Abstract
Despite the high isoform multiplicity of aquaporins in plants, with 35 homologues including 13 plasma membrane intrinsic proteins (PIPs) in Arabidosis thaliana, the individual and integrated functions of aquaporins under various physiological conditions remain unclear. To better understand aquaporin functions in plants under various stress conditions, we examined transgenic Arabidopsis and tobacco plants that constitutively overexpress Arabidopsis PIP1;4 or PIP2;5 under various abiotic stress conditions. No significant differences in growth rates and water transport were found between the transgenic and wild-type plants when grown under favorable growth conditions. The transgenic plants overexpressing PIP1;4 or PIP2;5 displayed a rapid water loss under dehydration stress, which resulted in retarded germination and seedling growth under drought stress. In contrast, the transgenic plants overexpressing PIP1;4 or PIP2;5 showed enhanced water flow and facilitated germination under cold stress. The expression of several PIPs was noticeably affected by the overexpression of PIP1;4 or PIP2;5 in Arabidopsis under dehydration stress, suggesting that the expression of one aquaporin isoform influences the expression levels of other aquaporins under stress conditions. Taken together, our results demonstrate that overexpression of an aquaporin affects the expression of endogenous aquaporin genes and thereby impacts on seed germination, seedling growth, and stress responses of the plants under various stress conditions.
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Abbreviations
- PIP:
-
Plasma membrane intrinsic protein
References
Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447
Alexandersson E, Fraysse L, Sjövall-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
Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266
Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434
Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptation to environmental stress. Plant Cell 7:1099–1111
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
Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitutes a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215
Comparot S, Morilon R, Badot PM (2000) Water permeability and revolving movement in Phaseolus vulgaris L. Plant Cell Physiol 41:114–118
Cooper AJ (1975) Crop production in recirculating nutrient solution. Sci Hort 3:251–258
Ding X, Iwasaki I, Kitagawa Y (2004) Overexpression of a lily PIP1 gene in tobacco increased the osmotic water permeability of leaf cells. Plant Cell Environ 27:177–186
Gallois P, Marinho P (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. Methods Mol Biol 49:39–48
Hachez C, Zelazny E, Chaumont F (2006) Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim Biophys Acta 1758:1142–1156
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, Thomas EP, 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, Franck 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, 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
Kaldenhoff R, Grote K, Zhu J-J, Zimmermann U (1998) Significance of plasmalemma aquaporins for water transport in Arabidopsis thaliana. Plant J 14:121–128
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
Kim JS, Kim YO, Ryu HJ, Kwak YS, Lee JY, Kang H (2003) Isolation of stress-related genes of rubber particles and latex in fig tree (Ficus carica) and their expressions by abiotic stress or plant hormone treatments. Plant Cell Physiol 44:412–419
Lee SH, Chung GC, Steudle E (2005a) Gating of aquaporins by low temperature in roots of chilling-sensitive cucumber and -tolerant figleaf gourd. J Exp Bot 56:985–995
Lee SH, Chung GC, Steudle E (2005b) Low temperature and mechanical stress differently gate aquaporins of root cortical cells of chilling-sensitive cucumber and -resistant figleaf gourd. Plant Cell Environ 28:1191–1202
Lian HL, Yu X, Ye Q, Ding X, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489
Mariaux JB, Bockel C, Salamini F, Bartels D (1998) Desiccation- and abscisic acid-responsive genes encoding major intrinsic proteins (MIPs) from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 38:1089–1099
Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110
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
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497
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
Ohshima Y, Iwasaki I, Suga S, Murakami M, Inoue K, Maeshima M (2001) Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a CAM plants Graptopetalum paraguayense: Comparison with radish. Plant Cell Physiol 42:1119–1129
Öquist G, Wass R (1988) A portable, microprocessor operated instrument for measuring chlorophyll fluorescence kinetic in stress philology. Physiol Plant 73:211–217
Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2001) From genome to function: the Arabidopsis aquaporins. Genome Biol 3:1–17
Sakr S, Alves G, Morillon R, Maurel K, Decourteix M, Guilliot A, Fleurat-Lessard P, Julien J-L, Chrispeels MJ (2003) Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiol 133:630–641
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
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Shulze ED, Hall AE, Landge OL, Walz H (1982) A portable steady state porometer for measuring the carbon dioxide and water vapour exchanges of leaves under natural conditions. Oecologia 53:141–145
Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876
Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693
Steudle E, Peterson CA (1998) How does water get through roots?. J Ex Bo 49:775–788
Suga S, Komatsu S, Maeshima M (2002) Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol 43:1229–1237
Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu D-T, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Yu Q, Hu Y, Li J, Wu Q, Lin Z (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
Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981
Acknowledgements
We thank Dr. M. Maeshima for anti-PAQs antibody. This work was supported by the SRC program of MOST/KOSEF (R11-2001-092-04002-0) to the Agricultural Plant Stress Research Center of Chonnam National University.
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Jang, J.Y., Lee, S.H., Rhee, J.Y. et al. Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64, 621–632 (2007). https://doi.org/10.1007/s11103-007-9181-8
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DOI: https://doi.org/10.1007/s11103-007-9181-8