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Plant Cell. Aug 1995; 7(8): 1129–1142.
PMCID: PMC160939

A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant.

Abstract

Seawater-strength salt stress of the ice plant (Mesembryanthemum crystallinum) initially results in wilting, but full turgor is restored within approximately 2 days. We are interested in a mechanistic explanation for this behavior and, as a requisite for in-depth biochemical studies, have begun to analyze gene expression changes in roots coincident with the onset of stress. cDNAs that suggested changes in mRNA amount under stress were found; their deduced amino acid sequences share homologies with proteins of the Mip (major intrinsic protein) gene family and potentially encode aquaporins. One transcript, MipB, was found only in root RNA, whereas two other transcripts, MipA and MipC, were detected in roots and leaves. Transcript levels of MipB were of low abundance. All transcripts declined initially during salt stress but later recovered to at least prestress level. The most drastic decline was in MipA and MipC transcripts. MipA mRNA distribution in roots detected by in situ hybridization indicated that the transcript was present in all cells in the root tip. In the expansion zone of the root where vascular bundles differentiate, MipA transcript amounts were most abundant in the endodermis. In older roots, which had undergone secondary growth, MipA was highly expressed in cell layers surrounding individual xylem strands. MipA was also localized in leaf vascular tissue and, in lower amounts, in mesophyll cells. Transcripts for MipB seemed to be present exclusively in the tip of the root, in a zone before and possibly coincident with the development of a vascular system. MipA- and MipB-encoded proteins expressed in Xenopus oocytes led to increased water permeability. mRNA fluctuations of the most highly expressed MipA and MipC coincided with turgor changes in leaves under stress. As the leaves regained turgor, transcript levels of these water channel proteins increased.

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Selected References

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  • Chrispeels MJ, Agre P. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci. 1994 Oct;19(10):421–425. [PubMed]
  • Clark AM, Verbeke JA, Bohnert HJ. Epidermis-specific gene expression in Pachyphytum. Plant Cell. 1992 Oct;4(10):1189–1198. [PMC free article] [PubMed]
  • Daniels MJ, Mirkov TE, Chrispeels MJ. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol. 1994 Dec;106(4):1325–1333. [PMC free article] [PubMed]
  • Deen PM, Verdijk MA, Knoers NV, Wieringa B, Monnens LA, van Os CH, van Oost BA. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science. 1994 Apr 1;264(5155):92–95. [PubMed]
  • De Rocher EJ, Harkins KR, Galbraith DW, Bohnert HJ. Developmentally regulated systemic endopolyploid in succulents with small genomes. Science. 1990 Oct 5;250(4977):99–101. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Fray RG, Wallace A, Grierson D, Lycett GW. 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. 1994 Feb;24(3):539–543. [PubMed]
  • Fushimi K, Uchida S, Hara Y, Hirata Y, Marumo F, Sasaki S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature. 1993 Feb 11;361(6412):549–552. [PubMed]
  • Gorin MB, Yancey SB, Cline J, Revel JP, Horwitz J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell. 1984 Nov;39(1):49–59. [PubMed]
  • Guerrero FD, Jones JT, Mullet JE. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol. 1990 Jul;15(1):11–26. [PubMed]
  • Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM, Chrispeels MJ. Vegetative and Seed-Specific Forms of Tonoplast Intrinsic Protein in the Vacuolar Membrane of Arabidopsis thaliana. Plant Physiol. 1992 Jun;99(2):561–570. [PMC free article] [PubMed]
  • Kaldenhoff R, Kölling A, Meyers J, Karmann U, Ruppel G, Richter G. The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. Plant J. 1995 Jan;7(1):87–95. [PubMed]
  • Maurel C, Reizer J, Schroeder JI, Chrispeels MJ. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J. 1993 Jun;12(6):2241–2247. [PMC free article] [PubMed]
  • Meyer G, Schmitt JM, Bohnert HJ. Direct screening of a small genome: estimation of the magnitude of plant gene expression changes during adaptation to high salt. Mol Gen Genet. 1990 Dec;224(3):347–356. [PubMed]
  • Miao GH, Hong Z, Verma DP. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. J Cell Biol. 1992 Jul;118(2):481–490. [PMC free article] [PubMed]
  • Ostrem JA, Olson SW, Schmitt JM, Bohnert HJ. Salt Stress Increases the Level of Translatable mRNA for Phosphoenolpyruvate Carboxylase in Mesembryanthemum crystallinum. Plant Physiol. 1987 Aug;84(4):1270–1275. [PMC free article] [PubMed]
  • Pao GM, Wu LF, Johnson KD, Höfte H, Chrispeels MJ, Sweet G, Sandal NN, Saier MH., Jr Evolution of the MIP family of integral membrane transport proteins. Mol Microbiol. 1991 Jan;5(1):33–37. [PubMed]
  • Preston GM, Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11110–11114. [PMC free article] [PubMed]
  • Preston GM, Carroll TP, Guggino WB, Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 1992 Apr 17;256(5055):385–387. [PubMed]
  • Rao Y, Jan LY, Jan YN. Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature. 1990 May 10;345(6271):163–167. [PubMed]
  • Reizer J, Reizer A, Saier MH., Jr 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. 1993;28(3):235–257. [PubMed]
  • Saier MH., Jr Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev. 1994 Mar;58(1):71–93. [PMC free article] [PubMed]
  • Tarczynski MC, Jensen RG, Bohnert HJ. Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science. 1993 Jan 22;259(5094):508–510. [PubMed]
  • Van Aelst L, Hohmann S, Zimmermann FK, Jans AW, Thevelein JM. A yeast homologue of the bovine lens fibre MIP gene family complements the growth defect of a Saccharomyces cerevisiae mutant on fermentable sugars but not its defect in glucose-induced RAS-mediated cAMP signalling. EMBO J. 1991 Aug;10(8):2095–2104. [PMC free article] [PubMed]
  • Vernon DM, Bohnert HJ. A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. EMBO J. 1992 Jun;11(6):2077–2085. [PMC free article] [PubMed]
  • Yamamoto YT, Taylor CG, Acedo GN, Cheng CL, Conkling MA. Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell. 1991 Apr;3(4):371–382. [PMC free article] [PubMed]
  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. Living with water stress: evolution of osmolyte systems. Science. 1982 Sep 24;217(4566):1214–1222. [PubMed]
  • Zeuthen T, Stein WD. Cotransport of salt and water in membrane proteins: membrane proteins as osmotic engines. J Membr Biol. 1994 Feb;137(3):179–195. [PubMed]
  • Zhang R, Skach W, Hasegawa H, van Hoek AN, Verkman AS. Cloning, functional analysis and cell localization of a kidney proximal tubule water transporter homologous to CHIP28. J Cell Biol. 1993 Jan;120(2):359–369. [PMC free article] [PubMed]

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