Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility

Plant Journal

Volumn 39, Issue 2, 2004, Pages 219-236

  Klein, Markus ^a   Geisler, Markus ^a   Su, Jeoung Suh ^a   Kolukisaoglu, H Üner ^b   Azevedo, Louis ^a   Plaza, Sonia ^a   Curtis, Mark D ^a   Richter, Andreas ^c   Weder, Barbara ^a   Schulz, Burkhard ^d   Martinoia, Enrico ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF ROSTOCK   (Germany)

^c UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

ATP binding cassette (ABC) transporter; Drought susceptibility; Guard cell; Multidrug resistance; Stomata

Indexed keywords

CELL MEMBRANES; CYTOLOGY; DETOXIFICATION; ELECTRIC CONDUCTIVITY; PROTEINS;

ATP BINDING CASSETTES (ABC); PLASMA MEMBRANES;

PLANTS (BOTANY);

CARBON DIOXIDE; METHOTREXATE; MULTIDRUG RESISTANCE PROTEIN;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; DISASTER; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; KINETICS; LIGHT; METABOLISM; MUTATION; PROTEIN TRANSPORT; REPORTER GENE; STROMA CELL; SWEATING;

ARABIDOPSIS; CARBON DIOXIDE; CELL MEMBRANE; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, REPORTER; KINETICS; LIGHT; METHOTREXATE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTATION; NATURAL DISASTERS; PLANT TRANSPIRATION; PROTEIN TRANSPORT; STROMAL CELLS;

ANIMALIA; ARABIDOPSIS; MAMMALIA;

EID: 3242697184     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02125.x     Document Type: Article

References (65)

1. Allaway, W.G. (1973) Accumulation of malate in guard cells of Vicia faba during stomatal opening. Planta, 110, 63-70.
2. Anderson, M.P., Gregory, R.J., Thompson, S., Souza, D.W., Paul, S., Mulligan, R.C., Smith, A.E. and Welsh, M.J. (1991) Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science, 253, 202-205.
3. Bauer, J., Hiltbrunner, A., Weibel, P., Vidi, P.A., Alvarez-Huerta, M., Smith, M.D., Schnell, D.J. and Kessler, F. (2002) Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. J. Cell. Biol. 159, 845-854.
4. Bauwe, H. and Kolukisaoglu, H.Ü. (2003) Genetic manipulation of glycine decarboxylation. J. Exp. Bot. 54, 1523-1535.
5. Bechthold, N., Ellis, J. and Pelletier, G. (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. 316, 1194-1199.
6. + channels. Biochim. Biophys. Acta, 1461, 285-303.
7. Chen, Z.S., Lee, K., Walther, S., Raftogianis, R.B., Kuwano, M., Zeng, H. and Kruh, G.D. (2002) Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res. 62, 3144-3150.
8. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. Cossins, E.A. (1987) Folate biochemistry and the metabolism of one-carbon units. In The Biochemistry of Plants, Vol. 11 (Davies, D.D., ed.). New York: Academic Press, pp. 317-353.
10. Curtis, M.D. and Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol., 133, 462-469.
11. + channel KCO1. Plant J. 29, 809-820.
12. Dean, M., Rzhetsky, A. and Allikmets, R. (2001) The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11, 1156-1166.
13. Farquhar, G.D., Ehleringer, J.R. and Hubick, K.T. (1989) Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503-537.
14. Forsthoefel, N.R., Wu, Y., Schulz, B., Bennett, M.J. and Feldmann, K.A. (1992) T-DNA insertion mutagenesis in Arabidopsis: prospects and perspectives. Aust. J. Plant Physiol. 19, 353-366.
15. Gaedeke, N., Klein, M., Kolukisaoglu, H.Ü. et al. (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J. 20, 1875-1887.
16. Geisler, M., Frangne, N., Gomès, E., Martinoia, E. and Palmgren, M.G. (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol. 124, 1814-1827.
17. Gottesman, M.M. and Pastan, I. (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62, 385-427.
18. Grabov, A. and Blatt, M. (1998) Co-ordination of signalling elements in guard cell ion channel control. J. Exp. Bot. 49, 351-360.
19. Hanson, A.D. and Gregory, J.F., III (2002) Synthesis and turnover of folates in plants. Curr. Opin. Plant Biol. 5, 244-249.
20. Henikoff, S., Greene, E.A., Pietrokovski, S., Bork, P., Attwood, T.K. and Hood, L. (1997) Gene families: the taxonomy of protein paralogs and chimeras. Science, 278, 609-614.
21. Higgins, C.F. (1992) ABC transporter: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113.
22. Higgins, C.F. (1995) The ABC of channel regulation. Cell, 82, 693-696.
23. Hosy, E., Vavasseur, A., Mouline, K. et al. (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc. Natl. Acad. Sci. USA, 100, 5549-5554.
24. Jabrin, S., Ravanel, S., Gambonnet, B., Douce, R. and Rebeille, F. (2003) One-carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development. Plant Physiol. 131, 1431-1439.
25. Jung, J.-Y., Kim, Y.-W., Kwak, J.M., Hwang, J.-U., Young, J., Schroeder, J.I., Hwang, I. and Lee, Y. (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell, 14, 2399-2412.
26. Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M. and Shimazaki, K.I. (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature, 414, 656-660.
27. Klein, M., Mamnun, Y.M., Eggmann, T., Schuller, C., Wolfger, H., Martinoia, E. and Kuchler, K. (2002) The ATP-binding cassette (ABC) transporter Bpt1p mediates vacuolar sequestration of glutathione conjugates in yeast. FEBS Lett. 520, 63-67.
28. Klein, M., Perfus-Barbeoch, L., Frelet, A., Gaedeke, N., Reinhardt, D., Mueller-Roeber, B., Martinoia, E. and Forestier, C. (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J. 33, 119-129.
29. Kolukisaoglu, H.Ü., Bovet, L., Klein, M., Eggmann, T., Geisler, M., Wanke, D., Martinoia, E. and Schulz, B. (2002) Family business: the multidrug-resistance related protein (MRP) ABC transporter genes in Arabidopsis thaliana. Planta, 216, 107-119.
30. König, J., Nies, A.T., Cui, Y., Leier, I. and Keppler, D. (1999) Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity and MRP2-mediated drug resistance. Biochim. Biophys. Acta, 1461, 377-394.
31. Leckie, C., McAinsh, M., Montgomery, L., Priestley, A., Staxen, I., Webb, A. and Hetherington, A. (1998) Abscisic acid induced stomatal closure mediated by cyclic ADP-ribose. J. Exp. Bot. 49, 339-349.
32. Leonhardt, N., Marin, E., Vavasseur, A. and Forestier, C. (1997) Evidence for the existence of a sulfonylurea-receptor-like protein in plants: modulation of stomatal movements and guard cell potassium channels by sulfonylureas and potassium channel openers. Proc. Natl. Acad. Sci. USA, 94, 14156-14161.
33. Leonhardt, N., Vavasseur, A. and Forestier, C. (1999) ATP binding cassette modulators control abscisic acid-regulated slow anion channels in guard cells. Plant Cell, 11, 1141-1151.
34. Liu, G., Sanchez-Fernandez, R., Li, Z.-S. and Rea, P.A. (2001) Enhanced multispecifity of Arabidopsis multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J. Biol. Chem. 267, 8648-8656.
35. Martienssen, R. (1998) Functional genomics: probing plant gene function and expression with transposons. Proc. Natl. Acad. Sci. USA, 95, 2021-2026.
36. Martinoia, E., Grill, E., Tommasini, R., Kreuz, K. and Amrheim, N. (1993) ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature, 364, 247-249.
37. Martinoia, E., Klein, M., Geisler, M., Sánchez-Fernández, R. and Rea, P.A. (2000) Vacuolar transport of secondary metabolites and xenobiotics. In Vacuolar Compartments. Annual Plant Reviews, Vol. 5 (Robinson, D.G. and Rogers, J.C., eds). Sheffield: Academic Press, pp. 221-253.
38. Martinoia, E., Klein, M., Geisler, M., Bovet, L., Forestier, C., Kolukisaoglu, H.U., Mueller-Roeber, B. and Schulz, B. (2002) Multifunctionality of plant ABC transporters: more than just detoxifiers. Planta, 214, 345-355.
39. McGuire, J.J. and Bertino, J.R. (1981) Enzymatic synthesis and function of folylpolyglutamates. Mol. Cell. Biochem. 38, 19-48.
40. Mustilli, A., Merlot, S., Vavasseur, A., Fenzi, F. and Giraudat, J. (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell, 14, 3089-3099.
41. Neuburger, M., Rébeillé, F., Jourdain, A., Nakamura, S. and Douce, R. (1996) Mitochondria are the major site for folate and thymidylate synthesis in plants. J. Biol. Chem. 271, 9466-9472.
42. Pei, Z.M., Kuchitsu, K., Ward, J.M., Schwarz, M. and Schroeder, J.I. (1997) Differential abscisic acid regulation of guard cell slow anion channel in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell, 9, 409-423.
43. Rashotte, A.M., DeLong, A. and Muday, G.K. (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell, 13, 1683-1697.
44. Ravanel, S., Cherest, H., Jabrin, S., Grunwald, D., Surdin-Kerjan, Y., Douce, R. and Rebeille, F. (2001) Tetrahydrofolate biosynthesis in plants: molecular and functional characterization of dihydrofolate synthetase and three isoforms of folylpolyglutamate synthetase in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA, 98, 15360-15365.
45. Rea, P.A., Sánchez-Fernández, R., Chen, S., Peng, M., Klein, M., Geisler, M. and Martinoia, E. (2003) The plant ABC transporter superfamily: the functions of a few and identities of many. In ABC Proteins - from Bacteria to Man (Holland, I.B., Cole, S.P.C., Kuchler, K. and Higgins, C.F. eds). New York: Academic Press, pp. 335-355.
46. Sanchez-Fernandez, R., Ardiles-Diaz, W., Van Montagu, M., Inze, D. and May, M.J. (1998) Cloning and expression analyses of AtMRP4, a novel MRP-like gene from Arabidopsis thaliana. Mol. Gen. Genet. 258, 655-662.
47. Sauer, N. and Stolz, J. (1994) SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana; expression and characterization in baker's yeast and identification of the histidine-tagged protein. Plant J. 6, 67-77.
48. + channel in insulin secreting cells. Biochem. Biophys. Res. Commun. 146, 21-25.
49. Schönknecht, G., Spoormaker, P., Steinmeyer, R., Bruggeman, L., Ache, P., Dutta, R., Reintanz, B., Godde, M., Hedrich, R. and Palme, K. (2002) KCO1 is a component of the slow-vacuolar (SV) ion channel. FEBS Lett. 511, 28-32.
50. Schroeder, J.I., Allen, G.J., Hugouvieux, V., Kwak, J.M. and Waner, D. (2001a) Guard cell signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-658.
51. Schroeder, J.I., Kwak, J.M. and Allen, G.J. (2001b) Guard cell abscisic acid signal transduction network and engineering of plant drought hardiness. Nature, 410, 327-330.
52. Schultz, B.D., Deroos, A.D.G., Venglarik, C.J., Singh, A.K., Frizzell, R.A. and Bridges, R.J. (1996) Glibenclamide blockade of CFTR chloride channels. Am. J. Physiol. 15, L192-L200.
53. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flügge, U.I. and Kunze, R. (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26.
54. Schweitzer, B.I., Dicker, A.P. and Bertino, J.R. (1990) Dihydrofolate reductase as a therapeutic target. FASEB J. 4, 2441-2452.
55. Sharma, K.G., Mason, D.L., Liu, G., Rea, P.A., Bachhawat, A.K. and Michaelis, S. (2002) Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot Cell, 1, 391-400.
56. Szyroki, A., Ivashikina, N., Dietrich, P. et al. (2001) KAT1 is not essential for stomatal opening. Proc. Natl. Acad. Sci. USA, 98, 2917-2921.
57. Talbott, L.D. and Zeiger, E. (1996) Central roles for potassium and sucrose in guard-cell osmoregulation. Plant Physiol. 111, 1051-1057.
58. Theodoulou, F.L., Clark, I.M., He, X.L., Pallett, K.E., Cole, D.J. and Hallahan, D.L. (2003) Co-induction of glutathione-S-transferases and multidrug resistance associated protein by xenobiotics in wheat. Pest Manag. Sci. 59, 202-214.
59. Tommasini, R., Vogt, E., Schmid, J., Fromentau, M., Amrhein, N. and Martinoia, E. (1997) Differential expression of genes coding for ABC transporters after treatment of Arabidopsis thaliana with xenobiotics. FEBS Lett. 411, 206-210.
60. Überlacker, B. and Werr, W. (1996) Vectors with rare cutter restriction enzyme sites for expression of open reading frames in transgenic plants. Mol. Breed. 2, 293-295.
61. Walker, J.E., Saraste, M., Runswick, M.J. and Gay, N.J. (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951.
62. Wanek, W., Heintel, S. and Richter, A. (2001) Preparation of starch and other carbon fractions from higher plant leaves for stable carbon isotope analysis. Rapid Commun. Mass Spectrom. 15, 1136-1140.
63. Wang, X.-Q., Ullah, H., Jones, A.M. and Assmann, S.M. (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science, 292, 2070-2072.
64. Wu, K., Atkinson, I.J., Cossins, E.A. and King, J. (1993) Methotrexate resistance in Datura innoxia - uptake and metabolism of methotrexate in wild-type and resistant cell lines. Plant Physiol. 101, 477-483.
65. Zeng, H., Chen, Z.S., Belinsky, M.G., Rea, P.A. and Kruh, G.D. (2001) Transport of methotrexate (MTX) and folates by multidrug resistance protein (MRP) 3 and MRP1: effect of polyglutamylation on MTX transport. Cancer Res. 61, 7225-7232.