either G box or I box sequences profoundly affects expression from the Ara-bidopsis thaliana rbcS-1A promoter. EMBO J. 9: 1717–1726.Google Scholar
  9. Espunya, M.C., Combettes, B., Dot, J., Chaubet-Gigot, N. and Martinez, M.C. 1999. Cell-cycle modulation of CK2 activity in tobacco BY-2 cells. Plant J. 19: 655–666.Google Scholar
  10. Gaxiola, R., Larrinoa, I.F., Villalba, J.M. and Serrano, R. 1992. A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J. 11: 3157–3164.Google Scholar
  11. Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L. and Fink, G.R. 1999. The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc. Natl. Acad. Sci.USA 96: 1480–1485.Google Scholar
  12. Garciadeblas, B., Rubio, F., Quintero, F.J., BaÑuelos, M.A., Haro, R. and Rodriguez-Navarro, A. 1993. Differential expression of two genes encoding isoforms of the ATPase involved in sodium efflux in Saccharomyces cerevisiae. Mol. Gen. Genet. 236: 363–368.Google Scholar
  13. Gietz, D., Jean, A.S.T., Woods, R.A. and Schiestl, R.H. 1992. Improved method for high efficiency transformation of yeast cells. Nucl. Acids Res. 20: 1425.Google Scholar
  14. Glover, C.V.C. 1998. On the physiological role of casein kinase II in Saccharomyces cerevisiae. In: Progress in Nucleic Acid Research and Molecular Biology, Academic Press, New York, pp. 95–133.Google Scholar
  15. Greenway, H. and Munns, R. 1980. Mechanisms of salt tolerance in nonhalophytes. Annu. Rev. Plant Physiol. 31: 149–190.Google Scholar
  16. Grein, S., Raymond, K., Cochet, C., Pyerin, W., Chambaz, E.M. and Filhol, O. 1999. Searching interaction partners of protein kinase CK2β subuntit by two-hybrid screening. Mol. Cell. Biochem. 191: 105–109.Google Scholar
  17. Hanna, D.E., Rethinaswamy, A. and Glover, C.V. 1995. Casein ki-nase II is required for cell cycle progression during G 1 and G 2 /M in Saccharomyces cerevisiae. J. Biol. Chem. 270: 25905–25914.Google Scholar
  18. Hanks, S.K. and Hunter, T. 1995. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9: 576–596.Google Scholar
  19. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K. and Bonnert, H.J. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 463–499.Google Scholar
  20. Hirt, H. 1997. Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci. 2: 11–15.Google Scholar
  21. Holappa, L.D. and Walker-Simmons, M.K. 1995. The wheat abscisic acid-responsive protein kinase mRNA, PKABA1, is upregulated by dehydration, cold temperature, and osmotic stress. Plant Physiol. 108: 1203–1210.Google Scholar
  22. Hwang, I. and Goodman, H.M. 1995. An Arabidipsis thaliana root-specific kinase homolog is induced by dehydration, ABA, and NaCl. Plant J. 8: 37–43.Google Scholar
  23. Kovtun, Y., Chiu, W.-L., Tena, G. and Sheen, J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97: 2940–2945.Google Scholar
  24. Kuo, M.-H, Nadeau, E.T. and Grayhack E.J. 1997. Multiple phosphorylated forms of the Saccharomyces cerevisiae Mcm1 protein include an isoform induced in response to high salt concentra-tions. Mol. Cell. Biol. 17: 819–832.Google Scholar
  25. Lauchli, A. and Epstein, E. 1990. Plant responses to saline and sodic conditions. In: K.K. Tanji (Ed.) Agricultural Salinity Assessments and Management, American Society of Civil Engineers, New York, pp. 113–137.Google Scholar
  26. Lee, Y., Lloyd, A.M. and Roux, S.J. 1999. Antisense expression of the CK2 α-subunit gene in Arabidopsis. Effects on light-regulated gene expression and plant growth. Plant Physiol. 119: 989–1000.Google Scholar
  27. Liu, J., Ishitani, M., Halfter, U., Kim, C.-S. and Zhu, J.-K. 2000. The Arabidopsis thaliana SOS2 encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. USA 97: 3730–3734.Google Scholar
  28. Ludwig, S.R., Oppenheimer, D.G., Silflow, C.D., and Snustad, D.P. 1987. Characterization of the α-tubulin gene family of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 84: 5833–5837.Google Scholar
  29. Maeda, T., Takekawa, M. and Saito, H. 1995. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science 269: 554–558.Google Scholar
  30. Marschner, H. 1995. Mineral Nutrition of Higher Plants. Springer-Verlag, Berlin.Google Scholar
  31. Mikami, K., Katagiri, T., Iuchi, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. 1998. A gene encoding phosphatidylinositol-4-phosphate 5-kinase is induced by water stress and abscisic acid in Arabidopsis thaliana. Plant J. 15: 563–568.Google Scholar
  32. Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N., Kamada, H. and Shinozaki, K. 1993. Cloning and characterization of two cDNAs encoding casein kinase II catalytic subunits in Arabidopsis thaliana. Plant Mol. Biol. 21: 279–289.Google Scholar
  33. Mizoguchi, T., Hayashida, N., Yamaguchi-Shinozaki, K., Kamada, H. and Shinozaki, K. 1995. Two genes that encode ribosomal-protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana. FEBS Lett. 358: 199–204.Google Scholar
  34. Mizoguchi, T., Ichimura, K. and Shinozaki, K. 1997. Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol. 15: 15–19.Google Scholar
  35. Mikolajczyk, M., Awotunde, O.S., Muszynska, G., Klessig, D.F. and Dobrowolska, G. 2000. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog protein kinase ASK1 in tobacco cells. Plant Cell 12: 165–178.Google Scholar
  36. Munnik, T., Ligterink, W., Meskiene, I., Calderini, O., Beyerly, J., Musgrave, A. and Hirt, H. 1999. Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J. 20: 381–388.Google Scholar
  37. Münstermann, U., Fritz, G., Seitz, G., Lu, Y.P., Schneider, H.R. and Issinger, O.G. 1990. Casein kinase II is elevated in solid human tumours and rapidly proliferating non-neoplastic tissue. Eur. J. Biochem. 189: 251–257.Google Scholar
  38. Nadal, E., Calero, F., Ramos, F. and AriÑo, J. 1999. Biochemical and genetic analyses of the role of yeast casein kinase 2 in salt tolerance. J. Bact. 181: 6456–6462.Google Scholar
  39. Niefind, K., Guerra, B., Pinna, L.A., Issinger, O.G. and Schomburg, D. 1998. Crystal structure of the catalytic subunit of protein kinase CK2 from Zea mays at 2.1Å resolution. EMBO J. 17: 2451–2462.Google Scholar
  40. Padmanabha, R., Chen-Wu, J.L., Hanna, E. and Glover, C.V.C. 1990. Isolation, sequencing and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 4089–4099.Google Scholar
  41. Piao, H.L., Pih, K.T., Lim, J.H., Kang, S.G., Jin, J.B., Kim, S.H. and Hwang, I. 1999. An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. Plant Physiol. 119: 1527–1534.Google Scholar
  42. Quintero, F.J., Garciadeblas, B. and Rodriguez-Navarro, A. 1996. 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. Plant Cell 8: 529–537.Google Scholar
  43. Rogers, S.O. and Bendich, A.J. 1994. Extraction of total cellular DNA from plants, algae and fungi. In: S.B. Gelvin and R.A. Schilperoort (Eds.) Plant Molecular Biology Manual, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. D1: 1–8.Google Scholar
  44. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K. and Izui, K. 2000. Overexpression of a single Ca 2 +-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J. 23: 319–327.Google Scholar
  45. Serrano, R. 1996. Salt tolerance in plants and microorganisms: toxicity targets and defense responses. Int. Rev. Cytiol. 165: 1–52.Google Scholar
  46. Sheen, J. 1996. Ca 2 +-dependent protein kinases and stress signal transduction in plants. Science 274: 1900–1902.Google Scholar
  47. Shi, H., Ishitani, M., Kim, C. and Zhu, J.K. 2000. The Arabidopsis thaliana gene SOS1 encodes a putative Na +/H +antiporter. Proc. Natl. Acad. Sci. USA 97: 6896–68901.Google Scholar
  48. Shinozaki, K. and Yamaguchi-Shinozaki, K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiol. 115: 327–334.Google Scholar
  49. Sugano, S., Andronis, C., Ong, M.S., Green, R.M., Wang, Z-Y. and Tobin, E.M. 1998. Protein kinase CK2 interacts with and phosphorylates the Arabidopsis circadian clock-associated 1 protein. Proc. Natl. Acad. Sci. USA. 95: 11020–11025.Google Scholar
  50. Sugano, S., Andronis, C., Ong, M.S., Green, R.M. and Tobin, E.M. 1999. The protein kinase CK2 is involved in regulation of circadian rhythms in Arabidopsis. Proc. Natl. Acad. Sci. USA. 96: 12362–12366.Google Scholar
  51. Tenney, K.A. and Glover, C.V.C. 1999. Transcriptional regulation of S. cerevisiae ENA1 gene by casein kinase II. Mol. Cell Biochem. 191: 161–167.Google Scholar
  52. Urao, T., Katagiri, T., Mizoguchi, T., Yamaguchi-Shinozaki, K., Hayashida, N. and Shinozaki, K. 1994. Two genes that encode Ca 2 +-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol. Gen. Genet. 244: 331–340.Google Scholar
  53. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T. and Shinozaki, K. 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell. 11: 1743–1754.Google Scholar
  54. Urao, T., Yamaguchi-Shinozaki, K. and Shinozaki, K. 2000. Two component systems in plant signal transduction. Trends Plant Sci. 5: 67–74.Google Scholar
  55. Wallis, J.W., Chrebet, G., Brodsky, G., Rolfe, M. and Rothstein, R. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58: 409–419.Google Scholar
  56. Zhu, J.-K., Liu, J. and Xiong, L. 1998. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell. 10: 1181–1191.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Rodolphe Kanhonou
    • 1
  • Ramon Serrano
    • 1
  • Roc Ros Palau
    • 2
  1. 1.Instituto de Biología Molecular y Celular de PlantasUniversidad Politécnica de Valencia-CSICValenciaSpain
  2. 2.Departament de Biologia Vegetal, Facultat de Ciències BiològiquesUniversitat de ValenciaBurjassot (Valencia)Spain

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