NITROGEN LIMITATION ADAPTATION, a target of MicroRNA827, Mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis

Plant Cell

Volumn 25, Issue 10, 2013, Pages 4061-4074

  Lin, Wei Yi ^a,b,c   Huang, Teng Kuei ^a,b,c   Chiou, Tzyy Jen ^a,b,c  

^a AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

^b ACADEMIA SINICA   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; MICRORNA; MIRN827 MICRORNA, ARABIDOPSIS; NLA PROTEIN, ARABIDOPSIS; PHO2 PROTEIN, ARABIDOPSIS; PHOSPHATE; PHOSPHATE TRANSPORTER; PLANT RNA; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ADAPTATION; ARABIDOPSIS; CELL MEMBRANE; CELL VACUOLE; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; PROTEIN DEGRADATION; UBIQUITINATION;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; ENDOCYTOSIS; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; MICRORNAS; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; PROTEOLYSIS; RNA, PLANT; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; VACUOLES;

EID: 84888397809     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.116012     Document Type: Article

References (66)

1. Auesukaree, C., Homma, T., Kaneko, Y., and Harashima, S. (2003). Transcriptional regulation of phosphate-responsive genes in lowaffinity phosphate-transporter-defective mutants in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 306: 843-850.
2. Aung, K., Lin, S.I., Wu, C.C., Huang, Y.T., Su, C.L., and Chiou, T.J. (2006). pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141: 1000-1011.
3. Banbury, D.N., Oakley, J.D., Sessions, R.B., and Banting, G. (2003). Tyrphostin A23 inhibits internalization of the transferrin receptor by perturbing the interaction between tyrosine motifs and the medium chain subunit of the AP-2 adaptor complex. J. Biol. Chem. 278: 12022-12028.
4. Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., and Vert, G. (2011). Monoubiquitin-dependent endocytosis of the ironregulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. USA 108: E450-E458.
5. Bari, R., Datt Pant, B., Stitt, M., and Scheible, W.R. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141: 988-999.
6. Bayle, V., Arrighi, J.F., Creff, A., Nespoulous, C., Vialaret, J., Rossignol, M., Gonzalez, E., Paz-Ares, J., and Nussaume, L. (2011). Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23: 1523-1535.
7. Bendahmane, A., Querci, M., Kanyuka, K., and Baulcombe, D.C. (2000). Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: Application to the Rx2 locus in potato. Plant J. 21: 73-81.
8. Castle, J.D. (2003). Purification of organelles from mammalian cells. Curr. Protoc. Immunol. (Hoboken: John Wiley & Sons), pp 56: 8.1B.1-8.1B.57.
9. Chiou, T.J., Aung, K., Lin, S.I., Wu, C.C., Chiang, S.F., and Su, C.L. (2006). Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412-421.
10. Chiou, T.J., and Lin, S.I. (2011). Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62: 185-206.
11. Chiou, T.J., Liu, H., and Harrison, M.J. (2001). The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J. 25: 281-293.
12. 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.
13. Conner, S.D., and Schmid, S.L. (2003). Regulated portals of entry into the cell. Nature 422: 37-44.
14. Delhaize, E., and Randall, P.J. (1995). Characterization of a phosphateaccumulator mutant of Arabidopsis thaliana. Plant Physiol. 107: 207-213.
15. Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., and Friml, J. (2007). Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17: 520-527.
16. Dowil, R.T., Lu, X., Saracco, S.A., Vierstra, R.D., and Downes, B.P. (2011). Arabidopsis membrane-anchored ubiquitin-fold (MUB) proteins localize a specific subset of ubiquitin-conjugating (E2) enzymes to the plasma membrane. J. Biol. Chem. 286: 14913-14921.
17. Dupré, S., Urban-Grimal, D., and Haguenauer-Tsapis, R. (2004). Ubiquitin and endocytic internalization in yeast and animal cells. Biochim. Biophys. Acta 1695: 89-111.
18. Duttweiler, H.M. (1996). A highly sensitive and non-lethal betagalactosidase plate assay for yeast. Trends in Genetics. 12: 340-341.
19. Eide, D., Broderius, M., Fett, J., and Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93: 5624-5628.
20. Galan, J.M., and Haguenauer-Tsapis, R. (1997). Ubiquitin lys63 is involved in ubiquitination of a yeast plasma membrane protein. EMBO J. 16: 5847-5854.
21. Giots, F., Donaton, M.C.V., and Thevelein, J.M. (2003). Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 47: 1163-1181.
22. González, E., Solano, R., Rubio, V., Leyva, A., and Paz-Ares, J. (2005). PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17: 3500-3512.
23. 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.
24. Hao, Y., Sekine, K., Kawabata, A., Nakamura, H., Ishioka, T., Ohata, H., Katayama, R., Hashimoto, C., Zhang, X., Noda, T., Tsuruo, T., and Naito, M. (2004). Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function. Nat. Cell Biol. 6: 849-860.
25. Hsieh, L.C., Lin, S.I., Shih, A.C., Chen, J.W., Lin, W.Y., Tseng, C.Y., Li, W.H., and Chiou, T.J. (2009). Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151: 2120-2132.
26. Hu, H.C., Wang, Y.Y., and Tsay, Y.F. (2009). AtCIPK8, a CBLinteracting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J. 57: 264-278.
27. Huang, T.-K., Han, C.-L., Lin, S.-I., Chen, Y.-J., Tsai, Y.-C., Chen, Y.-R., Chen, J.-W., Lin, W.-Y., Chen, P.-M., Liu, T.-Y., Chen, Y.-S., and Chiou, T.-J. (2013). Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25: 4044-4060.
28. Hürlimann, H.C., Pinson, B., Stadler-Waibel, M., Zeeman, S.C., and Freimoser, F.M. (2009). The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity. EMBO Rep. 10: 1003-1008.
29. Hürlimann, H.C., Stadler-Waibel, M., Werner, T.P., and Freimoser, F.M. (2007). Pho91 Is a vacuolar phosphate transporter that regulates phosphate and polyphosphate metabolism in Saccharomyces cerevisiae. Mol. Biol. Cell 18: 4438-4445.
30. Jia, H., Ren, H., Gu, M., Zhao, J., Sun, S., Zhang, X., Chen, J., Wu, P., and Xu, G. (2011). The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol. 156: 1164-1175.
31. Kang, X., Li, W., Zhou, Y., and Ni, M. (2013). A WRKY transcription factor recruits the SYG1-like protein SHB1 to activate gene expression and seed cavity enlargement. PLoS Genet. 9: e1003347.
32. Kant, S., Peng, M., and Rothstein, S.J. (2011). Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet. 7: e1002021.
33. Karthikeyan, A.S., Varadarajan, D.K., Mukatira, U.T., D'Urzo, M.P., Damsz, B., and Raghothama, K.G. (2002). Regulated expression of Arabidopsis phosphate transporters. Plant Physiol. 130: 221-233.
34. Kasai, K., Takano, J., Miwa, K., Toyoda, A., and Fujiwara, T. (2011). High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem. 286: 6175-6183.
35. Lagerstedt, J.O., Voss, J.C., Wieslander, A., and Persson, B.L. (2004). Structural modeling of dual-affinity purified Pho84 phosphate transporter. FEBS Lett. 578: 262-268.
36. Larsson, C., Widell, S., and Kjellbom, P. (1987). Preparation of highpurity plasma membranes. Methods Enzymol. 148: 558-568.
37. Lauwers, E., Jacob, C., and André, B. (2009). K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J. Cell Biol. 185: 493-502.
38. Leitner, J., Petrášek, J., Tomanov, K., Retzer, K., Pařezová, M., Korbei, B., Bachmair, A., Zažímalová, E., and Luschnig, C. (2012). Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl. Acad. Sci. USA 109: 8322-8327.
39. Lin, S.I., et al. (2010). Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol. 51: 2119-2131.
40. Lin, S.I., Wang, J.G., Poon, S.Y., Su, C.L., Wang, S.S., and Chiou, T.J. (2005). Differential regulation of FLOWERING LOCUS C expression by vernalization in cabbage and Arabidopsis. Plant Physiol. 137: 1037-1048.
41. + transport activity is required for systemic phosphate homeostasis involving shoot-to-root signaling in Arabidopsis. Plant Physiol. 156: 1176-1189.
42. Liu, T.Y., Huang, T.K., Tseng, C.Y., Lai, Y.S., Lin, S.I., Lin, W.Y., Chen, J.W., and Chiou, T.J. (2012). PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24: 2168-2183.
43. Lundh, F., Mouillon, J.M., Samyn, D., Stadler, K., Popova, Y., Lagerstedt, J.O., Thevelein, J.M., and Persson, B.L. (2009). Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter. Biochemistry 48: 4497-4505.
44. Marmagne, A., Rouet, M.A., Ferro, M., Rolland, N., Alcon, C., Joyard, J., Garin, J., Barbier-Brygoo, H., and Ephritikhine, G. (2004). Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Mol. Cell. Proteomics 3: 675-691.
45. Marschner, H. (1995). Functions of mineral nutrients: Macronutrients. In Mineral Nutrition of Higher Plants, 2nd ed (London: Academic Press), pp 265-277, 537-594.
46. Misson, J., Thibaud, M.-C., Bechtold, N., Raghothama, K., and Nussaume, L. (2004). Transcriptional regulation and functional properties of Arabidopsis Pht1;4, a high affinity transporter contributing greatly to phosphate uptake in phosphate deprived plants. Plant Mol. Biol. 55: 727-741.
47. Muchhal, U.S., Pardo, J.M., and Raghothama, K.G. (1996). Phosphate transporters from the higher plant Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93: 10519-10523.
48. Muchhal, U.S., and Raghothama, K.G. (1999). Transcriptional regulation of plant phosphate transporters. Proc. Natl. Acad. Sci. USA 96: 5868-5872.
49. Nühse, T.S., Stensballe, A., Jensen, O.N., and Peck, S.C. (2004). Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16: 2394-2405.
50. Nussaume, L., Kanno, S., Javot, H., Marin, E., Pochon, N., Ayadi, A., Nakanishi, T.M., and Thibaud, M.C. (2011). Phosphate import in plants: Focus on the PHT1 transporters. Front. Plant Sci. 2: 83.
51. Paszkowski, U., Kroken, S., Roux, C., and Briggs, S.P. (2002). Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 99: 13324-13329.
52. Peng, J., Schwartz, D., Elias, J.E., Thoreen, C.C., Cheng, D., Marsischky, G., Roelofs, J., Finley, D., and Gygi, S.P. (2003). A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21: 921-926.
53. Peng, M., Hannam, C., Gu, H., Bi, Y.M., and Rothstein, S.J. (2007). A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J. 50: 320-337.
54. Raghothama, K.G. (1999). Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 665-693.
55. Scheuring, D., Künzl, F., Viotti, C., Yan, M.S., Jiang, L., Schellmann, S., Robinson, D.G., and Pimpl, P. (2012). Ubiquitin initiates sorting of Golgi and plasma membrane proteins into the vacuolar degradation pathway. BMC Plant Biol. 12: 164.
56. 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: 842-851.
57. 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.
58. Shin, L.J., Lo, J.C., Chen, G.H., Callis, J., Fu, H., and Yeh, K.C. (2013). IRT1 DEGRADATION FACTOR1, a RING E3 ubiquitin ligase, regulates the degradation of IRON-REGULATED TRANSPORTER1 in Arabidopsis. Plant Cell.
59. Stone, S.L., Hauksdóttir, H., Troy, A., Herschleb, J., Kraft, E., and Callis, J. (2005). Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137: 13-30.
60. Sun, S., Gu, M., Cao, Y., Huang, X., Zhang, X., Ai, P., Zhao, J., Fan, X., and Xu, G. (2012). A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphatereplete rice. Plant Physiol. 159: 1571-1581.
61. Tian, G.-W., et al. (2004). High-throughput fluorescent tagging of fulllength Arabidopsis gene products in planta. Plant Physiol. 135: 25-38.
62. Tsay, Y.F., Schroeder, J.I., Feldmann, K.A., and Crawford, N.M. (1993). The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72: 705-713.
63. Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., and Curie, C. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14: 1223-1233.
64. Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T., and Lin, C.S. (2009). Tape-Arabidopsis Sandwich-A simpler Arabidopsis protoplast isolation method. Plant Methods 5: 16.
65. Yaeno, T., and Iba, K. (2008). BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol. 148: 1032-1041.
66. Yamada, K., Fuji, K., Shimada, T., Nishimura, M., and Hara-Nishimura, I. (2005). Endosomal proteases facilitate the fusion of endosomes with vacuoles at the final step of the endocytotic pathway. Plant J. 41: 888-898.