Abstract
The Arabidopsis thaliana Tonoplast Intrinsic Protein 1;1 (AtTIP1;1) is a member of the tonoplast aquaporin family. The tissue-specific expression pattern and intracellular localization of AtTIP1;1 were characterized using GUS and GFP fusion genes. Results indicate that AtTIP1;1 is expressed in almost all cell types with the notable exception of meristematic cells. The highest level of AtTIP1;1 expression was detected in vessel-flanking cells in vascular bundles. AtTIP1;1-GFP fusion protein labelled the tonoplast of the central vacuole and other smaller peripheral vacuoles. The fusion protein was not found evenly distributed along the tonoplast continuum but concentrated in contact zones of tonoplasts from adjacent vacuoles and in invaginations of the central vacuole. Such invaginations may result from partially engulfed small vacuoles. A knockout mutant was isolated and characterized to gain insight into AtTIP1;1 function. No phenotypic alteration was found under optimal growth conditions indicating that AtTIP1;1 function is not essential to the plant and that some members of the TIP family may act redundantly to facilitate water flow across the tonoplast. However, a conditional root phenotype was observed when mutant plants were grown on a glycerol-containing medium.
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Abbreviations
- AQP:
-
Aquaporin
- GFP:
-
Green fluorescent protein
- GUS:
-
β-Glucuronidase
- MIP:
-
Membrane intrinsic protein
- NIP:
-
Nodulin-like intrinsic protein
- PIP:
-
Plasma membrane intrinsic protein
- TIP:
-
Tonoplast intrinsic protein
References
Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon C, Guggino WB, Nielsen S (1993) Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol Renal Physiol 265:F463–F476
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. doi:10.1007/s11103-005-0352-1
An G, Costa MA, Mitra A, Ha S-B, Márton L (1988) Organ-specific and developmental regulation of the nopaline synthase promoter in transgenic tobacco plants. Plant Physiol 88:547–552
Aubert S, Gout E, Bligny R, Douce R (1994) Multiple effects of glycerol on plant cell metabolism. Phosphorus-31 nuclear magnetic resonance studies. J Biol Chem 269:21420–21427
Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133:1251–1263. doi:10.1083/jcb.133.6.1251
Barrieu F, Chaumont F, Chrispeels MJ (1998) High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant Physiol 117:1153–1163. doi:10.1104/pp.117.4.1153
Barrieu F, Marty-Mazars D, Thomas D, Chaumont F, Charbonnier M, Marty F (1999) Desiccation and osmotic stress increase the abundance of mRNA of the tonoplast aquaporin BobTIP26-1 in cauliflower cells. Planta 209:77–86. doi:10.1007/s004250050608
Bienert GP, Schüssler MD, Jahn TP (2008) Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci 33:20–26. doi:10.1016/j.tibs.2007.10.004
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. doi:10.1104/pp.105.065029
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x
Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38:366–379. doi:10.1111/j.1365-313X.2004.02051.x
Daniels MJ, Chrispeels MJ, Yeager M (1999) Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J Mol Biol 294:1337–1349. doi:10.1006/jmbi.1999.3293
Denecke J, De Rycke R, Botterman J (1992) Plant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope. EMBO J 11:2345–2355
Duckett CM, Oparka KJ, Prior DAM, Dolan L, Roberts K (1994) Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120:3247–3255
Eastmond PJ (2004) Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J 37:617–625. doi:10.1111/j.1365-313X.2003.01989.x
Epimashko S, Meckel T, Fischer-Schliebs E, Lüttge U, Thiel G (2004) Two functionally different vacuoles for static and dynamic purposes in one plant mesophyll leaf cell. Plant J 37:294–300
Escobar NM, Haupt S, Thow G, Boevink P, Chapman S, Oparka K (2003) High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523. doi:10.1105/tpc.013284
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. doi:10.1105/tpc.017194
Foresti O, daSilva LL, Denecke J (2006) Overexpression of the Arabidopsis syntaxin PEP12/SYP21 inhibits transport from the prevacuolar compartment to the lytic vacuole in vivo. Plant Cell 18:2275–2293. doi:10.1105/tpc.105.040279
Gerbeau P, Güçlü J, Ripoche P, 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. doi:10.1046/j.1365-313x.1999.00481.x
Gerber DW, Byerrum RU, Gee RW, Tolbert NE (1988) Glycerol concentrations in crop plants. Plant Sci 56:31–38. doi:10.1016/0168-9452(88)90182-3
Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429:193–197. doi:10.1038/nature02503
Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323. doi:10.1007/s11103-006-9022-1
Harvengt P, Vlerick A, Fuks B, Wattiez R, Ruysschaert JM, Homble F (2000) Lentil seed aquaporins form a hetero-oligomer which is phosphorylated by a Mg(2+)-dependent and Ca(2+)-regulated kinase. Biochem J 352:183–190. doi:10.1042/0264-6021:3520183
Hawes C, Saint-Jore CM, Brandizzi F, Zheng H, Andreeva AV, Boevink P (2001) Cytoplasmic illuminations: in planta targeting of fluorescent proteins to cellular organelles. Protoplasma 215:77–88. doi:10.1007/BF01280305
Hiroaki Y, Tani K, Kamegawa A, Gyobu N, Nishikawa K, Suzuki H, Walz T, Sasaki S, Mitsuoka K, Kimura K, Mizoguchi A, Fujiyoshi Y (2006) Implications of the aquaporin-4 structure on array formation and cell adhesion. J Mol Biol 355:628–639. doi:10.1016/j.jmb.2005.10.081
Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM, Chrispeels MJ (1992) Vegetative and seed-specific forms of tonoplast intrinsic protein in the vacuolar membrane of Arabidopsis thaliana. Plant Physiol 99:561–570
Huang CG, Lamitina T, Agre P, Strange K (2007) Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am J Physiol Cell Physiol 292:C1867–C1873. doi:10.1152/ajpcell.00514.2006
Hunter PR, Craddock CP, Di Benedetto S, Roberts LM, Frigerio L (2007) Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol 145:1371–1382. doi:10.1104/pp.107.103945
Jackson AL, Bartz SR, Schelter J, Kobayashi SV, Burchard J, Mao M, Li B, Cavet G, Linsley PS (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol 21:635–637. doi:10.1038/nbt831
Jauh GY, Fischer AM, Grimes HD, Ryan CA, Rogers JC (1998) delta-Tonoplast intrinsic protein defines unique plant vacuole functions. Proc Natl Acad Sci USA 95:12995–12999. doi:10.1073/pnas.95.22.12995
Jauh GY, Phillips TE, Rogers JC (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11:1867–1882. doi:10.1105/tpc.11.10.1867
Jiang L, Phillips TE, Rogers SW, Rogers JC (2000) Biogenesis of the protein storage vacuole crystalloid. J Cell Biol 150:755–770. doi:10.1083/jcb.150.4.755
Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall 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. doi:10.1104/pp.126.4.1358
Keijzer CJ, Hoek IHS, Willemse MTM (1987) The processes of anther dehiscence and pollen dispersal. 3. The dehydration of the filament tip and the anther in 3 monocotyledonous species. New Phytol 106:281–287. doi:10.1111/j.1469-8137.1987.tb00143.x
Leegood RC (1988) Phosphate sequestration by glycerol and its effects on photosynthetic carbon assimilation by leaves. Planta 176:117–126. doi:10.1007/BF00392487
Lin W, Peng Y, Li G, Arora R, Tang Z, Su W, Cai W (2007) Isolation and functional characterization of PgTIP1, a hormone-autotrophic cells-specific tonoplast aquaporin in ginseng. J Exp Bot 58:947–956. doi:10.1093/jxb/erl255
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Ludevid D, Höfte H, Himelblau E, Chrispeels MJ (1992) The expression pattern of the tonoplast intrinsic protein gamma-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639
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. doi:10.1111/j.1365-313X.2004.02265.x
Marty-Mazars D, Clemencet MC, Dozolme P, Marty F (1995) Antibodies to the tonoplast from the storage parenchyma cells of beetroot recognize a major intrinsic protein related to TIPs. Eur J Cell Biol 66:106–118
Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48:399–429. doi:10.1146/annurev.arplant.48.1.399
Maurel C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581:2227–2236. doi:10.1016/j.febslet.2007.03.021
Maurel C, Reizer J, Schroeder JI, Chrispeels MJ (1993) The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J 12:2241–2247
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. doi:10.1016/S0074-7696(02)15007-8
Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14:47–56. doi:10.1105/tpc.010216
Moriyasu Y, Hattori M, Jauh GY, Rogers JC (2003) Alpha tonoplast intrinsic protein is specifically associated with vacuole membrane involved in an autophagic process. Plant Cell Physiol 44:795–802. doi:10.1093/pcp/pcg100
Müller O, Sattler T, Flötenmeyer M, Schwarz H, Plattner H, Mayer A (2000) Autophagic tubes: vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. J Cell Biol 151:519–528. doi:10.1083/jcb.151.3.519
Neuhaus JM, Paris N (2006) Plant vacuoles: from biogenesis to function. In: Šamaj JBF, Menzel D (eds) Plant endocytosis. Springer Verlag, Berlin, pp 63–82
Neuhaus JM, Rogers JC (1998) Sorting of proteins to vacuoles in plant cells. Plant Mol Biol 38:127–144. doi:10.1023/A:1006032627036
Olbrich A, Hillmer S, Hinz G, Oliviusson P, Robinson DG (2007) Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles. Plant Physiol 145:1383–1394. doi:10.1104/pp.107.108985
Paris N, Stanley CM, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563–572. doi:10.1016/S0092-8674(00)81256-8
Peng Y, Lin W, Cai W, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729–740. doi:10.1007/s00425-007-0520-4
Reisen D, Leborgne-Castel N, Özalp C, Chaumont F, Marty F (2003) Expression of a cauliflower tonoplast aquaporin tagged with GFP in tobacco suspension cells correlates with an increase in cell size. Plant Mol Biol 52:387–400. doi:10.1023/A:1023961332391
Reisen D, Marty F, Leborgne-Castel N (2005) New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol 5:13. doi:10.1186/1471-2229-5-13
Roberts IN, Oliver RP, Punt PJ, van den Hondel CA (1989) Expression of the Escherichia coli beta-glucuronidase gene in industrial and phytopathogenic filamentous fungi. Curr Genet 15:177–180. doi:10.1007/BF00435503
Saito C, Ueda T, Abe H, Wada Y, Kuroiwa T, Hisada A, Furuya M, Nakano A (2002) A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J 29:245–255. doi:10.1046/j.0960-7412.2001.01189.x
Schäffner AR (1998) Aquaporin function, structure, and expression: are there more surprises to surface in water relations? Planta 204:131–139. doi:10.1007/s004250050239
Schüssler MD, Alexandersson E, Bienert GP, Kichey T, Laursen KH, Johanson U, Kjellbom P, Schjoerring JK, Jahn TP (2008) The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana. Plant J 56:756–767. doi:10.1111/j.1365-313X.2008.03632.x
Siefritz F, Biela A, Eckert M, Otto B, Uehlein N, Kaldenhoff R (2001) The tobacco plasma membrane aquaporin NtAQP1. J Exp Bot 52:1953–1957. doi:10.1093/jexbot/52.363.1953
Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542. doi:10.1093/jexbot/51.350.1531
Sussman MR, Amasino RM, Young JC, Krysan PJ, Austin-Phillips S (2000) The Arabidopsis knockout facility at the University of Wisconsin-Madison. Plant Physiol 124:1465–1467. doi:10.1104/pp.124.4.1465
Temmei Y, Uchida S, Hoshino D, Kanzawa N, Kuwahara M, Sasaki S, Tsuchiya T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579:4417–4422. doi:10.1016/j.febslet.2005.06.082
Tian GW, Mohanty A, Chary SN, Li S, Paap B, Drakakaki G, Kopec CD, Li J, Ehrhardt D, Jackson D, Rhee SY, Raikhel NV, Citovsky V (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol 135:25–38. doi:10.1104/pp.104.040139
Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JAC (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 50:1055–1071. doi:10.1093/jexbot/50.suppl_1.1055
Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194. doi:10.1046/j.0016-8025.2001.00791.x
Uemura T, Yoshimura SH, Takeyasu K, Sato MH (2002) Vacuolar membrane dynamics revealed by GFP-AtVam3 fusion protein. Genes Cells 7:743–753. doi:10.1046/j.1365-2443.2002.00550.x
van Bel AJE (1993) Strategies of phloem loading. Annu Rev Plant Physiol Plant Mol Biol 44:253–281. doi:10.1146/annurev.pp.44.060193.001345
van der Rest B, Boisson AM, Gout E, Bligny R, Douce R (2002) Glycerophosphocholine metabolism in higher plant cells. Evidence of a new glyceryl-phosphodiester phosphodiesterase. Plant Physiol 130:244–255. doi:10.1104/pp.003392
von Arnim AG, Deng XW, Stacey MG (1998) Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene 221:35–43. doi:10.1016/S0378-1119(98)00433-8
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. doi:10.1104/pp.103.033415
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. doi:10.1021/bi0511888
Weig AR, Jakob C (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett 481:293–298. doi:10.1016/S0014-5793(00)02027-5
Yano D, Sato M, Saito C, Sato MH, Morita MT, Tasaka M (2003) A SNARE complex containing SGR3/AtVAM3 and ZIG/VTI11 in gravity-sensing cells is important for Arabidopsis shoot gravitropism. Proc Natl Acad Sci USA 100:8589–8594. doi:10.1073/pnas.1430749100
Acknowledgments
Azeez Beebo gratefully acknowledges the support of a doctoral fellowship from the French Ministère des Affaires Etrangères et Européennes and the Institut Kurde de Paris. This work was also supported by grants from the French Ministère de l’Enseignement Supérieur et de la Recherche, INRA and CNRS. The authors thank the Arabidopsis Knockout Facility of the University of Wisconsin Biotech Center for providing the pools of T-DNA mutants. We are grateful to Dr. Jeannine Lherminier for her help with electron microscopy. We also wish to thank Dr. Vivienne Gianinazzi-Pearson for her helpful comments on the manuscript.
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Azeez Beebo and Dominique Thomas have contributed equally to this work.
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The Arabidopsis Genome Initiative locus identifier for the AtTIP1;1 (γ-TIP) gene is At2g36830.
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Movie 1
Motion of highly fluorescent vacuolar membranes in leaf epidermal cells (MPG 2741 kb)
Movie 2
Cytochalasin D-induced immobilization of highly fluorescent vacuolar membranes in leaf epidermal cells (MPG 1326 kb)
Movie 3
Constrained motion of nested vacuolar membranes in cortical parenchyma cells of stamen filament (MPG 425 kb)
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Beebo, A., Thomas, D., Der, C. et al. Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles. Plant Mol Biol 70, 193–209 (2009). https://doi.org/10.1007/s11103-009-9465-2
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DOI: https://doi.org/10.1007/s11103-009-9465-2