Lack of the Golgi phosphate transporter PHT4;6 causes strong developmental defects, constitutively activated disease resistance mechanisms and altered intracellular phosphate compartmentation in Arabidopsis

Plant Journal

Volumn 72, Issue 5, 2012, Pages 732-744

  Hassler, Sebastian ^a   Lemke, Lilia ^a   Jung, Benjamin ^a   Möhlmann, Torsten ^a   Krüger, Falco ^b   Schumacher, Karin ^b   Espen, Luca ^c   Martinoia, Enrico ^d   Neuhaus, H Ekkehard ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Arabidopsis; Golgi apparatus; inorganic phosphate; mimic disease; phosphate compartmentation; vacuole

Indexed keywords

ARABIDOPSIS; COMPARTMENTATION; GOLGI APPARATUS; INORGANIC PHOSPHATES; VACUOLE;

BIOLOGY; PLANTS (BOTANY);

PROTEINS;

ALKALOID; ALPHA MANNOSIDASE; ARABIDOPSIS PROTEIN; BREFELDIN A; HEMICELLULOSE; KIFUNENSINE; PHOSPHATE TRANSPORTER; PHT4;6 PROTEIN, ARABIDOPSIS; POLYSACCHARIDE;

ARABIDOPSIS; ARTICLE; CELL WALL; CHEMISTRY; DISEASE RESISTANCE; DRUG EFFECT; GENE SILENCING; GENETIC COMPLEMENTATION; GENETICS; GOLGI COMPLEX; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; RICE; TRANSGENIC PLANT;

ALKALOIDS; ALPHA-MANNOSIDASE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BREFELDIN A; CELL WALL; DISEASE RESISTANCE; GENE KNOCKDOWN TECHNIQUES; GENETIC COMPLEMENTATION TEST; GOLGI APPARATUS; MUTATION; ORYZA SATIVA; PHOSPHATE TRANSPORT PROTEINS; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; POLYSACCHARIDES; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS; ORYZA SATIVA; PSEUDOMONAS SYRINGAE;

EID: 84870063499     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05106.x     Document Type: Article

References (71)

1. Arpat, A.B., Magliano, P., Wege, S., Rouached, H., Stefanovic, A., and, Poirier, Y., (2012) Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. Plant J. 71, 479-491.
2. + antiporters NHX5 and NHX6 are endosome-associated and necessary for plant growth and development. Plant Cell, 23, 224-239.
3. Bucher, M., (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol. 173, 11-26.
4. Cao, H., Li, X., and, Dong, X., (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl Acad. Sci. USA, 95, 6531-6536.
5. Chang, A.B., Lin, R., Keith, S.W., Tran, C.V., and, Saier, M.H. Jr, (2004) Phylogeny as a guide to structure and function of membrane transport proteins. Mol. Membr. Biol. 21, 171-181.
6. 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.
7. Collins, N.C., Thordal-Christensen, H., Lipka, V., et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973-977.
8. 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, 2, 535-552.
9. Denecke, J., Carlsson, L.E., Vidal, S., Hoglund, A.S., Ek, B., van Zeijl, M.J., Sinjorgo, K.M., and, Palva, E.T., (1995) The tobacco homolog of mammalian calreticulin is present in protein complexes in vivo. Plant Cell, 7, 391-406.
10. Eschrich, W., and, Currier, H.-B., (1964) Identification of callose by its diachrome and fluorochrome reactions. Stain Technology, 39, 303-307.
11. 31P-nuclear magnetic resonance in vivo study. Planta, 210, 985-992.
12. Fischer, K., Kammerer, B., Gutensohn, M., Arbinger, B., Weber, A., Häusler, R., and, Flügge, U.I., (1997) A new class of plastidic phosphate translocator: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell, 9, 453-462.
13. Foster, C.E., Martin, T.M., and, Pauly, M., (2010) Comprehensive compositional analysis of plant cell walls (lignocellulosic biomass) part II: carbohydrates. J. Vis. Exp. 12, 1837.
14. Frank, J., Kaulfürst-Soboll, H., Rips, S., Koiwa, H., and, von Schaewen, A., (2008) Comparative analyses of Arabidopsis complex glycan1 mutants and genetic interaction with staurosporin and temperature sensitive3a. Plant Physiol. 148, 1354-1367.
15. Gleave, A.P., (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol., 20, 1203-1207.
16. Guo, B., Irigoyen, S., Fowler, T.B., and, Versaw, W.K., (2008a) Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues. Plant Signal. Behav. 3, 784-790.
17. Guo, B., Jin, Y., Wussler, C., Blancaflor, E.B., Motes, C.M., and, Versaw, W.K., (2008b) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 177, 889-898.
18. Handford, M.G., Sicilia, F., Brandizzi, F., Chung, J.H., and, Dupree, P., (2004) Arabidopsis thaliana expresses multiple Golgi-localised nucleotide-sugar transporters related to GONST1. Mol. Genet. Genomics, 272, 397-410.
19. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and, Mullineaux, P.M., (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
20. Hering, K.W., Karaveg, K., Moremen, K.W., and, Pearson, W.H., (2005) A practical synthesis of kifunensine analogues as inhibitors of endoplasmic reticulum α-mannosidase I. J. Org. Chem. 70, 9892-9904.
21. Hirschberg, C.B., (1997) Transporters of nucleotide sugars, nucleotide sulfate and ATP in the Golgi apparatus membrane: where next? Glycobiology, 7, 169-171.
22. Jung, B., Hoffmann, C., and, Möhlmann, T., (2011) Arabidopsis nucleoside hydrolases involved in intracellular and extracellular degradation of purines. Plant J. 65, 703-711.
23. Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A., and, Flügge, U.I., (1998) Molecular characterisation of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell, 10, 105-117.
24. Kang, J.S., Frank, J., Kang, C.H., et al. (2008) Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl Acad. Sci. USA, 105, 5933-5938.
25. Kariola, T., Brader, G., Li, J., and, Palva, E.T., (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell, 17, 282-294.
26. 31P nuclear magnetic resonance to higher plant tissue. J. Exp. Bot. 33, 670-681.
27. Koiwa, H., Li, F., McCully, M.G., et al. (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell, 15, 2273-2284.
28. Krebs, M., Beyhl, D., Gorlich, E., Al-Rasheid, K.A., Marten, 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.
29. Kunkel, B.N., Bent, A.F., Dahlbeck, D., Innes, R.W., and, Staskawicz, B.J., (1993) RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell, 5, 865-875.
30. Kwon, C., Neu, C., Pajonk, S., et al. (2008) Co-option of a default secretory pathway for plant immune responses. Nature, 451, 835-840.
31. Lai, E., Teodoro, T., and, Volchuk, A., (2007) Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology, 22, 193-201.
32. Leroch, M., Kirchberger, S., Haferkamp, I., Wahl, M., Neuhaus, H.E., and, Tjaden, J., (2005) Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. J. Biol. Chem. 280, 17992-18000.
33. Liu, J.X., and, Howell, S.H., (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell, 22, 2930-2942.
34. Maeda, Y., and, Kinoshita, T., (2010) The acidic environment of the Golgi is critical for glycosylation and transport. Methods Enzymol. 480, 495-510.
35. Mandal, D.K., and, Brewer, C.F., (1993) Differences in the binding affinities of dimeric concanavalin A (including acetyl and succinyl derivatives) and tetrameric concanavalin A with large oligomannose-type glycopeptides. Biochemistry, 32, 5116-5120.
36. Martinoia, E., Maeshima, M., and, Neuhaus, H.E., (2007) Vacuolar transporters and their essential role in plant metabolism. J. Exp. Bot. 58, 83-102.
37. Mazel, A., Leshem, Y., Tiwari, B.S., and, Levine, A., (2004) Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant Physiol. 134, 118-128.
38. Meuwly, P., and, Metraux, J.P., (1993) Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal. Biochem. 214, 500-505.
39. Miyaji, T., Echigo, N., Hiasa, M., Senoh, S., Omote, H., and, Moriyama, Y., (2008) Identification of a vesicular aspartate transporter. Proc. Natl Acad. Sci. USA, 105, 11720-11724.
40. Morita-Yamamuro, C., Tsutsui, T., Sato, M., et al. (2005) The Arabidopsis gene CAD1 controls programmed cell death in the plant immune system and encodes a protein containing a MACPF domain. Plant Cell Physiol. 46, 902-912.
41. Müller, R., Morant, M., Jarmer, H., Nilsson, L., and, Nielsen, T.H., (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol. 143, 156-171.
42. Nakamura, Y., Koizumi, R., Shui, G., Shimojima, M., Wenk, M.R., Ito, T., and, Ohta, H., (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc. Natl Acad. Sci. USA, 106, 20978-20983.
43. Nebenführ, A., Ritzenthaler, C., and, Robinson, D.G., (2002) Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130, 1102-1108.
44. Negrutiu, I., Shillito, R., Potrykus, I., Biasini, G., and, Sala, F., (1987) Hybrid genes in the analysis of transformation conditions. Plant Mol. Biol. 8, 363-373.
45. Peiter, E., Montanini, B., Gobert, A., Pedas, P., Husted, S., Maathuis, F.J., 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.
46. Petersen, M., Brodersen, P., Naested, H., et al. (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell, 103, 1111-1120.
47. 31P-nuclear magnetic resonance study using methylphosphonate as a Pi analog. Plant Physiol. 151, 1646-1657.
48. Rausch, C., and, Bucher, M., (2002) Molecular mechanisms of phosphate transport in plants. Planta, 216, 23-37.
49. Reimer, R.J., and, Edwards, R.H., (2004) Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflügers Arch. 447, 629-635.
50. Reiser, J., Linka, N., Lemke, L., Jeblick, W., and, Neuhaus, H.E., (2004) Molecular physiological analysis of the two plastidic ATP/ADP transporters from Arabidopsis thaliana. Plant Physiol. 136, 3524-3536.
51. 31P NMR. Nature, 283, 870-872.
52. Roth, C., Menzel, G., Petétot, J.M., 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.
53. Saint-Jore, C.M., Evins, J., Batoko, H., Brandizzi, F., Moore, I., and, Hawes, C., (2002) Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29, 661-678.
54. Sawada, K., Echigo, N., Juge, N., Miyaji, T., Otsuka, M., Omote, H., Yamamoto, A., and, Moriyama, Y., (2008) Identification of a vesicular nucleotide transporter. Proc. Natl Acad. Sci. USA, 105, 5683-5686.
55. Schoberer, J., Vavra, U., Stadlmann, J., Hawes, C., Mach, L., Steinkellner, H., and, Strasser, R., (2009) Arginine/lysine residues in the cytoplasmic tail promote ER export of plant glycosylation enzymes. Traffic, 10, 101-115.
56. Shah, J., (2003) The salicylic acid loop in plant defense. Curr. Opin. Plant Biol. 6, 365-371.
57. Shi, H., Kim, Y., Guo, Y., Stevenson, B., and, Zhu, J.K., (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell, 15, 19-32.
58. Shin, H., Shin, H.S., Dewbre, G.R., and, Harrison, M.J., (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 39, 629-642.
59. 31P nuclear magnetic resonance study. Plant Physiol. 99, 856-863.
60. Stefanovic, A., Arpat, A.B., Bligny, R., Gout, E., Vidoudez, C., Bensimon, M., and, Poirier, Y., (2011) Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. Plant J. 66, 689-699.
61. Thulke, O.U., and, Conrath, U., (1998) Salicylic acid has a dual role in the activation of defense related genes in parsley. Plant J. 14, 35-42.
62. Ticconi, C.A., Lucero, R.D., Sakhonwasee, S., Adamson, A.W., Creff, A., Nussaume, L., Desnos, T., and, Abel, S., (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl Acad. Sci. USA, 106, 14174-14179.
63. Uemura, T., Kim, H., Saito, C., Ebine, K., Ueda, T., Schulze-Lefert, P., and, Nakano, A., (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc. Natl Acad. Sci. USA, 109, 1784-1789.
64. Uknes, S., Mauch-Mani, B., Moyer, M., Potter, S., Williams, S., Dincher, S., Chandler, D., Slusarenko, A., Ward, E., and, Ryals, J., (1992) Acquired resistance in Arabidopsis. Plant Cell, 4, 645-656.
65. 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.
66. 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. Mol. Biol. Cell, 17, 4257-4269.
67. Weber, A.P., Schwacke, R., and, Flügge, U.I., (2005) Solute transporters of the plastid envelope membrane. Annu. Rev. Plant Biol. 56, 133-164.
68. Whalen, M.C., Innes, R.W., Bent, A.F., and, Staskawicz, B.J., (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell, 3, 49-59.
69. Wick, P., Gansel, X., Oulevey, C., Page, V., Studer, I., Dürst, M., and, Sticher, L., (2003) The expression of the t-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol. 132, 343-351.
70. Wilson, I.B.H., Harthill, J.E., Mullin, N.P., Ashford, D.A., and, Altmann, F., (1998) Core β-1,3-fucose is a key part of the epitope recognized by antibodies reacting against plant N-linked oligosaccharides and is present in a wide variety of plant extracts. Glycobiology, 8, 651-661.
71. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.