Functional and physiological characterization of Arabidopsis Inositol Transporter1, a novel tonoplast-localized transporter for myo-inositol

Plant Cell

Volumn 20, Issue 4, 2008, Pages 1073-1087

  Schneider, Sabine ^a   Beyhl, Diana ^b   Hedrich, Rainer ^b   Sauer, Norbert ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS PROTEIN; BACTERIAL DNA; COTRANSPORTER; INOSITOL; PRIMER DNA; T DNA; T-DNA;

ARABIDOPSIS; ARTICLE; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PHYSIOLOGY; PROMOTER REGION; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA PRIMERS; DNA, BACTERIAL; INOSITOL; MOLECULAR SEQUENCE DATA; PATCH-CLAMP TECHNIQUES; PROMOTER REGIONS (GENETICS); SACCHAROMYCES CEREVISIAE; SYMPORTERS;

EID: 48549090923     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.107.055632     Document Type: Article

References (86)

1. Abel, S., and Theologis, A. (1994). Transient transformation of Arabidopsis leaf protoplasts: A versatile experimental system to study gene expression. Plant J. 5: 421-427.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Aluri, S., and Büttner, M. (2007). Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc. Natl. Acad. Sci. USA 104: 2537-2542.
4. Barth, I., Meyer, S., and Sauer, N. (2003). PmSUC3: Characterization of a SUT2/SUC3-type sucrose transporter from Plantago major. Plant Cell 15: 1375-1385.
5. Becker, D., Kemper, E., Schell, J., and Masterson, R. (1992). New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20: 8123-8128.
6. Bentsink, L., Yuan, K., Korneef, M., and Vreugdenhil, D. (2003). The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theor. Appl. Genet. 106: 1234-1243.
7. Bertl, A., et al. (1992). Electrical measurements on endomembranes. Science 258: 873-874.
8. Beyreuther, K., Bieseler, B., Ehring, R., Griesser, H.-W., Mieschendahl, M., Müller-Hill, B., and Triesch, I. (1980). Investigation of structure and function of lactose permease of Escherichia coli. Biochem. Soc. Trans. 8: 675-676.
9. Bohnert, H.J., Nelson, D.E., and Jensen, R.G. (1995). Adaptations to environmental stresses. Plant Cell 7: 1099-1111.
10. Brearley, C.A., and Hanke, D.E. (2000). Metabolic relations of inositol 3,4,5,6-tetrakisphosphate revealed by cell permeabilization. Identification of inositol 3,4,5,6-tetrakisphosphate 1-kinase and inositol 3,4,5,6-tetrakisphosphate phosphatase activities in mesophyll cells. Plant Physiol. 122: 1209-1216.
11. Brinch-Pedersen, H., Hatzack, F., Stöger, E., Arcalis, E., Pontopidan, K., and Holm, P.B. (2006). Heat-stable phytases in transgenic wheat (Triticum aestivum L.): Deposition pattern, thermostability, and phytate hydrolysis. J. Agric. Food Chem. 54: 4624-4632.
12. Brinch-Pedersen, H., Sørensen, L.D., and Holm, P.B. (2002). Engineering crop plants: Getting a handle on phosphate. Trends Plant Sci. 7: 118-125.
13. Büttner, M. (2007). The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Lett. 581: 2318-2324.
14. Carpaneto, A., Geiger, D., Bamberg, E., Sauer, N., Fromm, J., and Hedrich, R. (2005). Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf. J. Biol. Chem. 280: 21437-21443.
15. Carter, C., Pan, S., Zouhar, J., Avila, E.L., Girke, T., and Raikhel, N.V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16: 3285-3303.
16. +-antiport in Mesembryanthemum crystallinum. Plant J. 24: 511-522.
17. Chiou, T.J., and Bush, D.R. (1996). Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiol. 110: 511-520.
18. 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.
19. Cohen, J.D., and Bandurski, R.S. (1982). Chemistry and physiology of the bound auxins. Annu. Rev. Plant Physiol. 33: 403-430.
20. Dunn, S.D. (1986). Effects of the modification of transfer buffer composition on the renaturation of proteins in gels on the recognition of proteins on Western blots by monoclonal antibodies. Anal. Biochem. 157: 144-153.
21. Emr, S.D., Schekman, R., Flessel, M.C., and Thorner, J. (1983). An MF alpha 1-SUC2 (alpha-factor-invertase) gene fusion for study of protein localization and gene expression in yeast. Proc. Natl. Acad. Sci. USA 80: 7080-7084.
22. Endler, A., Meyer, S., Schelbert, S., Schneider, T., Weschke, W., Peters, S.W., Keller, F., Baginsky, S., Martinoia, E., and Schmidt, U.G. (2006). Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141: 196-207.
23. + symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J. 6: 697-706.
24. Gao, Z., Maurousset, L., Lemoine, R., Yoo, S.D., Van Nocker, S., and Loescher, W. (2003). Cloning, expression, and characterization of sorbitol transporters from developing sour cherry fruit and leaf sink tissues. Plant Physiol. 131: 1566-1575.
25. García-Mata, R., Bebök, Z., Sorscher, E.J., and Sztul, E.S. (1999). Characterization and dynamics of aggresome formation by a cytosolic GFP-chimera. J. Cell Biol. 146: 1239-1254.
26. Gietz, D., Jean, W.S., Woods, R.A., and Schiestl, R.H. (1992). Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
27. Granot, D., and Snyder, M. (1991). Glucose induces cAMP-independent growth-related changes in stationary phase cells of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88: 5724-5728.
28. Greenwood, J.S., and Bewley, J.D. (1984). Subcellular distribution of phytin in the endosperm of developing castor bean: A possibility for its synthesis in the cytoplasm prior to deposition within protein bodies. Planta 160: 113-120.
29. Guindon, S., and Gascuel, O. (2003). Systematic biology. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
30. Hanahan, D. (1983). Studies on transformation of E. coli with plasmids. J. Mol. Biol. 166: 557-580.
31. Holsters, M., Silva, B., Van Vliet, F., Genetello, C., De Block, M., Dhaese, P., Depicker, A., Inze, D., Engler, G., Villarroel, R., Van Montagu, M., and Schell, J. (1980). The functional organization of the nopaline Agrobacterium tumefaciens plasmid pTiC58. Plasmid 3: 212-230.
32. + currents through SV-type vacuolar channels are sensitive to elevated luminal sodium levels. Plant J. 41: 606-614.
33. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., and Bourguignon, J. (2007). A proteomic dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol. Cell. Proteomics 6: 394-412.
34. Kandler, O., and Hopf, H. (1982). Oligosaccharides based on sucrose (sucrosyl oligosaccharides). In Plant Carbohydrates 1. Encyclopedia of Plant Physiology: Plant Carbohydrates I, Intracellular Carbohydrates, New Series, Vol. 13A, F.A. Loewus and W. Tanner, eds (Berlin: Springer-Verlag), pp. 348-383.
35. Kanter, U., Usadel, B., Guerineau, F., Li, Y., Pauly, M., and Tenhaken, R. (2005). The inositol oxygenase gene family of Arabidopsis is involved in the biosynthesis of nucleotide sugar precursors for cellwall matrix polysaccharides. Planta 221: 243-254.
36. Kim, D.H., Eu, Y.-J., Yoo, C.M., Kim, Y.-W., Pih, K.T., Jin, J.B., Kim, S.J., Stenmark, H., and Inhwan Hwang, I. (2001). Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell 13: 287-301.
37. Klebl, F., Wolf, M., and Sauer, N. (2003). A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepo L.), and by Arabidopsis thaliana δ-TIP or γ-TIP. FEBS Lett. 547: 69-74.
38. +-symport of numerous substrates, including myo-inositol, glycerol, and ribose. Plant Cell 17: 204-218.
39. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
40. Lehle, L. (1990). Phosphatidyl inositol metabolism and its role in signal transduction in growing plants. Plant Mol. Biol. 15: 647-658.
41. Loewus, F.A., and Murthy, P.P.N. (2000). myo-Inositol metabolism in plants. Plant Sci. 150: 1-19.
42. Lorence, A., Chevone, B.I., Mendes, P., and Nessler, C.L. (2004). myo-Inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiol. 134: 1200-1205.
43. Macbeth, M.R., Schubert, H.L., VanDemark, A.P., Lingam, A.T., Hill, C.P., and Bass, B.L. (2005). Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309: 1534-1539.
44. Marger, M.D., and Saier, M.H., Jr. (1993). A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18: 13-20.
45. +-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19: 2023-2038.
46. Martinoia, E., Locher, R., and Vogt, E. (1993). Inositol triphosphate metabolism in subcellular fractions of barley (Hordeum vulgare L.) mesophyll cells. Plant Physiol. 102: 101-105.
47. Martinoia, E., Maeshima, M., and Neuhaus, E. (2007). Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58: 83-102.
48. Miyashita, M., Shugyo, M., and Nikawa, J. (2003). Mutational analysis and localization of the inositol transporters of Saccharomyces cerevisiae. J. Biosci. Bioeng. 96: 291-297.
49. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
50. Nelson, D.E., Koukoumanos, M., and Bohnert, H.J. (1999). Myo-inositol-dependent sodium uptake in ice plant. Plant Physiol. 119: 165-172.
51. Nelson, D.E., Rammesmayer, G., and Bohnert, H.J. (1998). Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell 10: 753-764.
52. Nikawa, J., Hosaka, K., and Yamashita, S. (1993). Differential regulation of two myo-inositol transporter genes of Saccharomyces cerevisiae. Mol. Microbiol. 10: 955-961.
53. Nikawa, J., Tskugoshi, Y., and Yamashita, S. (1991). Isolation and characterization of two distinct myo-inositol transporter genes of Saccharomyces cerevisiae. J. Biol. Chem. 266: 11184-11191.
54. Nishimura, M., and Beevers, H. (1978). Hydrolases in vacuoles from castor bean endosperm. Plant Physiol. 62: 44-48.
55. Noiraud, N., Maurousset, L., and Lemoine, R. (2001). Identification of a mannitol transporter, AgMaT1, in celery phloem. Plant Cell 13: 695-705.
56. Otegui, M.S., Capp, R., and Staehelin, L.A. (2002). Developing seeds of Arabidopsis store different minerals in two types of vacuoles and in the endoplasmic reticulum. Plant Cell 14: 1311-1327.
57. Page, R.D.M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358.
58. Phillippy, B.Q., Bland, J.M., and Evens, T.J. (2003). Ion chromatography of phytate in roots and tubers. J. Agric. Food Chem. 51: 350-353.
59. Raboy, V. (2003). myo-Inositol-1,2,3,4,5,6- hexakisphosphate. Phytochemistry 64: 1033-1043.
60. Ramsperger-Gleixner, M., Geiger, D., Hedrich, R., and Sauer, N. (2004). Differential expression of sucrose transporter and polyol transporter genes during maturation of common plantain companion cells. Plant Physiol. 134: 147-160.
61. Reinders, A., Panshyshyn, J.A., and Ward, J.M. (2005). Analysis of transport activity of Arabidopsis sugar alcohol permease homolog AtPLT5. J. Biol. Chem. 280: 1594-1602.
62. Sato, T., Ohsumi, Y., and Anraku, Y. (1984). Substrate specificities of active transport systems for amino acids in vacuolar-membrane vesicles of Saccharomyces cerevisiae. J. Biol. Chem. 259: 11505-11508.
63. Sauer, N. (2007). Molecular physiology of higher plant sucrose transporters. FEBS Lett. 581: 2309-2317.
64. Sauer, N., Friedlander, K., and Gräml-Wicke, U. (1990). Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO J. 9: 3045-3050.
65. +/monosaccharide co-transporter from Nicotiana tabacum: Cloning and heterologous expression in baker's yeast. Plant J. 4: 601-610.
66. 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.
67. Sauer, N., and Stolz, J. (2000). Expression of foreign transport proteins in yeast. In Practical Approach Series, S.A. Baldwin, ed (Oxford, UK: Oxford University Press), pp. 79-105.
68. Schmidt, U.G., Endler, A., Schelbert, S., Brunner, A., Schnell, M., Neuhaus, H.E., Marty-Mazars, D., Marty, F., Baginsky, S., and Martinoia, E. (2007). Novel tonoplast transporters identified using a proteomic approach with vacuoles isolated from cauliflower buds. Plant Physiol. 145: 216-229.
69. +-transport of myo-inositol across the plasma membrane. Plant Physiol. 141: 565-577.
70. +-symport of different inositols across the plasma membrane. Plant Physiol. 145: 1395-1407.
71. Schultz, C., Gilson, P., Oxley, D., Youl, J., and Bacic, A. (1998). GPI-anchors on arabinogalactan-proteins: Implications for signalling in plants. Trends Plant Sci. 3: 426-431.
72. Schulz-Lessdorf, B., and Hedrich, R. (1995). Protons and calcium modulate SV-type channels in the vacuolar-lysosomal compartment - Channel interaction with calmodulin inhibitors. Planta 197: 655-671.
73. Sherson, S.M., Hemmann, G., Wallace, G., Forbes, S., Germain, V., Stadler, R., Bechtold, N., Sauer, N., and Smith, S.M. (2000). Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J. 24: 849-857.
74. Shi, J., Wang, H., Hazebroek, J., Ertl, D.S., and Harp, T. (2005). The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds. Plant J. 42: 708-719.
75. Shi, J., Wang, H., Schellin, K., Li, B., Faller, F., Stoop, J.M., Meeley, R.B., Ertl, D.S., Ranch, J.P., and Glassman, K. (2007). Embryo-specific silencing of a transporter reduces phytic acid content of maize and soybean seeds. Nat. Biotechnol. 25: 930-937.
76. Shimaoka, T., Ohnishi, M., Sazuka, T., Mitsuhashi, N., Hara-Nishimura, I., Shimazaki, K., Maeshima, M., Yokota, A., Tomizawa, K., and Mimura, T. (2004). Isolation of intact vacuoles and proteomic analysis of tonoplast from suspension-cultured cells of Arabidopsis thaliana. Plant Cell Physiol. 45: 672-683.
77. Su, Y.-H., Frommer, W.B., and Ludewig, U. (2004). Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol. 136: 3104-3113.
78. Szponarski, W., Sommerer, N., Boyer, J.C., Rossignol, M., and Gibart, R. (2004). Large-scale characterization of integral proteins from Arabidopsis vacuolar membrane by two-dimensional liquid chromatography. Proteomics 4: 397-406.
79. Tan, X., Calderon-Villalobos, L.I.A., Sharon, M., Zheng, C., Robinson, C.V., Estelle, M., and Zheng, N. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640-645.
80. Wang, H.X., Weerasinghe, R.R., Perdue, T.D., Cakmakci, N.G., Taylor, J.P., Marzluff, W.F., and Jones, A.M. (2006). A Golgi-localized hexose transporter is involved in heterotrimeric G protein-mediated early development in Arabidopsis. Plant Cell 17: 4257-4269.
81. Weber, A., Servaites, J.C., Geiger, D.R., Kofler, H., Hille, D., Groner, F., Hebbeker, U., and Flügge, U.I. (2000). Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787-802.
82. Weise, A., Barker, L., Kühn, C., Lalonde, S., Buschmann, H., Frommer, W.B., and Ward, J.M. (2000). A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12: 1345-1355.
83. Wink, M. (1993). The plant vacuole: A multifunctional compartment. J. Exp. Bot. 44: 231-246.
84. Wormit, A., Trentmann, O., Feifer, I., Lohr, C., Tjaden, J., Meyer, S., Schmidt, U., Martinoia, E., and Neuhaus, H.E. (2006). Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18: 3476-3490.
85. Yoshida, S. (1979). Freezing injury and phospholipid degradation in vivo in woody plant cells. I. Subcellular localization of phospholipase D in living bark tissue of the black locust tree (Robinia pseudoacacia L.). Plant Physiol. 64: 241-246.
86. Xu, L., Paulsen, A.Q., Ryu, S.B., and Wang, X. (1996). lntracellular localization of phospholipase D in leaves and seedling tissues of castor bean. Plant Physiol. 111: 101-107.