Journal of Plant Research

, 111:411 | Cite as

Early salt-stress effects on expression of genes for aquaporin homologues in the halophyte sea aster (Aster tripolium L.)

  • Yuichi Uno
  • Takeshi Urao
  • Kazuko Yamaguchi-Shinozaki
  • Michio Kanechi
  • Noboru Inagaki
  • Susumu Maekawa
  • Kazuo Shinozaki
Original Articles

Abstract

Six partial PCR fragments that encode aquaporin homologues in the halophyte sea asterAster tripolium were cloned using genomic DNA and cDNA as templates. The deduced amino acid sequences were highly similar to those of other major intrinsic proteins (MIPs) in plants. The expression patterns of sea astermip genes in leaves and suspension-cultured cells during a 24-hr NaCL stress period were studied with PCR samip (sea aster major intrinsic protein) fragments. Three samip (A-C) fragments were obtained by PCR with genomic DNA as templates, and 3 samip (D-F) fragments were obtained by RT-PCR. Among the 6 genes, expression ofSamip A, B, andC was significantly inducible by salt stress. The level ofSamip A, B andC mRNAs was dependent on NaCL concentration in both whole plants and cultured cells. However, no significant accumulation ofSamip transcripts was observed in salt-adapted cells. These observations suggest thatSamip A, B andC genes play an important role in the early salt-adaptable stage in sea asters.

Key words

Adapted cell Cell suspension culture Major intrinsic protein NaCl stress Salt tolerance Water channel protein 

Abbreviations

MIP

major intrinsic protein

P-5-C

Δ1-pyrroline-5-carboxylase

RT-PCR

reverse transcription PCR

References

  1. Agre, P., Preston, G.M., Smith, B.L., Jung, J.S., Raina, S., Moon, C., Guggino, W.B. andNielsen, S. 1993. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol.,265: 463–476.Google Scholar
  2. Barkla, B.J. andBlumwald, E. 1991. Identification of a 170-kDa protein associated with the vacuolar Na+/H+ antiport ofBeta vulgaris. Proc. Natl. Acad. Sci. USA88: 11177–11181.PubMedCrossRefGoogle Scholar
  3. Cairney, J., Newton, R.J., Funkhouser, E.A., Chang, S. andHayes, D. 1995. Nucleotide Sequence of a cDNA for a water channel protein (Aquapprin) homolog fromAtriplex canescens (Pursh.) Nutt. Plant Physiol.108: 1291–1292.CrossRefGoogle Scholar
  4. Chrispeels, M.J. andAgre, R. 1994. Aquaporins: The molecular basis of facilitated water movement through living plant cells? Plant Physiol.105: 9–13.PubMedCrossRefGoogle Scholar
  5. Chrispeels, M.J. andMaurel, C. 1994. Aquaporins: Water channel proteins of plant and animal cells. Trends Biol. Sci.1g: 421–425.CrossRefGoogle Scholar
  6. Culianez-Macia, F.A. andMartin, C. 1993. DIP: a member of the MIP family of membrane proteins that is expressed in mature seed and dark-grown seedlings ofAntirrhinum majus. Plant J.4: 717–725.PubMedCrossRefGoogle Scholar
  7. Daniels, M.J., Mlrkov, T.E. andChrispeels, M.J. 1994. The plasma membrane ofArabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol.106: 1325–1333.PubMedCrossRefGoogle Scholar
  8. Flowers, T.J., Troke, P.F. andYeo, A.R. 1977. The mechanism of salt tolerance in halophytes. Annu. Rev. Plant Physiol.28: 89–121.CrossRefGoogle Scholar
  9. Fray R.G., Wallace, A., Grierson, D. andLycett, G.W. 1994. Nucleotide sequence and expression of a ripening and water stress-related cDNA from tomato with homology to the MIP class of membrane channel proteins. Plant Mol. Biol.24: 539–543.PubMedCrossRefGoogle Scholar
  10. Goas, G., Goas, M. andLarher, F. 1982. Accumulation of free proline and glycine betaine inAster tripolium subjected to a saline shock: A kinetic study related to light period. Physiol. Plant.55: 383–388.CrossRefGoogle Scholar
  11. Gorin, M.B., Yancey, S.B., Cline, J., Revel, J.R. andHorwitz, J. 1984. The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning. Cell39: 49–59.PubMedCrossRefGoogle Scholar
  12. Guerrero, F.D., Jones, J.T. andMullet, J.E. 1990. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted: Sequence and expression of three inducible genes. Plant Mol. Biol.15: 11–26.PubMedCrossRefGoogle Scholar
  13. Henzler, T. andSteudle, E. 1995. Reversible closing of water channels inChara intermodes provides evidence for a composite transport model of the plasma membrane. J. Exp. Bot.46: 199–209.Google Scholar
  14. Höfte, H., Hubbard, L., Reizer, J., Ludevid, D., Herman, E.M. andChrispeels, M.J. 1992. Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane ofArabidopsis thaliana. Plant Physiol.99: 561–570.PubMedCrossRefGoogle Scholar
  15. Johnson, K.D., Höfte, H. andChrispeels, M.J. 1990. An intrinsic tonoplast protein of protein storage vacuoles in seeds in structurally related to a bacterial solute transporter (GlpF). Plant Cell2: 525–532.PubMedCrossRefGoogle Scholar
  16. Kammerloher, W., Fischer, U., Piechour, G. andSchaffner, A.R. 1994. Water channels in the plasma membrane cloned by immunoselection from a mammalian expression system. Plant J.6: 187–199.PubMedCrossRefGoogle Scholar
  17. Knepper, M.A. 1994. The aquaporin family of molecular water channels. Proc. Natl. Acad. Sci. USA.91: 6255–6258.PubMedCrossRefGoogle Scholar
  18. Liu, Q., Umeda, M. andUchlyama, H. 1994. Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol. Biol.26: 2003–2007.PubMedCrossRefGoogle Scholar
  19. Logemann, J., Schell, J. andWillmitzer, L. 1987. Improved method for the isolation of RNA from plant tissues. Anal. Biochem.163: 16–20.PubMedCrossRefGoogle Scholar
  20. Löw, R., Rockel, B., Kirsch, M., Ratajczak, R., Hdrtensteiner, S., Martinoia, E., Luttge, U. andRausch, T. 1996. Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves ofMesembryanthemum crystallinum. Plant Physiol.110: 259–265.PubMedCrossRefGoogle Scholar
  21. Maniatis, T., Fritsch, E.F. andSambrook, J. 1982. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  22. Maurel, C., Reizer, J., Schroeder, J.I. andChrispeels, M.J. 1993. The vacuolar membrane protein γ-TIP creates water specific channels inXenopus oocytes. EMBO J.12: 2241–2247.PubMedGoogle Scholar
  23. Miao, G.H. andVerma, D.P. 1993. Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell5: 781–794.PubMedCrossRefGoogle Scholar
  24. Nagy, F., Kay, S.A. andChua, N.-H. 1988. Analysis of gene expression in transgenic plants.In S.V. Gelvin and R.A. Schiperoort, eds., Plant Molecular Biology Manual, B4. pp. 1–29. Kluwer Academic Publishers, Dordrecht.Google Scholar
  25. Niu, X., Narasimhan, M.L., Salzman, R.A., Bressan, R.A. andHasegawa, P.M. 1993. NaCl regulation of plasma membrane H+-ATPase gene expression in a glycophyte and a halophyte. Plant Physiol.103: 713–718.PubMedCrossRefGoogle Scholar
  26. Pao, J.M., Wu, L.F., Höfte, H., Chrispeels, M.J., Sweet, G., Sandal, N.N. andSaier, M.H. Jr. 1991. Evolution of the MIP family of integral membrane transport proteins. Mol. Microbiol.5: 33–37.PubMedGoogle Scholar
  27. Perera, L.K.R.R., Mansfield, T.A. andMalloch, A.J.C. 1994. Stomatal responses to sodium ions inAster tripolium: a new hypothesis to explain salinity regulation in above-ground tissues. Plant Cell Env.7: 335–340.CrossRefGoogle Scholar
  28. Qi, X., Tai, C. andWasserman, B.P. 1995. Plasma membrane intrinsic proteins ofBeta vulgaris L. Plant Physiol.108: 387–392.PubMedCrossRefGoogle Scholar
  29. Sandal, N.N. andMarcker, K.A. 1988. Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucleic Acids Res.16: 9347.PubMedGoogle Scholar
  30. Treichel, S. 1986. The influence of NaCl on Δ1-pyrroline-5-carboxylate reductase in proline-accumulating cell suspension cultures ofMesembryanthemum nodiflorum and other halophytes. Physiol. Plant.67: 173–181.CrossRefGoogle Scholar
  31. Uno, Y., Kanechi, M., Inagaki, N., Sugimoto, M. andMaekawa, S. 1996a. The evaluation of salt tolerance in germination and vegetative growth of asparagus, table beet and sea aster. J. Jap. Soc. Hort. Sci.65: 579–585.CrossRefGoogle Scholar
  32. Uno, Y., Kanechi, M., Inagaki, N., Taki, N. andMaekawa, S. 1996b. Growth and protein profile responses in the halophyte sea aster (Aster tripolium L.) suspension-cultured cells to salinity. J. Plant Res.109: 409–414.CrossRefGoogle Scholar
  33. Yamaguchi-Shinozaki, K., Koizumi, M., Urao, S. andShinozaki, K. 1992. Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation inArabidopsis thaliana: Sequence analysis of one cDNA that encodes a putative transmembrane channel protein. Plant Cell Physiol.33: 217–224.Google Scholar
  34. Yamada, S., Katsuhara, M., Kelly, W.B., Michalowski, C.B. andBohnert, H.J. 1995. A family of transcripts encoding water channel proteins: Tissue-specific expression in the common ice plant. Plant Cell7: 1129–1142.PubMedCrossRefGoogle Scholar
  35. Yamamoto, Y.T., Taylor, C.G., Acedo, G.N., Cheng, C.-L. andConkling, M.A. 1991. Characterization ofcis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell3: 371–382.PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan 1998

Authors and Affiliations

  • Yuichi Uno
    • 1
    • 2
    • 3
    • 4
  • Takeshi Urao
    • 2
  • Kazuko Yamaguchi-Shinozaki
    • 2
  • Michio Kanechi
    • 4
  • Noboru Inagaki
    • 1
  • Susumu Maekawa
    • 1
  • Kazuo Shinozaki
    • 3
  1. 1.Division of Environmental Science, The Graduate School of Science & TechnologyKobe UniversityKobeJapan
  2. 2.Biological Resources Division, Japan International Research Center for Agricultural Science (JIRCAS)Ministry of Agriculture, Forestry and FisheriesTsukuba, IbarakiJapan
  3. 3.Laboratory of Plant Molecular Biology, The Institute of Physical and Chemical Research (RIKEN)Tsukuba, Life Science CenterTsukuba, IbarakiJapan
  4. 4.Faculty of AgricultureKobe UniversityKobeJapan

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