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Expression of two PIP genes in rapidly growing internodes of rice is not primarily controlled by meristem activity or cell expansion

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Abstract

Membrane intrinsic proteins facilitate movement of small molecules often times functioning as water channels. We have identified two genes from rice which encode proteins with characteristic features of plasma membrane intrinsic proteins (PIP). They possess six membrane-spanning domains, an NPA repeat, overall high sequence homologies and characteristic C- and N-terminal hallmark motifs which allowed assignment of OsPIP1a to the PIP1 subfamily and of OsPIP2a to the PIP2 subfamily. OsPIP1a and OsPIP2a showed similar but not identical expression patterns. The two genes were expressed at higher levels in seedlings than in adult plants and expression in the primary root was regulated by light. In internodes of deepwater rice plants which were induced to grow rapidly by submergence, transcript levels were slightly induced in the intercalary meristem (IM) and slightly reduced in the elongation zone (EZ) after 18 h. In internodes of GA-induced excised stem sections transcript levels transiently declined in the IM and EZ after 1 h and subsequently recovered to elevated levels after 18 h. GA also induced OsPIP expression in non-growing tissue after 18 h. In the IM of submergence-induced stem sections transcript levels remained constitutive. The different growth-promoting treatments showed no direct correlation between growth rate and OsPIP gene expression in dividing or expanding cells. In fact, treatment of excised stem sections with ABA or drought stress induced similar changes in OsPIP expression in the growing zone during the first 6 h as GA did. We conclude that regulation of OsPIP1a and OsPIP2a expression is not primarily controlled by growth. GA-induced growth may however change the water status of cells which in turn results in altered PIP abundance.

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References

  • Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.

    Article  PubMed  Google Scholar 

  • Bairoch, A. and Apweiler, R. 1998. The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1998. Nucl. Acids Res. 26: 38–42.

    PubMed  Google Scholar 

  • Barker, M.E. and Saier, M.H. Jr. 1990. A common ancestor for bovine lens fiber major intrinsic protein, nodulin 26 protein and E.coliglycerol facilitator. Cell 60: 185–186.

    Article  PubMed  Google Scholar 

  • Bleecker, A.B., Schuette, J.L. and Kende, H. 1986. Anatomical analysis of growth and developmental patterns of deepwater rice. Planta 169: 490–497.

    Google Scholar 

  • Cosgrove, D.J. 1993. Water uptake by growing cells: an assessment of the controlling roles of wall relaxation, solute uptake, and hydraulic conductance. Int. J. Plant Sci. 154: 10–21.

    PubMed  Google Scholar 

  • Dellaporta, S.L., Wood, J. and Hicks, J.B. 1983. A plant DNA minipreparation: Version II. Plant Mol. Biol. Rep. 1(4): 19–21.

    Google Scholar 

  • Guerrero, F.D., Jones, J.T. and Mullet, 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.

    Google Scholar 

  • Hanahan, D. 1993. Studies on transformation of Escherichia coliwith plasmids. J. Mol. Biol. 166: 557.

    Google Scholar 

  • Hoffmann-Benning, S. and Kende, H. 1992. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol. 99: 1156–1161.

    Google Scholar 

  • Johansson, I., Larsson, C., Ek, B. and Kjellbom, P. 1996. The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2C and apoplastic water potential. Plant Cell 8: 1181–1191.

    PubMed  Google Scholar 

  • Kaldenhoff, R., Kölling, A.G. and Richter, G. 1993. A novel blue light-and abscisic acid-inducible gene of Arabidopsis thalianaencoding an intrinsic membrane protein. Plant Mol. Biol. 23: 1187–1198.

    PubMed  Google Scholar 

  • Kaldenhoff, R., Kölling, A.G., Meyers, J., Karmann, U., Ruppel, G. and Richter, G. 1995. The blue light-responsive AthH2gene of Arabidopsis thalianais primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasma membrane. Plant J 7: 87–95.

    PubMed  Google Scholar 

  • Kaldenhoff, R., Grote, K., Zhu, J.-J. and Zimmermann, U. 1998. Significance of plasmalemma aquaporins for water transport in Arabidopsis thaliana. Plant J. 14: 121–128.

    Google Scholar 

  • Kammerloher, W., Fischer, U., Piechottka, G.P. and Schäffner, A.R. 1994. Water channels in the plasma membrane cloned by immunoselection from a mammalian expression system. Plant J. 6: 187–199.

    PubMed  Google Scholar 

  • Lee, S.H. and Clark, J.B. 1997. High-yield method for isolation of λDNA. BioTechniques 23: 598–600.

    PubMed  Google Scholar 

  • Lorbiecke, R. and Sauter, M. 1998. Induction of cell growth and cell division in the intercalary meristem of submerged deepwater rice (Oryza sativaL.). Planta 204: 140–145.

    Google Scholar 

  • Manfioletti, G. and Schneider, C. 1988. A new and fast method for preparing high quality lambda DNA suitable for sequencing. Nucl. Acids Res. 16: 2873–2884.

    PubMed  Google Scholar 

  • Maurel, C. 1997. Aquaporins and water permeability of plant membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 399–429.

    PubMed  Google Scholar 

  • Maurel, C., Reizer, J., Schroeder, J.I. and Chrispeels, M.J. 1993. The vacuolar membrane protein γ-TIP creates water specific channels in Xenopusoocytes. EMBO J. 15: 3028–3035.

    Google Scholar 

  • Maurel, C., Tacnet, F., Güclü, J. Guern, J. and Ripoche, P. 1997. Purified vesicles of tobacco cell vacuolar and plasma membranes exhibit dramatically different water permeability and water channel activity. Proc. Natl. Acad. Sci USA 94: 7103–7108.

    PubMed  Google Scholar 

  • Nicholas, K.B., Nicholas, H.B. Jr. 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. www.cris.com/”ketchup/genedoc.shtml

  • Niemitz, C.M. and Tyerman, S.D. 1997. Characterization of water channels in wheat root membrane vesicles. Plant Physiol. 115: 561–567.

    PubMed  Google Scholar 

  • Philipps, A.L. and Huttly, A.K. 1994. Cloning of two gibberellinregulated cDNAs from Arabidopsis thalianaby subtractive hybridization: expression of the tonoplast water channel, γ-TIP, is increased by GA3. Plant Mol. Biol. 24: 603–615.

    PubMed  Google Scholar 

  • Preston, G.M., Caroll, T.P., Guggino, W.B. and Agre, P. 1992. Appearance of water channels in Xenopusooxytes expressing red cell CHIP28 protein. Science 256: 385–387.

    PubMed  Google Scholar 

  • Puissant, C. and Houdebine, L.-M. 1990. An improvement of the single step method of RNA isolation by acid guanidinum thiocyanate-phenol-chloroform extraction. BioTechniques 8: 148–149.

    PubMed  Google Scholar 

  • Qi, X., Tai, C.-Y. and Wasserman, B.P. 1995. Plasma membrane intrinsic proteins of Beta vulgarisL. Plant Physiol. 108: 387–392.

    Google Scholar 

  • Raskin, I. and Kende, H. 1984a. Role of gibberellin in the growth response of submerged deepwater rice. Plant Physiol. 76: 947–950.

    Google Scholar 

  • Raskin, I. and Kende, H. 1994b. Regulation of growth in stem sections of deepwater rice. Planta 160: 66–72.

    Google Scholar 

  • Reizer, J., Reizer, A., Saier, M.H. Jr. 1993. The MIP family of integral membrane channel proteins: sequence comparisons, evolutionary relationships, reconstructed pathway of evolution and proposed functional differentiation of the two repeated halves of the proteins. Crit. Rev. Biochem. Mol. Biol. 28: 235–257.

    Google Scholar 

  • Robinson, D.G., Sieber, H., Kammerloher, W. and Schäffner, A.R. 1996. PIP1 aquaporins are concentrated in plasmalemmasomes of Arabidopsis thalianamesophyll. Plant Physiol. 111: 645–649.

    PubMed  Google Scholar 

  • Rose-John, S. and Kende, H. 1985. Short-term growth response of deep-water rice to submergence and ethylene. Plant Sci. 38: 129–134.

    Google Scholar 

  • Saier, M.H. Jr. 1994. Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, evolution. Microbiol. Rev. 58: 71–93.

    PubMed  Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Sanger, F., Nicklen, S. and Coulsen, A.R. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.

    PubMed  Google Scholar 

  • Sauter, M. 1997. Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2genes from rice during the cell cycle and in response to gibberellin. Plant J. 11: 181–190.

    PubMed  Google Scholar 

  • Sauter, M. and Kende, H. 1992. Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188: 362–368.

    Google Scholar 

  • Sauter, M., Seagull, R.W. and Kende, H. 1993. Internodal elongation and orientation of cellulose microfibrils and microtubules in deepwater rice. Planta 190: 354–362.

    Google Scholar 

  • Schäffner, A.R. 1998. Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204: 131–139.

    PubMed  Google Scholar 

  • Stünzi, J.T. and Kende, H. 1989. Gas composition in the internal air space of deepwater rice in relation to growth induced by submergence. Plant Cell Physiol. 30: 49–56.

    Google Scholar 

  • Weig, A., Deswarte, C. and Chrispeels, M.J. 1997. The major intrinsic protein family of Arabidopsishas 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol. 114: 1347–1357.

    PubMed  Google Scholar 

  • Yamada, S. Katsuhara, M., Kelly, W.B., Michalowsky, C.B. and Bohnert, H.J. 1995. A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7: 1129–1142.

    PubMed  Google Scholar 

  • Yamada, S., Nelson, D.E., Ley, E., Marquez, S. and Bohnert, H.J. 1997a. The expression of an aquaporin promoter from Mesembryanthemum crystallinumin tobacco. Plant Cell Physiol. 38: 1326–1332.

    PubMed  Google Scholar 

  • Yamada, S., Komori, T., Myers, P.N., Kuwata, S., Kubo, T. and Imaseki, H. 1997b. Expression of plasma membrane water channel genes under water stress in Nicotiana excelsior. Plant Cell Physiol. 38: 1226–1231.

    PubMed  Google Scholar 

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Malz, S., Sauter, M. Expression of two PIP genes in rapidly growing internodes of rice is not primarily controlled by meristem activity or cell expansion. Plant Mol Biol 40, 985–995 (1999). https://doi.org/10.1023/A:1006265528015

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