Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate

Plant Journal

Volumn 71, Issue 3, 2012, Pages 479-491

  Arpat, A Bulak ^a   Magliano, Pasqualina ^a   Wege, Stefanie ^a   Rouached, Hatem ^a   Stefanovic, Aleksandra ^a   Poirier, Yves ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Arabidopsis; export; Golgi; PHO1; phosphate; trans Golgi network

Indexed keywords

ARABIDOPSIS; EXPORT; GOLGI; PHO1; TRANS-GOLGI NETWORK;

CELL MEMBRANES; CYANIDES; PHOSPHATES; TISSUE;

CELL CULTURE;

ARABIDOPSIS PROTEIN; HYBRID PROTEIN; NITRATE; PHO1 PROTEIN, ARABIDOPSIS; PHOSPHATE;

ARABIDOPSIS; ARTICLE; CELL MEMBRANE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GOLGI COMPLEX; HOMEOSTASIS; METABOLISM; ONION; PLANT; PLANT LEAF; PLANT ROOT; PROMOTER REGION; PROTOPLAST; SEEDLING; TOBACCO; TRANS GOLGI NETWORK; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GOLGI APPARATUS; HOMEOSTASIS; NITRATES; ONIONS; PHOSPHATES; PLANT LEAVES; PLANT ROOTS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTOPLASTS; RECOMBINANT FUSION PROTEINS; SEEDLING; TOBACCO; TRANS-GOLGI NETWORK;

ALLIUM CEPA; ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

EID: 84864450616     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05004.x     Document Type: Article

References (52)

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. Ames, B.N., (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 8, 115-118.
3. Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., and, Vert, G., (2011) Monoubiquitin-dependent endocytosis of the IRON-REGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants Proc. Natl Acad. Sci. USA 108, E450-E458.
4. Barthes, L., Bousser, A., Hoarau, J., and, Deleens, E., (1995) Reassessment of the relationship between nitrogen supply and xylem exudation in detopped maize seedlings. Plant Physiol. Biochem. 33, 173-183.
5. Bassil, E., Ohto, M.-A., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., Belonte, M., Peleg, Z., Yamaguchi, T., and, Blumwald, E., (2011) The Arabidopsis intracellular Na+/H+ antiporter NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23, 224-239.
6. Batistič, O., Waadt, R., Steinhorst, L., Held, K., and, Kudla, J., (2010) CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. Plant J. 61, 211-222.
7. Bonfante, P., and, Genre, A,. (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Commun. 1, 1-10.doi:.
8. Brand, L., Horler, M., Nuesch, E., Vassalli, S., Barrell, P., Yang, W., Jefferson, R.A., Grossniklaus, U., and, Curtis, M.D., (2006) A versatile and reliable two-component system for tissue-specific gene induction in Arabidopsis. Plant Physiol. 141, 1194-1204.
9. Bucher, M., (2006) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol. 173, 11-26.
10. Carvalho, A., Meireles, L., and, Malcata, F., (1998) Rapid spectrophotometric determination of nitrates and nitrites in marine aqueous culture media. Analusis 26, 347-351.
11. Chanroj, S., Lu, Y., Padmanaban, S., Nanatani, K., Uozumi, N., Rao, R., and, Sze, H., (2011) Plant-specific cation/H+ exchanger 17 and its homologs are endomembrane K+ transporters with roles in protein sorting. J. Biol. Chem. 286, 33931-33941.
12. Chiou, T.-J., and, Lin, S.-I., (2011) Signaling network in sensing phosphate availability. Ann. Rev. Plant Biol. 62, 185-206.
13. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 6, 735-743.
14. Cubero, B., Nakagawa, Y., Jiang, X.Y., Miura, K.J., Li, F., Raghothama, K.G., Bressan, R.A., Hasegawa, P.M., and, Pardo, J.M., (2009) The phosphate transporter PHT4;6 Is a determinant of salt tolerance that Is localized to the golgi apparatus of Arabidopsis. Mol. Plant-Microbe Interact. 2, 535-552.
15. Curtis, M.D., and, Grossniklaus, U., (2003) A gateway cloning vectors set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
16. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M., and, Scheible, W., (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139, 5-17.
17. Dasilva, L., Foresti, O., and, Denecke, J., (2006) Targeting of the plant vacuolar sorting receptor BP80 is dependent on multiple sorting signals in the cytosolic tail. Plant Cell, 18, 1477-1497.
18. Delhaize, E., Gruber, B., Pittman, J.K., White, R., Leung, H., Miao, Y., Jiang, L., Ryan, P., and, Richardson, A., (2007) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. Plant J. 51, 198-210.
19. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D., and, Schumacher, K., (2006) Vaciolar H1-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell, 18, 715-730.
20. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D., Mravec, J., Stierhof, Y., and, Friml, J., (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520-527.
21. von der Fecht-Bartenbach, J., Bogner, M., Krebs, M., Stierhof, Y.-D., Schumacher, K., and, Ludewig, U., (2007) Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J. 50, 466-474.
22. Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferrière, N., Thibaud, J.-B., and, Sentenac, H., (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell, 94, 647-655.
23. Geldner, N., Dénervaud-Tendon, V., Hyman, D.L., Mayer, U., Stierhof, Y.D., and, Chory, J., (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 59, 169-178.
24. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and, Blatt, M., (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355-365.
25. Guo, B., Jin, Y.H., Wussler, C., Blancaflor, E.B., Motes, C.M., and, Versaw, W.K., (2008) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporter. New Phytol. 177, 889-898.
26. Hamburger, D., Rezzonico, E., MacDonald-Comber Petétot, J., Somerville, C., and, Poirier, Y., (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell, 14, 889-902.
27. Krebs, M., Beyhl, D., Görlich, E., Al-Rasheid, K.S., NMarten, I., Stierhof, Y.D., Hedrich, R., and, Schumacher, K., (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl Acad. Sci. USA, 107, 3251-3256.
28. Lagerstedt, J.O., Zvyagilskaya, R., Pratt, J.R., Pattison-Granberg, J., Kruckeberg, A.L., Berden, J.A., and, Persson, B.L., (2002) Mutagenic and functional analysis of the C-terminus of Saccharomyces cerevisae Pho84 phosphate transporter. FEBS Lett. 526, 31-37.
29. Langhans, M., Forster, S., Helmchen, G., and, Robinson, D., (2011) Differential effects of the brefeldin A analogue (6R)-hydroxy-BFA in tobacco and Arabidopsis. J. Exp. Bot. 62, 2949-2957.
30. Lapinskas, P., Cunningham, K., Liu, X., Fink, G., and, Culotta, V., (1995) Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase Mol. Cell. Biol. 15, 1382-1388.
31. Li, X., Chanroj, S., Wu, Z., Romanowsky, S.M., Harper, J.F., and, Sze, H., (2008) A distinct endosomal Ca2 + /Mn2 + pump affects root growth through the secretory process. Plant Physiol. 147, 1675-1689.
32. Lin, S.H., Kuo, H.F., Canivenc, G., et al. (2008) Mutation of the Arabidopsis NTR1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell, 20, 2514-2528.
33. Ma, P., Liu, J., He, H., Yang, M., Li, M., Zhu, X., and, Wang, X., (2009) A viral suppressor P1/HC-Pro increases the GFP gene expression in Agrobacterium-mediated transient assay Appl. Biochem. Biotechnol. 158, 243-252.
34. Marmagne, A., Vinauger-Douard, M., Monachello, D., Falcon de Longevialle, A., XCharon, C., Allot, M., Rappaport, F., Wollman, F.-A., Barbier-Brygoo, H., and, Ephritikhine, G., (2007) Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively. J. Exp. Bot. 58, 3385-3393.
35. McLean, B.G., Hempel, F.D., and, Zambryski, P.C., (1997) Plant intercellular communication via plasmodesmata. Plant Cell, 9, 1043-1054.
36. Mills, R.F., Doherty, M.L., Lopez-Marqués, R.L., Weimar, T., Dupree, P., Palgren, M.G., Pittman, J.K., and, Williams, L.E., (2008) ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. Plant Physiol. 146, 116-128.
37. Nebenfuhr, A., Ritzenthaler, C., and, Robinson, D., (2002) Brefeldin A: Deciphering an enigmatic inhibitor of secretion Plant Physiol. 130, 1102-1108.
38. Nelson, B.K., Cai, X., and, Nebenführ, A., (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
39. Ortiz-Zapater, E., Soriano-Ortega, E., Marcote, M., Ortiz-Masia, D., and, Aniento, F., (2006) Trafficking of the human transferrin receptor in plant cells: effects of tyrphostin A23 and brefeldin A. Plant J. 48, 757-770.
40. Peiter, E., Montanini, B., Gobert, A., Pedas, P., Husted, S., Maathuis, F.J.M., Blaudez, D., Chalot, M., and, Sanders, D., (2007) A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc. Natl Acad. Sci. USA, 104, 8532-8537.
41. Poirier, Y., and, Bucher, M., (2002) Phosphate transport and homeostasis in Arabidopsis. In The Arabidopsis Book (, Somerville, C.R., and, Meyerowitz, E.M., eds). Rockville, MD: American Society of Plant Biologists. 1-35.
42. Poirier, Y., Thoma, S., Somerville, C., and, Schiefelbein, J., (1991) A mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 97, 1087-1093.
43. Roth, C., Menzel, G., Petetot, J., Rochat-Hacker, S., and, Poirier, Y., (2004) Characterization of a protein of the plastid inner envelope having homology to animal inorganic phosphate, chloride and organic-anion transporters. Planta, 218, 406-416.
44. Rutledge, R.G., and, Cote, C., (2003) Mathematics of quantitative kinetic PCR and the application of standard curves. Nucleic Acid Res. 31, e93.
45. Sambrook, J., and, Russel, D,. (2001) Molecular cloning, a laboratory manual Cold Spring Harbor, USA: Cold Spring Harbor Laboratory Press.
46. Secco, D., Baumann, A., and, Poirier, Y., (2010) Charcaterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol. 152, 1693-1704.
47. Secco, D., Wang, C., Arpat, B.A., Wang, Z., Poirier, Y., Tyerman, S.D., Wu, P., Shou, H., and, Whelan, J., (2012) The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol. 193, 852-841.
48. Stefanovic, A., Arpat, A.B., Bligny, R., Gout, E., Vidoudez, C., Bensimon, M., and, Poirier, Y., (2011) Overexpression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J. 66, 689-699.
49. Takano, J., Noguchi, K., Yasumori, M., Kobayashi, M., Gajdos, Z., Miwa, K., Hayashi, H., Yoneyama, T., and, Fujiwara, T., (2002) Arabidopsis boron transporter for xylem loading. Nature, 420, 337-340.
50. Venema, K., Belver, A., Marín-Manzano, M.M., Rodríguez- Rosales, M.P., and, Donaire, R.P., (2003) A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. J. Biol. Chem. 278, 22453-22459.
51. Wang, Y., Ribot, C., Rezzonico, E., and, Poirier, Y., (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol. 135, 400-411.
52. Wang, Y., Secco, D., and, Poirier, Y., (2008) Characterization of the PHO1 gene family and the responses to phosphate deficiency of Physcomitrella patens. Plant Physiol. 146, 646-656.