Plant Molecular Biology

, Volume 54, Issue 6, pp 881–893 | Cite as

Tissue-specific expression and functional complementation of a yeastpotassium-uptake mutant by a salt-induced ice plant gene mcSKD1

  • Yingtzy Jou
  • Pin Chou
  • Mengchun He
  • Yuhui Hung
  • Hungchen Emilie Yen
Article

Abstract

A full-length salt-induced transcript homologous to SKD1 (suppressor of K+ transport growth defect) of the AAA (ATPase associated with a variety of cellular activities)-type ATPase family has been identified from the halophyte Mesembryanthemum crystallinum (ice plant). The expression of mcSKD1 was induced by 200 mM NaCl or higher in cultured ice plant cells. When cultured ice plant cells were grown in a high K+ (42.6 mM) medium, the level of mcSKD1 expression decreased. At the whole plant level, constitutive expression of mcSKD1 was observed in roots, stems, leaves and floral organs. Addition of 400 mM NaCl increased the transcript level in roots and stems. The expression of atSKD1, a homologue gene in Arabidopsis, was down regulated by salt stress. Under salt stress, mcSKD1 was preferentially expressed in the outer cortex of roots and stems and in the epidermal bladder cells of leaves. The mcSKD1 transcript was constitutively expressed in placenta and integuments of the developing floral buds. Expression of the full-length or C-terminal deletion of mcSKD1 was able to complement the K+ uptake-defect phenotype in mutant Saccharomyces cerevisiae, which is defective in high- and low-affinity K+ uptake. Deletion of the N-terminal coiled-coil motif of mcSKD1, a structure required for membrane association, resulted in greatly reduced K+ transport. Expression of mcSKD1 also increased the salt-tolerant ability of yeast mutants and either N- or C-terminal deletion decreased the efficiency. The physiological relevancies of mcSKD1 for K+ uptake under high salinity environments are discussed.

: AAA-type ATPase halophyte ice plant salt-induced gene mcSKD1 yeast complementation 

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References

  1. Adams, P., Nelson, D.E., Yamada, S., Chmara, W., Jensen, R.G., Bohnert, H.J. and Griffiths, H. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol. 138: 171–190.Google Scholar
  2. Babst, M., Katzmann, D.J., Estepa, E.J., Meerloo, T. and Emr, S.D. 2002. ESCRT-III: an endosome-assoicated heterooligomeric protein complex required for MVB sorting. Dev. Cell 3: 271–282.PubMedGoogle Scholar
  3. Babst, M., Wendland, B., Estepa, E.J. and Emr, S.D. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17: 2982–2993.PubMedGoogle Scholar
  4. Barkla, B.J., Zingaelli, L., Blumwald, E. and Smith, J.A.C. 1995. Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiol. 109: 549–556.PubMedGoogle Scholar
  5. Beyer, A. 1997. Sequence analysis of the AAA protein family. Protein Sci. 6: 2043–2058.PubMedGoogle Scholar
  6. Binzel, M.L., Hess, F.D., Bressan, R.A. and Hasegawa, P.M. 1988. Intracellular compartmentation of ions in salt adapted tobacco cells. Plant Physiol. 86: 607–614.Google Scholar
  7. Bishop, N. and Woodman, P. 2000. ATPase-defective mannalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11: 227–239.PubMedGoogle Scholar
  8. Chu, C., Dai, Z., Ku, M.S.B. and Edwards, G.E. 1990. Induction of Crassulacean acid metabolism in the facultative halophyte Mesembryanthemum crystallinum by abscisic acid. Plant Physiol. 93: 1253–1260.Google Scholar
  9. Esienberg, H. 1995. Perspectives in biochemistry and biophysics life in unusual environments: Progress in understanding the structure and function of enzymes from extreme halophilic bacteria. Arch. Biochem. Biophys. 318: 1–5.PubMedGoogle Scholar
  10. Fu, H.-H. and Luan, S. 1998. AtKUP1: A dual-affinity K + transporter from Arabidopsis. Plant Cell 10: 63–73.PubMedGoogle Scholar
  11. Fujita, H., Yamanaka, M., Imamura, K., Tanaka, Y., Nara, A., Yoshimori, T., Yokota, S. and Himeno, M. 2003. A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J. Cell Sci. 116: 401–414.PubMedGoogle Scholar
  12. Gietz, R.D., Schiestl, R.H., Willems, A.R. and Woods, R.A. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355–360.PubMedGoogle Scholar
  13. Golldack, D. and Dietz, K.-J. 2001. Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol. 125: 1354–1643.PubMedGoogle Scholar
  14. Gong, Z., Koiwa, H., Cushman, M.A., Ray, A., Bufford, D., Kore-eda, S., Matsumoto, T.K., Zhu, J., Cushman, J.C., Bressan, R.A. and Hasegawa, P.M. 2001. Genes that are uniquely stress regulated in salt overly sensitive (sos) mutants. Plant Physiol. 126: 363–375.PubMedGoogle Scholar
  15. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K. and Bohnert, H.J. 2000. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 463–499.PubMedGoogle Scholar
  16. Horie, T., Yoshida, K., Nakayama, H., Yamada, K., Oiki, S. and Shinmyo, A. 2001. Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J. 27: 129–138.PubMedGoogle Scholar
  17. Ko, C.H. and Gaber, R.F. 1991. TRK1 and TRK2 encode structurally related K+ transporters in Saccharomyces cerevisiae. Mol. Cell Biol. 11: 4266–4273.PubMedGoogle Scholar
  18. Leyman, B., Geelen, D. and Blatt, M.R. 2000. Localization and control of expression of Nt-Syr1, a tobacco snare protein. Plant J. 24: 369–381.PubMedGoogle Scholar
  19. Liu, J. and Zhu, J.K. 1997. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proc. Natl. Acad. Sci. USA 94: 14960–14964.PubMedGoogle Scholar
  20. Löw, R., Rockel, B., Kirsch, M., Ratajczak, R., Hörtensteiner, S., Martinoia, E., Lüttge, U. and Rausch, T. 1996. Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol. 110: 259–265.PubMedGoogle Scholar
  21. Madern, D., Ebel, C. and Zaccai, G. 2000. Halophilic adaptation of enzyme. Extremophiles 4: 91–98.PubMedGoogle Scholar
  22. Mäser, P., Hosoo, Y., Goshima, S., Horie, T., Eckelman, B., Yamada, K., Yoshida, K., Bakker, E.P., Shinmyo, A., Oiki, S., Schroeder, J.I. and Uozumi, N. 2002. Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc. Natl. Acad. Sci. USA 99: 6428–6433.PubMedGoogle Scholar
  23. Maurizi, M.R. and Li, C.C.H. 2001. AAA proteins: in search of a common molecular basis. EMBO Rep. 21: 980–985.Google Scholar
  24. Niu, X., Bressan, R.A., Hasegawa, P.M. and Pardo, J.M. 1995. Ion homeostasis in NaCl stress environments. Plant Physiol. 109: 735–742.PubMedGoogle Scholar
  25. Ogura, T. and Wilkinson, A.J. 2001. AAA + superfamily ATPase: common structure-diverse function. Gene Cells 6: 575–597.Google Scholar
  26. Périer, F., Coulter, K.L., Liang, H., Radeke, C.M., Garber, R.F. and Vandenberg, C.A. 1994. Identification of a novel mammalian member of the NSF/CDC48p/Pas1p/TBP-1 family through heterologous expression in yeast. FEBS Lett. 351: 286–290.PubMedGoogle Scholar
  27. Rains, D.W. and Epstein, E. 1967. Sodium absorption by barley roots: Its mediation by mechanism 2 of alkali cation transport. Plant Physiol. 42: 314–318.Google Scholar
  28. Rubio, F., Gassmann, W. and Schroeder, J.I. 1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270: 1660–1663.PubMedGoogle Scholar
  29. Rubio, F., Schwarz, M., Gassmann, W. and Schroeder, J.I. 1999. Genetic selection of mutations in the high affinity K+transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. J. Biol. Chem. 274: 6839–6847.PubMedGoogle Scholar
  30. Rus, A., Yokoi, S., Sharkuu, A., Reddy, M., Lee, B.-H., Matsumoto, T.K., Koiwa, H., Zhu, J.-K., Bressan, R.A. and Hasegawa, P.M. 2001. AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc. Natl. Acad. Sci. USA 98: 14150–14155.PubMedGoogle Scholar
  31. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  32. Sanderfoot, A.A., Kovaleva, V., Bassham, D.C. and Raikhel, N.V. 2001. Interactions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar compartment in Arabidopsis root cells. Plant Physiol. 121: 929–938.Google Scholar
  33. Santa-Maria, G.E., Rubio, F., Dubcovsky, J. and Rodgriguez-Navarro, A. 1997. The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9: 2281–2289.PubMedGoogle Scholar
  34. Schachtman, D.P. and Schroeder, J.I. 1994. Structure and transport mechanism of a high affinity potassium uptake transporter from higher plants. Nature 370: 655–658.PubMedGoogle Scholar
  35. Scheuring, S., Bodor, O., Röhricht, R.A., Müller, S., Beyer, A. and Köhrer, K. 1999. Cloning, characterisation, and functional expression of the Mus musculus SKD1 gene in yeast demonstrates that the mouse SKD1 and the yeast VPS4 genes are orthologues and involved in intracellular protein trafficking. Gene 234: 149–159.PubMedGoogle Scholar
  36. Su, H., Golldack, D., Zhao, C. and Bohnert, H.J. 2002. The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol. 129: 1482–1493.PubMedGoogle Scholar
  37. Treichel, S. 1986. The influence of NaCl on △-pyrroline-5-carboxylate reductase in proline-accumulating cell suspension cultures of Mesembryanthemum nodiflorum and other halophytes. Physiol. Plant 67: 173–181.Google Scholar
  38. Uozumi, N., Kim, E.J., Rubio, F., Yamaguchi, T., Muto, S., Tsuboi, A., Bakker, E.P., Nakamura, T. and Schroeder, J.I. 2000. The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in Xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol. 122: 1249–1259.PubMedGoogle Scholar
  39. Vera-Estrella, R., Barkla, B.J., Bohnert, H.J. and Pantoja, O. 1999. Salt stress in Mesembryanthemum crystallinum L. cell suspensions activates adaptive mechanisms similar to those observed in the whole plant. Planta 207: 426–435.PubMedGoogle Scholar
  40. Walker, J.E., Saraste, M.J., Runswick, J.J. and Gay, N.J. 1982. Distantly related sequences in the alpha-and beta-subunits of ATP synthase myosin kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1: 945–951.PubMedGoogle Scholar
  41. Watad, A-EA., Reinhold, L. and Lerner, H.R. 1983. Comparison between a stable NaCl-selected Nicotiana cell line and the wild type. K+, Na+, and proline pools as a function of salinity. Plant Physiol. 73: 624–629.Google Scholar
  42. Wu, S.-J., Ding, L. and Zhu, J.K. 1996. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617–627.PubMedGoogle Scholar
  43. Yen, H.E., Grimes, H.D. and Edwards, G.E. 1995. The effects of high salinity, water-deficit, and abscisic acid on phosphoenolpyruvate carboxylase activity and proline accumulation in Mesembryanthemum crystallinum cell cultures. J Plant Physiol. 145: 557–564.Google Scholar
  44. Yen, H.E., Wu, S-M., Hong, Y.-H. and Yen, S.-K. 2000. Isolation of 3 salt-induced low-abundance cDNAs from lightgrown callus of Mesembryanthemum crystallinum by suppression subtractive hybridization. Physiol. Plant 110: 402–409.Google Scholar
  45. Yen, H.E., Zhang, D., Lin, J-H., Edwards, G.E. and Ku, M.S.B. 1997. Salt-induced changes in protein composition in light-grown callus of Mesembryanthemum crystallinum. Physiol. Plant 101: 526–532.Google Scholar
  46. Yen, S.K., Chung, M.-C., Chen, P.-C. and Yen, H.E. 2001. Environmental and developmental regulation of a wound-induced cell wall protein WI12 in halophyte Mesembryanthemum crystallinum. Plant Physiol. 127: 517–528.PubMedGoogle Scholar
  47. Yeo, S.C.L., Xu, L., Ren, J., Boulton, V.J., Wagle, M.D., Liu, C., Ren, G., Wong, P., Zahn, R., Sasajala1, P., Yang, H., Piper, R.C. and Munn, A.L. 2003. Vps20p and Vta1p interact with Vps4p and function in multivesicular body sorting and endosomal transport in Saccharomyces cerevisiae. J. Cell Sci. 116: 3957–3960.PubMedGoogle Scholar
  48. Yoshimori, T., Yamagata, F., Yamamoto, A., Mizushima, N., Kabeya, Y., Nara, A., Miwako, I., Ohashi, M., Ohsumi, M. and Ohsumi, Y. 2000. The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Mol. Biol. Cell 11: 747–763.PubMedGoogle Scholar
  49. Zhu, J.K. 2001. Plant salt tolerance. Trends Plant Sci. 6: 66–71.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Yingtzy Jou
    • 1
  • Pin Chou
    • 1
  • Mengchun He
    • 1
  • Yuhui Hung
    • 1
  • Hungchen Emilie Yen
    • 1
  1. 1.Department of Life SciencesNational Chung-Hsing UniversityTaiwan

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