Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins

FEBS Letters

Volumn 586, Issue 4, 2012, Pages 289-295

  Secco, David ^a,b   Wang, Chuang ^a   Shou, Huixia ^a,b   Whelan, James ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Budding yeast; Phosphate homeostasis; Phosphate starvation; Saccharomyces cerevisiae; SPX domain

Indexed keywords

GDE1 PROTEIN; PHO81 PROTEIN; PHO87 PROTEIN; PHO90 PROTEIN; PHO91 PROTEIN; PHOSPHATE; REGULATOR PROTEIN; SPX DOMAIN CONTAINING PROTEIN; SYG1 PROTEIN; UNCLASSIFIED DRUG; VTC2 PROTEIN; VTC3 PROTEIN; VTC4 PROTEIN; YDR089 PROTEIN;

FUNGAL GENE; NONHUMAN; PHOSPHATE METABOLISM; PHOSPHATE RESPONSIVE SIGNALING PATHWAY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; GENES, FUNGAL; HOMEOSTASIS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; PHOSPHORIC DIESTER HYDROLASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; VESICULAR TRANSPORT PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84862813084     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.01.036     Document Type: Review

References (64)

1. N. Ogawa, J. DeRisi, and P.O. Brown New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis Mol. Biol. Cell 11 2000 4309 4321
2. M.E. Lenburg, and E.K. O'Shea Signaling phosphate starvation Trends Biochem. Sci. 21 1996 383 387 (Pubitemid 26338675)
3. B.L. Persson, J.O. Lagerstedt, J.R. Pratt, J. Pattison-Granberg, K. Lundh, S. Shokrollahzadeh, and F. Lundh Regulation of phosphate acquisition in Saccharomyces cerevisiae Curr. Genet. 43 2003 225 244 (Pubitemid 36833702)
4. J.M. Mouillon, and B.L. Persson New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae FEMS Yeast Res. 6 2006 171 176
5. C. Auesukaree, T. Homma, Y. Kaneko, and S. Harashima Transcriptional regulation of phosphate-responsive genes in low-affinity phosphate-transporter- defective mutants in Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 306 2003 843 850 (Pubitemid 36776208)
6. M. Bun-Ya, M. Nishimura, S. Harashima, and Y. Oshima The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter Mol. Cell. Biol. 11 1991 3229 3238 (Pubitemid 21895710)
7. P. Martinez, R. Zvyagilskaya, P. Allard, and B.L. Persson Physiological regulation of the derepressible phosphate transporter in Saccharomyces cerevisiae J. Bacteriol. 180 1998 2253 2256 (Pubitemid 28212718)
8. D.D. Wykoff, and E.K. O'Shea Phosphate transport and sensing in Saccharomyces cerevisiae Genetics 159 2001 1491 1499 (Pubitemid 34087591)
9. H.C. Hurlimann, M. Stadler-Waibel, T.P. Werner, and F.M. Freimoser Pho91 is a vacuolar phosphate transporter that regulates phosphate and polyphosphate metabolism in Saccharomyces cerevisiae Mol. Biol. Cell 18 2007 4438 4445 (Pubitemid 350060171)
10. D. Secco The emerging importance of the SPX domain-containing proteins in phosphate homeostasis New Phytol 2012
11. B.H. Spain, D. Koo, M. Ramakrishnan, B. Dzudzor, and J. Colicelli Truncated forms of a novel yeast protein suppress the lethality of a G protein alpha subunit deficiency by interacting with the beta subunit J. Biol. Chem. 270 1995 25435 25444
12. Y. Zhou, and M. Ni Short hypocotyl under blue1 truncations and mutations alter its association with a signaling protein complex in Arabidopsis Plant Cell 22 2010 703 715
13. H.C. Hurlimann, B. Pinson, M. Stadler-Waibel, S.C. Zeeman, and F.M. Freimoser The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity EMBO Rep. 10 2009 1003 1008
14. D. Hamburger, E. Rezzonico, J. MacDonald-Comber Petetot, C. Somerville, and Y. Poirier Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem Plant Cell 14 2002 889 902 (Pubitemid 34519610)
15. C. Wang, S. Ying, H. Huang, K. Li, P. Wu, and H. Shou Involvement of OsSPX1 in phosphate homeostasis in rice Plant J. 57 2009 895 904
16. S.I. Lin Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation Plant Cell Physiol. 51 2010 2119 2131
17. S. Kant, M. Peng, and S.J. Rothstein Genetic regulation by NLA and MicroRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis PLoS Genet. 7 2011 e1002021
18. D. Secco, A. Baumann, and Y. Poirier Characterization 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 2010 1693 1704
19. Y. Wang, D. Secco, and Y. Poirier Characterization of the PHO1 gene family and the responses to phosphate deficiency of Physcomitrella patens Plant Physiol. 146 2008 646 656 (Pubitemid 351230793)
20. H. Rouached, A. Stefanovic, D. Secco, A. Bulak Arpat, E. Gout, R. Bligny, and Y. Poirier Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis Plant J. 65 2011 557 570
21. K. Duan, K. Yi, L. Dang, H. Huang, W. Wu, and P. Wu Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation Plant J. 54 2008 965 975 (Pubitemid 351794016)
22. D. Shao, C.L. Creasy, and L.W. Bergman A cysteine residue in helixII of the bHLH domain is essential for homodimerization of the yeast transcription factor Pho4p Nucleic Acids Res. 26 1998 710 714 (Pubitemid 28291268)
23. J.P. Magbanua, N. Ogawa, S. Harashima, and Y. Oshima The transcriptional activators of the PHO regulon, Pho4p and Pho2p, interact directly with each other and with components of the basal transcription machinery in Saccharomyces cerevisiae J. Biochem. 121 1997 1182 1189 (Pubitemid 27290537)
24. B. Smets, R. Ghillebert, P. De Snijder, M. Binda, E. Swinnen, C. De Virgilio, and J. Winderickx Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae Curr. Genet. 56 2010 1 32
25. X. Zhou, and E.K. O'Shea Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4 Mol. Cell 42 2011 826 836
26. A. Komeili, and E.K. O'Shea Roles of phosphorylation sites in regulating activity of the transcription factor Pho4 Science 284 1999 977 980 (Pubitemid 29288439)
27. K.R. Schneider, R.L. Smith, and E.K. O'Shea Phosphate-regulated inactivation of the kinase Pho80-Pho85 by the CDK Inhibitor Pho81 Science 266 1994 122 125
28. E.M. O'Neill, A. Kaffman, E.R. Jolly, and E.K. O'Shea Regulation of Pho4 nuclear localization by the Pho80-Pho85 cyclin-CDK complex Science 271 1996 209 212
29. F. Fassetti, O. Leone, L. Palopoli, S.E. Rombo, and A. Saiardi IP6K gene identification in plant genomes by tag searching BMC Proc. 5 Suppl. 2 2011 S1
30. Y.S. Lee, S. Mulugu, J.D. York, and E.K. O'Shea Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates Science 316 2007 109 112 (Pubitemid 46559529)
31. Y.S. Lee, H. Huang, F. Quiocho, and E. O'Shea Molecular basis of cyclin-CDK-CKI regulation by reversible binding of an inositol pyrophosphate Nat. Chem. Biol. 4 2008 25 32 (Pubitemid 350273651)
32. C.L. Creasy, S.L. Madden, and L.W. Bergman Molecular analysis of the Pho81 gene of Saccharomyces cerevisiae Nucleic Acids Res. 21 1993 1975 1982 (Pubitemid 23178918)
33. N. Ogawa, K. Noguchi, H. Sawai, Y. Yamashita, C. Yompakdee, and Y. Oshima Functional domains of Pho81p, an inhibitor of Pho85p protein kinase, in the transduction pathway of Pi signals in Saccharomyces cerevisiae Mol. Cell. Biol. 15 1995 997 1004
34. S. Huang, D.A. Jeffery, M.D. Anthony, and E.K. O'Shea Functional analysis of the cyclin-dependent kinase inhibitor Pho81 identifies a novel inhibitory domain Mol. Cell. Biol. 21 2001 6695 6705 (Pubitemid 32927435)
35. M. Lee, S. O'Regan, J.L. Moreau, A.L. Johnson, L.H. Johnston, and C.R. Goding Regulation of the Pcl7-Pho85 cyclin-CDK complex by Pho81 Mol. Microbiol. 38 2000 411 422
36. E. Swinnen, J. Rosseels, and J. Winderickx The minimum domain of Pho81 is not sufficient to control the Pho85-Rim15 effector branch involved in phosphate starvation-induced stress responses Curr. Genet. 48 2005 18 33 (Pubitemid 41086353)
37. S. Al-Khodor, C.T. Price, A. Kalia, and Y. Abu Kwaik Functional diversity of ankyrin repeats in microbial proteins Trends Microbiol. 18 2010 132 139
38. R. Ghillebert, E. Swinnen, P. De Snijder, B. Smets, and J. Winderickx Differential roles for the low-affinity phosphate transporters Pho87 and Pho90 in Saccharomyces cerevisiae Biochem. J. 434 2011 243 251
39. B. Pinson, M. Merle, J.M. Franconi, and B. Daignan-Fornier Low affinity orthophosphate carriers regulate PHO gene expression independently of internal orthophosphate concentration in Saccharomyces cerevisiae J. Biol. Chem. 279 2004 35273 35280 (Pubitemid 39100524)
40. F. Giots, M. Donaton, and J. Thevelein 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 2003 1163 1181 (Pubitemid 36232809)
41. J.M. Thevelein Nutrient sensing systems for rapid activation of the protein kinase A pathway in yeast Biochem. Soc. Trans. 33 2005 253 256 (Pubitemid 40313814)
42. M. Rubio-Texeira, G. Van Zeebroeck, K. Voordeckers, and J.M. Thevelein Saccharomyces cerevisiae plasma membrane nutrient sensors and their role in PKA signaling FEMS Yeast Res. 10 2010 134 149
43. Y. Popova, P. Thayumanavan, E. Lonati, M. Agrochao, and J.M. Thevelein Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor Proc. Natl. Acad. Sci. USA 107 2010 2890 2895
44. D.D. Wykoff, A.H. Rizvi, J.M. Raser, B. Margolin, and E.K. O'Shea Positive feedback regulates switching of phosphate transporters in S. cerevisiae Mol. Cell 27 2007 1005 1013 (Pubitemid 47488184)
45. H.C. Hürlimann, B. Pinson, M. Stadler-Waibel, S.C. Zeeman, and F.M. Freimoser The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity EMBO Rep. 10 2009 1003 1008
46. S. Levy, M. Kafri, M. Carmi, and N. Barkai The competitive advantage of a dual-transporter system Science 334 2011 1408 1412
47. L.A. Estrella, S. Krishnamurthy, C.R. Timme, and M. Hampsey The Rsp5 E3 ligase mediates turnover of low affinity phosphate transporters in Saccharomyces cerevisiae J. Biol. Chem. 283 2008 5327 5334
48. F. Lundh, J.M. Mouillon, D. Samyn, K. Stadler, Y. Popova, J.O. Lagerstedt, J.M. Thevelein, and B.L. Persson Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter Biochemistry 48 2009 4497 4505
49. R.A. Zvyagilskaya, F. Lundh, D. Samyn, J. Pattison-Granberg, J.M. Mouillon, Y. Popova, J.M. Thevelein, and B.L. Persson Characterization of the Pho89 phosphate transporter by functional hyper expression in Saccharomyces cerevisiae FEMS Yeast Res. 8 2008 685 696
50. O. Muller Role of the Vtc proteins in V-ATPase stability and membrane trafficking J. Cell Sci. 116 2003 1107 1115 (Pubitemid 36395620)
51. A. Uttenweiler, H. Schwarz, H. Neumann, and A. Mayer The vacuolar transporter chaperone (VTC) complex is required for microautophagy Mol. Biol. Cell 18 2007 166 175 (Pubitemid 46066718)
52. M. Hothorn Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase Science 324 2009 513 516
53. O. Muller, M. Bayer, C. Peters, J. Andersen, M. Mann, and A. Mayer The Vtc proteins in vacuole fusion: coupling NSF activity to V0 trans-complex formation EMBO J. 21 2002 259 269 (Pubitemid 34137288)
54. A. Cohen, N. Perzov, H. Nelson, and N. Nelson A novel family of yeast chaperons involved in the distribution of V-ATPase and other membrane proteins J. Biol. Chem. 274 1999 26885 26893
55. H. Javot, N. Pumplin, and M.J. Harrison Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles Plant, Cell Environ. 30 2007 310 322 (Pubitemid 46184432)
56. K. Urech, M. Durr, T. Boller, A. Wiemken, and J. Schwencke Localization of polyphosphate in vacuoles of Saccharomyces cerevisiae Arch. Microbiol. 116 1978 275 278 (Pubitemid 8309220)
57. P.J. Rooney, L. Ayong, C.M. Tobin, S.N. Moreno, and L.J. Knoll TgVTC2 is involved in polyphosphate accumulation in Toxoplasma gondii Mol. Biochem. Parasitol. 176 2011 121 126
58. V.S. Reddy, A.K. Singh, and R. Rajasekharan The Saccharomyces cerevisiae PHM8 gene encodes a soluble magnesium-dependent lysophosphatidic acid phosphatase J. Biol. Chem. 283 2008 8846 8854
59. E. Fisher Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae J. Biol. Chem. 280 2005 36110 36117 (Pubitemid 41633882)
60. J.L. Patton-Vogt, and S.A. Henry GIT1, a gene encoding a novel transporter for glycerophosphoinositol in Saccharomyces cerevisiae Genetics 149 1998 1707 1715 (Pubitemid 28375944)
61. E. Fisher, C. Almaguer, R. Holic, P. Griac, and J. Patton-Vogt Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae J. Biol. Chem. 280 2005 36110 36117 (Pubitemid 41633882)
62. J.P. Fernandez-Murray, and C.R. McMaster Glycerophosphocholine catabolism as a new route for choline formation for phosphatidylcholine synthesis by the Kennedy pathway J. Biol. Chem. 280 2005 38290 38296 (Pubitemid 43853726)
63. L. Cheng White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases Plant Physiol. 156 2011 1131 1148
64. Y. Cheng, W. Zhou, N.I. El Sheery, C. Peters, M. Li, X. Wang, and J. Huang Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation Plant J. 66 2011 781 795