Abstract
The ubiquitous cell membrane proteins called aquaporins are now firmly established as channel proteins that control the specific transport of water molecules across cell membranes in all living organisms. The aquaporins are thus likely to be of fundamental significance to all facets of plant growth and development affected by plant–water relations. A majority of plant aquaporins have been found to share essential structural features with the human aquaporin and exhibit water-transporting ability in various functional assays, and some have been shown experimentally to be of critical importance to plant survival. Furthermore, substantial evidence is now available from a number of plant species that shows differential gene expression of aquaporins in response to abiotic stresses such as salinity, drought, or cold and clearly establishes the aquaporins as major players in the response of plants to conditions that affect water availability. This review summarizes the function and regulation of these genes to develop a greater understanding of the response of plants to water insufficiency, and particularly, to identify tolerant genotypes of major crop species including wheat and rice and plants that are important in agroforestry.
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References
Agre P, Kozono D (2003) Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 555:72–78
Agre P, Sasaki S, Chrispeels M (1993) Aquaporins: a family of water channel proteins. Am J Physiol 261:F461
Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels—from atomic structure to clinical medicine. J Physiol 542:3–16
Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484
Amodeo G, Dorr R, Vallejo A, Stuka M, Parisi M (1999) Radial and axial water transport in the sugar beet storage root. J Exp Bot 50:509–516
Aroca R, Amodeo G, Fernandez-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353
Azaizeh H, Gunse B, Steudle E (1992) Effects of NaCl and CaCl2 on water transport across root cells of maize (Zea mays L.) seedlings. Plant Physiol 99:886–894
Barkla BJ, Vera-Estrella R, Pantoja O, Kirch H-H, Bohnert HJ (1999) Aquaporin localization—how valid are the TIP and PIP labels? Trends Plant Sci 4:86–88
Barrieu F, Thomas D, Martymazars D, Charbonnier M, Marty F (1998) Tonoplast intrinsic proteins from cauliflower (Brassica oleracea L. var. botrytis): immunogold analysis, cDNA cloning and evidence for expression in merstematic tissues. Planta 204:335–344
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58
Beitz E, Wu B, Holm LM, Schultz JE, Zeuthen T (2006) Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proc Natl Acad Sci USA 103:269–274
Bernstein L (1975) Effects of salinity and sodicity on plant growth. Annu Rev Phytopathol 13:295–312
Beuron F, Cahérec FL, Guillam M-T, Cavalier A, Garret A, Tassan J-P, Delamarche C, Schultz P, Mallouh V, Rolland J-P, Hubert J-F, Gouranton J, Thomas D (1995) Structural analysis of a MIP family protein from the digestive tract of Cicadella viridis. J Biol Chem 270:17414–17422
Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805
Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J Biol Chem 270:29063–29066
Carbrey JM, Bonhivers M, Boeke JD, Agre P (2001) Aquaporins in Saccharomyces: characterization of a second functional water channel protein. Proc Natl Acad Sci USA 98:1000–1005
Chakrabarti N, Roux B, Pomes R (2004a) Structural determinants of proton blockage in aquaporins. J Mol Biol 343:493–510
Chakrabarti N, Tajkhorshid E, Roux B, Pomes R (2004b) Molecular basis of proton blockage in aquaporins. Structure 12:65–74
Chaumont F, Barrieu F, Herman EM, Chrispeels MJ (1998) Characterization of a maize tonoplast aquaporin expressed in zones of cell division and elongation. Plant Physiol 117:1143–1152
Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034
Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215
Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764
Chretien S, Cartron JP, de Figueiredo M (1999) A single mutation inside the NPA motif of aquaporin-1 found in a Colton-null phenotype. Blood 93:4021–4023
Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134
Daniels MJ, Mirkov TE, Chrispeels MJ (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 106:1325–1333
Daniels MJ, Chaumont F, Mirkov TE, Chrispeels MJ (1996) Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell 8:587–599
de Groot BL, Grubmuller H (2005) The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr Opin Struct Biol 15:176–183
de Groot BL, Frigato T, Helms V, Grubmuller H (2003) The mechanism of proton exclusion in the aquaporin-1 water channel. J Mol Biol 333:279–293
Deen PM, Verdijik MA, Knoers NV, Wieringa B, Monnens LA, van Os CH, van Oost BA (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 264:92–95
Denker BM, Smith BL, Kuhajda FP, Agre P (1988) Identification, purification and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem 263:15634–15642
Doering-Saad C, Newbury HJ, Bale JS, Pritchard J (2002) Use of aphid stylectomy and RT-PCR for the detection of transporter mRNAs in sieve elements. J Exp Bot 56:631–637
Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228
Finkelstein A (1987) Water movement through lipid bilayers, pores, and plasma membranes: theory and reality. In: Distinguished lecture series of the Society of General Physiologists, vol 4. Wiley, New York, pp 1–228
Fortin MG, Morrison NA, Verma DPS (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15:813–824
Fotiadis D, Jeno P, Mini T, Wirtz S, Muller S, Fraysse L, Kjellbom P, Engel A (2001) Structural characterisation of two aquaporins isolated from native spinach leaf plasma membranes. J Biol Chem 276:1707–1714
Fu D, Libson A, Miercke LJW, Weitzman C, Nollert P, Krucinski J, Stroud RM (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–486
Gao Y-P, Young L, Bonham-Smith P, Gusta LV (1999) Characterization and expression of plasma and tonoplast membrane aquaporins in primed seed of Brassica napus during germination under stress conditions. Plant Mol Biol 40:635–644
Gaspar M, Bousser A, Sissoëff I, Roche O, Hoarau J, Mahé A (2003) Cloning and characterization of ZmPIP1-5b, an aquaporin transporting water and urea. Plant Sci 165:21–31
Gerbeau P, Güçlü J, Pierre R, Maurel C (1999) Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J 18:577–587
Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma membrane intrinsic protein gene family. Cell Res 16:277–286
Gustavsson S, Lebrun A-S, Norden K, Chaumont F, Johanson U (2005) A novel plant major intrinsic protein in Physcomitrella patens most similar to bacterial glycerol channels. Plant Physiol 139:287–295
Guttman JA, Samji FN, Li Y, Deng W, Lin A, Finlay BB (2007) Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol 9:131–141
Haines TH (1994) Water transport across biological membranes. FEBS Lett 346:115–122
Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529
Harries WEC, Akhavan D, Miercke LJW, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-Å resolution. Proc Natl Acad Sci USA 101:14045–14050
Hedfalk K, Tornroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, Neutze R (2006) Aquaporin gating. Curr Opin Struct Biol 16:447–456
Higuchi T, Suga S, Tsuchiya T, Hisada H, Morishima S, Okada Y, Maeshima M (1998) Molecular cloning, water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin. Plant Cell Physiol 39:905–913
Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM, Chrispeels MJ (1992) Vegetative and seed-specific forms of tonoplast intrinsic proteins in the vacuolar membrane of Arabidopsis thaliana. Plant Physiol 99:561–570
Hollenbach B, Dietz KJ (1995) Molecular-cloning of EMIP, a member of the major intrinsic protein (MIP) gene family, preferentially expressed in epidermal cells of barley leaves. Botanica Acta 108:425–431
Houde M, Belcaid M, Ouellet F, Danyluk J, Monroy AF, Dryanova A, Gulick P, Bergeron A, Laroche A, Links MG, MacCarthy L, Crosby WL, Sarhan F (2006) Wheat EST resources for functional genomics of abiotic stress. BMC Genomics 7:149
Hu J, Verkman AS (2006) Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. FASEB J 20:1892–1894
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
Inoue K, Takeuchi Y, Nishimura M, Hara-Nishimura I (1995) Characterization of two integral membrane proteins located in the protein bodies of pumpkin seeds. Plant Mol Biol 28:1089–1101
Ishibashi K (2006) Aquaporin subfamily with unusual NPA boxes. Biochim Biophys Acta 1758:989–993
Ishibashi K, Kuwahara M, Kageyama Y, Sasaki S, Suzuki M, Imai M (2000) Molecular cloning of a new aquaporin superfamily in mammals: AQPX1 and AQPX2. In: Hohmann S, Nielsen S (eds) Molecular biology and physiology of water and solute transport. Kluwer/Plenum, New York, pp 123–126
Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820
Jahn TP, Møller ALB, Zeuthen T, Holm LM, Klærke DA, Mohsin B, Kühlbrandt W, Schjoerring JK (2004) Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett 574:31–36
Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725
Jauh GY, Phillips TE, Rogers JC (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11:1867–1882
Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Güçlü J, Vinh J, Heyes J, Franch KI, Schäffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369
Johansson I, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181–1191
Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459
Johansson I, Karlsson M, Johanson U, Larsson C, Kjellbom P (2000) The role of aquaporins in cellular and whole plant water balance. Biochim Biophys Acta 1465:324–342
Johnson KD, Herman EM, Chrispeels MJ (1989) An abundant, highly conserved tonoplast protein in seeds. Plant Physiol 91:1006–1013
Jung JS, Preston GM, Smith BL, Guggino WB, Agre P (1994) Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem 269:14648–14654
Kaldenhoff R, Fischer M (2006) Functional aquaporin diversity in plants. Biochim Biophys Acta 1758:1134–1141
Kaldenhoff R, Grote K, Zhu J-J, Zimmerman U (1998) Significance of plasmalemma aquaporins for water transport in Arabidopsis thaliana. Plant J 14:121–128
Kaldenhoff R, Kölling A, Meyers J, Karmann U, Ruppel G, Richter G (1995) 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 7:87–95
Kammerloher W, Fischer U, Piechottka GP, Schäffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199
Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893
Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K (2003) Over-expression of a barley aquaporin increased the shoot/root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiol 44:1378–1383
Kawasaki S, Borchert C, Deyholes M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905
Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205
King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698
Kirch H-H, Vera-Estrella R, Golldack D, Quigley F, Michalowski CB, Barkla BJ, Bohnert HJ (2000) Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol 123:111–124
Kobae Y, Mizutani M, Segami S, Maeshima M (2006) Immunochemical analysis of aquaporin isoforms in Arabidopsis suspension-cultured cells. Biosci Biotechnol Biochem 70:980–987
Kong Y, Ma J (2001) Dynamic mechanisms of the membrane water channel aquaporin-1 (AQP1). Proc Natl Acad Sci USA 98:14345–14349
Kozono D, Ding XD, Iwasaki I, Meng XY, Kamagata Y, Agre P, Kitagawa Y (2003) Functional expression and characterization of an archaeal aquaporin-AqpM from Methanothermobacter marburgensis. J Biol Chem 278:10649–10656
Ktitorova IN, Skobeleva OV, Sharova EI, Ermakov EI (2002) Hydrogen peroxide appears to mediate a decrease in hydraulic conductivity in wheat roots under salt stress. Russ J Plant Physiol 49:369–380
Li L, Li S, Tao Y, Kitagawa Y (2000) Molecular cloning of a novel water channel from rice: its products expression in Xenopus oocytes and involvement in chilling tolerance. Plant Sci 154:43–51
Lian H-L, Yu X, Ye Q, Ding X, Kitagawa Y, Kwak S-S, Su W-A, Tang Z-C (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489
Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA (2006) Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 16:651–660
Liu Q, Umeda M, Uchimiya H (1994) Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol Biol 26:2003–2007
Liu L-H, Ludewig U, Gassert B, Frommer WB, von Wiren N (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol 133:1220–1228
Liu Y, Guo CA, Ren HB, Chen F (2004) Isolation and characterization of a novel cis-acting sequences regulating root-specific gene from Daucus carota L. Chinese Sci Bull 49:2393–2398
Lopez F, Bousser A, Sissoeff I, Hoarau J, Mahe A (2004) Characterization in maize of ZmTIP2-3, a root-specific tonoplast intrinsic protein exhibiting aquaporin activity. J Exp Bot 55:539–541
Loque D, Ludewig U, Yuan LX, von Wiren N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 132:671–680
Lu D, Grayson P, Schulten K (2003) Glycerol conductance and physical asymmetry of the Escherichia coli glycerol facilitator GlpF. Biophys J 85:2977–2987
Ludevid D, Höfte H, Himelblau E, Chrispeels MJ (1992) The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639
Luu D-T, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96
Ma S, Quist TM, Ulanov A, Joly R, Bohnert HJ (2004) Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. Plant J 40:845–859
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691
Macey RI (1984) Transport of water and urea in red blood cells. Am J Physiol 246:C195–C203
Maeshima M, Mimura T, Sato T (1994) Distribution of vacuolar H+-pyrophosphatase and a membrane integral protein in a variety of green plants. Plant Cell Physiol 35:323–328
Malz S, Sauter M (1999) 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
Martre P, Morillon R, Barrieu F, North GB, S. NP, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110
Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol 48:399–429
Maurel C, Reizer JU, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein γ-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–3347
Maurel C, Kado RT, Guern J, Chrispeels MJ (1995) Phosphorylation regulates the water channel activity of the seed-specific aquaporin alpha-TIP. EMBO J 14:3028–3035
Maurel C, Chrispeels MJ, Lurin C, Tacnet F, Geelen D, Ripoche P, Guern J (1997a) Function and regulation of seed aquaporins. J Exp Bot 48:421–430
Maurel C, Tacnet F, Guclu J, Guern J, Ripoche P (1997b) 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
Maurel C, Javot H, Lauvergeat V, Gerbeau P, Tournaire C, Santoni V, Heyes J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215:105–148
Meristem Land & Science (2002) ‘Aquaporin’ genes hold key to sprouting-resistant cereal crops. Meristem Information Resources Ltd. October 25, 2002. Cited October 6 2004. http://www.meristem.com/wheat/ws02_08.html
Mitra BN, Yoshino R, Morio T, Yokoyama M, Maeda M, Urushihara H, Tanaka Y (2000) Loss of a member of the aquaporin gene family, aqpA affects spore dormancy in Dictyostelium. Gene 27:131–139
Morillon R, Lassalles J-P (2002) Water deficit during root development: effects on the growth of roots and osmotic water permeability of isolated root protoplasts. Planta 214:392–399
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605
Niemietz CM, Tyerman SD (1997) Characterization of water channels in wheat root membrane vesicles. Plant Physiol 115:561–567
Niemietz CM, Tyerman SD (2000) Channel-mediated permeation of ammonia gas through the peribacteroid membrane of soybean nodules. FEBS Lett 465:110–114
Ohshima Y, Iwasaki I, Suga S, Murkamami M, Inoue K, Maeshima M (2001) Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a CAM plant Graptopetalum paraguayense: comparison with radish. Plant Cell Physiol 42:1119–1129
Oono Y, Seki M, Nanjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Iida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microarray. Plant J 34:868–887
Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K (2006) Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics 6:212–234
Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387
Preston GM, Jung JS, Guggino WB, Agre P (1993) The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem 268:17–20
Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2001) From genome to function: the Arabidopsis aquaporins. Genome Biol 3:research0001.1–research0001.17
Reizer J, Reizer A, Saier MHJ (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
Rivers RL, Dean RM, Chandy G, Hall JE, Roberts DM, Zeidel ML (1997) Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J Biol Chem 272:16256–16261
Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696
Robinson DG, Sieber H, Kammerloher W, Schäffner AR (1996) PIP1 aquaporins are concentrated in plasmalemmasomes of Arabidopsis thaliana mesophyll. Plant Physiol 11:645–649
Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792
Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct Integr Genomics 6:263–284
Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577
Sarda X, Tousch D, Ferrare K, Legrand E, Dupuis JM, Casse-Delbart F, Lamaze T (1997) Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J 12:1103–1111
Savage DF, Egea PF, Robles-Colmenares Y, O’Connell JD, Stroud RM (2003) Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of Aquaporin Z. PLoS Biol 1:334–340
Schunmann PH, Ougham HJ (1996) Identification of three cDNA clones expressed in the leaf extension zone and with altered patterns of expression in the slender mutant of barley: a tonoplast intrinsic protein, a putative structural protein and protochlorophyllide oxidoreductase. Plant Mol Biol 31:529–537
Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915
Siefritz F, Otto B, Bienert GP, van der Krol A, Kaldenhoff R (2004) The plasma membrane aquaporin NtAQP1 is a key component of the leaf unfolding mechanism in tobacco. Plant J 37:147–155
Smith BL, Agre P (1991) Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J Biol Chem 266:6407–6415
Smith-Espinoza CJ, Richter A, Salamini F, Bartels D (2003) Dissecting the response to dehydration and salt (NaCl) in the resurrection plant Craterostigma plantagineum. Plant Cell Environ 26:1307–1315
Sui H, Han B-G, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878
Tajkhorshid E, Nollert P, Jensen MO, Miercke LJW, O’Connell J, Stroud RM, Schulten K (2002) Control of the selectivity of the aquaporin water channel family by global orientational tuning. Science 296:525–530
Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83
Thomas D, Bron P, Ranchy G, Duchesne L, Cavalier A, Rolland J-P, Raguenes-Nicol C, Hubert J-F, Haase W, Delamarche C (2002) Aquaglyceroporins, one channel for two molecules. Biochim Biophys Acta-Bioenergetics 1555:181–186
Tyerman S, Bohnert H, Maurel C, Steudle E, Smith J (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 50:1055–1071
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737
van Hoek AN, Hom ML, Luthjens LH, de Jong MD, Dempster JA, van Os CH (1991) Functional unit of 30 kDa for proximal tubule water channels as revealed by radiation inactivation. J Biol Chem 266:16633–16635
Vander Willigen C, Pammenter NW, Mundree SG, Farrant JM (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartmentalization of subcellular components and metabolites play a role? J Exp Bot 55:651–661
Vander Willigen C, Postaire O, Tournaire-Roux C, Boursiac Y, Maurel C (2006) Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant Cell Physiol 47:1241–1250
Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135:2318–2329
Verbavatz JM, Brown D, Sabolic I, Valenti G, Ausiello DA, Van Hoek AN, Ma T, Verkman AS (1993) Tetrameric assembly of CHIP28 water channels in liposomes and cell membranes: a freeze-fracture study. J Cell Biol 123:605–618
Verkman AS (2000) Water permeability measurement in living cells and complex tissues. J Membr Biol 173:73–87
Veselova TV, Veselovskii VA, Usmanov PD, Usmanova OV, Kozar VI (2003) Hypoxia and imbibition injuries to aging seeds. Russ J Plant Physiol 50:835–842
Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068
Wallace IS, Roberts DM (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44:16826–16834
Wallace IS, Wills DM, Guenther JF, Roberts DM (2002) Functional selectivity for glycerol of the nodulin 26 subfamily of plant membrane intrinsic proteins. FEBS Lett 523:109–112
Walz T, Typke D, Smith BL, Agre P, Engel A (1995) Projection map of aquaporin-1 determined by electron crystallography. Nat Struct Biol 3:730–732
Wang Y, Schulten K, Tajkhorshid E (2005) What makes an aquaporin a glycerol channel? A comparative study of AqpZ and GlpF. Structure 13:1107–1118
Yamada S, Bohnert HJ (2000) Expression of the PIP aquaporin promoter-MipA from the common ice plant in tobacco. Plant Cell Physiol 41:719–725
Yamada S, Katsuhara M, Kelly WB, Michalowski CB, Bohnert HJ (1995) A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7:1129–1142
Yamada C, Nelson D, Ley E, Marquez S, Bohnert HJ (1997) The expression of an aquaporin promoter from Mesembryanthemum crystallinum in tobacco. Plant Cell Physiol 38:1326–1332
Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K (1992) Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 33:217–224
Yamamoto YT, Taylor CG, Acedo GH, Cheng C-L, Conkling MA (1991) Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell 3:371–382
Yu QJ, Hu YL, Li JF, Wu Q, Lin ZP (2005) Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. Plant Sci 169:647–656
Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16:599–608
Zardoya R (2005) Phylogeny and evolution of the major intrinsic protein family. Biol Cell 97:397–414
Zardoya R, Villalba S (2001) A phylogenetic framework for the Aquaporin family in eukaryotes. J Mol Evol 52:391–404
Zeidel ML, Ambudkar SV, Smith BL, Agre P (1992) Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 31:7436–7440
Zeng H, Zhong Y, Luo L (2006) Drought tolerance genes in rice. Funct Integr Genomics 6:338–341
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298
Zhang W-H, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120:849–857
Zhang WH, Tyerman SD (1991) Effect of low O2 concentration and azide on hydraulic conductivity and osmotic volume of cortical cells of wheat roots. Aust J Plant Physiol 18:603–613
Zhang R, van Hoek AN, Biwersi J, Verkman AS (1993) A point mutation at cysteine-189 blocks the water permeability of rat kidney water channel CHIP28k. Biochemistry 32:2938–2941
Zhu C, Schraut D, Hartung W, Schaffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981
Acknowledgements
KF (nee’ Smith) thanks the Grains Research and Development Corporation, Australia (GRDC) for a Ph.D. scholarship. The authors gratefully acknowledge Prof. Rudi Appels for the critical editorial comments on the manuscript, which benefited its preparation significantly.
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Forrest, K.L., Bhave, M. Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct Integr Genomics 7, 263–289 (2007). https://doi.org/10.1007/s10142-007-0049-4
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DOI: https://doi.org/10.1007/s10142-007-0049-4