Grapevine aquaporins: Gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Leitão, Luís ^a,b   Prista, Catarina ^a   Moura, Teresa F ^c   Loureiro Dias, Maria C ^a   Soveral, Graça ^c,d  

^a INSTITUTO SUPERIOR DE AGRONOMIA   (Portugal)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^c UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^d RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AQUAPORIN; ASPARTIC ACID; HISTIDINE; MEMBRANE PROTEIN; TONOPLAST INTRINSIC PROTEIN; TONOPLAST INTRINSIC PROTEIN 2 1; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; TONOPLAST INTRINSIC PROTEIN, PLANT; VEGETABLE PROTEIN; WATER;

ACIDIFICATION; ARTICLE; CELL MEMBRANE; CELL PH; CULTIVAR; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE LOCATION; GRAPE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PLANT GENE; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; TONOPLAST; VVTNPIP1 1 GENE; VVTNPIP2 1 GENE; VVTNPIP2 2 GENE; WATER PERMEABILITY; WATER TRANSPORT; YEAST; DNA SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; PERMEABILITY; PH; VITIS;

VITIS; VITIS VINIFERA;

AQUAPORINS; BASE SEQUENCE; CYTOSOL; GREEN FLUORESCENT PROTEINS; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PERMEABILITY; PLANT PROTEINS; SEQUENCE ANALYSIS, DNA; VITIS; WATER; YEASTS;

EID: 84858063921     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033219     Document Type: Article

References (60)

1. Tyerman SD, Niemietz CM, Bramley H, (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25: 173-194.
2. Fouquet R, Leon C, Ollat N, Barrieu F, (2008) Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Rep 27: 1541-1550.
3. Danielson JA, Johanson U, (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8: 45.
4. Maeshima M, Ishikawa F, (2008) ER membrane aquaporins in plants. Pflugers Arch 456: 709-716.
5. Chaumont F, Moshelion M, Daniels MJ, (2005) Regulation of plant aquaporin activity. Biol Cell 97: 749-764.
6. Ye Q, Wiera B, Steudle E, (2004) A cohesion/tension mechanism explains the gating of water channels (aquaporins) in Chara internodes by high concentration. J Exp Bot 55: 449-461.
7. Wan X, Steudle E, Hartung W, (2004) Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J Exp Bot 55: 411-422.
8. Soveral G, Macey RI, Moura TF, (1997) Membrane stress causes inhibition of water channels in brush border membrane vesicles from kidney proximal tubule. Biol Cell 89: 275-282.
9. Soveral G, Madeira A, Loureiro-Dias MC, Moura TF, (2008) Membrane tension regulates water transport in yeast. Biochim Biophys Acta 1778: 2573-2579.
10. Gerbeau P, Amodeo G, Henzler T, Santoni V, Ripoche P, et al. (2002) The water permeability of Arabidopsis plasma membrane is regulated by divalent cations and pH. Plant J 30: 71-81.
11. Alleva K, Niemietz CM, Sutka M, Maurel C, Parisi M, et al. (2006) Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. J Exp Bot 57: 609-621.
12. 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.
13. Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, et al. (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10: 451-459.
14. Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, et al. (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425: 393-397.
15. Tornroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, et al. (2006) Structural mechanism of plant aquaporin gating. Nature 439: 688-694.
16. Vera-Estrella R, Barkla BJ, Bohnert HJ, Pantoja O, (2004) Novel regulation of aquaporins during osmotic stress. Plant Physiol 135: 2318-2329.
17. Santoni V, Verdoucq L, Sommerer N, Vinh J, Pflieger D, et al. (2006) Methylation of aquaporins in plant plasma membrane. Biochem J 400: 189-197.
18. 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.
19. Lee SH, Singh AP, Chung GC, (2004) Rapid accumulation of hydrogen peroxide in cucumber roots due to exposure to low temperature appears to mediate decreases in water transport. J Exp Bot 55: 1733-1741.
20. Guo L, Wang ZY, Lin H, Cui WE, Chen J, et al. (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16: 277-286.
21. Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, et al. (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149: 445-460.
22. Troggio M, Vezzulli S, Pindo M, Malacarne G, Fontana P, et al. (2008) Beyond the genome, opportunities for a modern viticulture: A research overview. American Journal of Enology and Viticulture 59: 117-127.
23. Hayes MA, Davies C, Dry IB, (2007) Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential roles in sink and source tissues. J Exp Bot 58: 1985-1997.
24. Fischer M, Kaldenhoff R, (2008) On the pH regulation of plant aquaporins. J Biol Chem 283: 33889-33892.
25. Shelden MC, Howitt SM, Kaiser BN, Tyerman SD, (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct Plant Biol 36: 1065-1078.
26. Baiges I, Schaffner AR, Mas A, (2001) Eight cDNA encoding putative aquaporins in Vitis hybrid Richter-110 and their differential expression. J Exp Bot 52: 1949-1951.
27. Galmes J, Pou A, Alsina MM, Tomas M, Medrano H, et al. (2007) Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta 226: 671-681.
28. Suga S, Maeshima M, (2004) Water channel activity of radish plasma membrane aquaporins heterologously expressed in yeast and their modification by site-directed mutagenesis. Plant Cell Physiol 45: 823-830.
29. Soveral G, Madeira A, Loureiro-Dias MC, Moura TF, (2007) Water transport in intact yeast cells as assessed by fluorescence self-quenching. Appl Environ Microbiol 73: 2341-2343.
30. Preston GM, Jung JS, Guggino WB, Agre P, (1994) Membrane topology of aquaporin CHIP. Analysis of functional epitope-scanning mutants by vectorial proteolysis. J Biol Chem 269: 1668-1673.
31. Hove RM, Bhave M, (2011) Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol Biol 75: 413-430.
32. Bonhivers M, Carbrey JM, Gould SJ, Agre P, (1998) Aquaporins in Saccharomyces. Genetic and functional distinctions between laboratory and wild-type strains. J Biol Chem 273: 27565-27572.
33. Zelenina M, Bondar AA, Zelenin S, Aperia A, (2003) Nickel and extracellular acidification inhibit the water permeability of human aquaporin-3 in lung epithelial cells. J Biol Chem 278: 30037-30043.
34. Zhang WH, Tyerman SD, (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120: 849-858.
35. Hedfalk K, Tornroth-Horsefield S, Nyblom M, Johanson U, Kjellbom P, et al. (2006) Aquaporin gating. Curr Opin Struct Biol 16: 447-456.
36. Bellati J, Alleva K, Soto G, Vitali V, Jozefkowicz C, et al. (2010) Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol Biol 74: 105-118.
37. Soveral G, Prista C, Moura TF, Loureiro-Dias MC, (2010) Yeast water channels: an overview of orthodox aquaporins. Biol Cell 103: 35-54.
38. Leao C, Van Uden N, (1984) Effects of ethanol and other alkanols on passive proton influx in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 774: 43-48.
39. Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, et al. (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci U S A 104: 12359-12364.
40. Sutka M, Alleva K, Parisi M, Amodeo G, (2005) Tonoplast vesicles of Beta vulgaris storage root show functional aquaporins regulated by protons. Biol Cell 97: 837-846.
41. Soto G, Fox R, Ayub N, Alleva K, Guaimas F, et al. (2010) TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J 64: 1038-1047.
42. Kaldenhoff R, Ribas-Carbo M, Sans JF, Lovisolo C, Heckwolf M, et al. (2008) Aquaporins and plant water balance. Plant Cell Environ 31: 658-666.
43. Jackson PA, Galinha CI, Pereira CS, Fortunato A, Soares NC, et al. (2001) Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalyzed by a 40-kilodalton peroxidase. Plant Physiol 127: 1065-1076.
44. Murashige F, Skoog F, (1962) A revised medium for rapid growth and bioassays with tobacco tissue. Physiol Plant 15: 493-497.
45. Hanahan D, (1985) Techniques for transformation of Escherichia coli; In: Glover DM, editors. Oxford IRL Press.
46. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning: A Laboratory Manual NY Cold Spring Harbor.
47. Pronk JT, (2002) Auxotrophic yeast strains in fundamental and applied research. Appl Environ Microbiol 68: 2095-2100.
48. Geitz RD, Schiestl RH, (1995) Transforming Yeast with DNA pp. 255-269.
49. Birnboim HC, Doly J, (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7: 1513-1523.
50. Hoffman CS, Winston F, (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
51. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
52. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2010) GenBank. Nucleic Acids Res 38: D46-51.
53. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2011) GenBank. Nucleic Acids Res 39: D32-37.
54. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
55. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
56. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-469.
57. Breeuwer P, Abee T, (2000) Assessment of the intracellular pH of immobilized and continuously perfused yeast cells employing fluorescence ratio imaging analysis. J Microbiol Methods 39: 253-264.
58. van Heeswijk MP, van Os CH, (1986) Osmotic water permeabilities of brush border and basolateral membrane vesicles from rat renal cortex and small intestine. J Membr Biol 92: 183-193.
59. Henriques M, Quintas C, Loureiro-Dias MC, (1997) Extrusion of benzoic acid in Saccharomyces cerevisiae by an energy-dependent mechanism. Microbiology 143 (Pt 6): 1877-1883.
60. Pampulha ME, Loureiro-Dias MC, (1989) Combined effect of acetic acid, pH and ethanol on internal pH of fermenting yeast. Appl Microbiol Biot 31: 547-550.