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Conservation of PHO pathway in ascomycetes and the role of Pho84

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Abstract

In budding yeast, Saccharomyces cerevisiae, the phosphate signalling and response pathway, known as PHO pathway, monitors phosphate cytoplasmic levels by controlling genes involved in scavenging, uptake and utilization of phosphate. Recent attempts to understand the phosphate starvation response in other ascomycetes have suggested the existence of both common and novel components of the budding yeast PHO pathway in these ascomycetes. In this review, we discuss the components of PHO pathway, their roles in maintaining phosphate homeostasis in yeast and their conservation across ascomycetes. The role of high-affinity transporter, Pho84, in sensing and signalling of phosphate has also been discussed

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References

  • Ault-Riché D, Fraley CD, Tzeng CM and Kornberg A 1998 Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J. Bacteriol. 180 1841–1847

    PubMed Central  PubMed  Google Scholar 

  • Berben G, Legrain M, Gilliquet V and Hilger F 1990 The yeast regulatory gene PHO4 encodes a helix-loop-helix motif. Yeast 6 451–454

    Article  CAS  PubMed  Google Scholar 

  • Carter-O'Connell I, Peel MT, Wykoff DD and O'Shea EK 2012 Genome-wide characterization of the phosphate starvation response in Schizosaccharomyces pombe. BMC Genomics 13 697

    Article  PubMed Central  PubMed  Google Scholar 

  • Cassone A, Carpinelli G, Angiolella L, Maddaluno G and Podo F 1983 31P nuclear magnetic resonance study of growth and dimorphic transition in Candida albicans. J. Gen. Microbiol. 129 1569–1575

    CAS  PubMed  Google Scholar 

  • Cordes FS, Bright JN and Sansom MSP 2002 Proline-induced distortions of transmembrane helices. J. Mol. Biol. 323 951–960

    Article  CAS  PubMed  Google Scholar 

  • Dick CF, Dos-Santos ALA and Meyer-Fernandes JR 2011 Inorganic phosphate as an important regulator of phosphatases. Enzyme Res. 2011 103980

    Article  PubMed Central  PubMed  Google Scholar 

  • Gagneur J, Sinha H, Perocchi F, Bourgon R, Huber W and Steinmetz LM 2009 Genome-wide allele- and strand-specific expression profiling. Mol. Syst. Biol. 5 274

    Article  PubMed Central  PubMed  Google Scholar 

  • Ghillebert R, Swinnen E, De Snijder P, Smets B and Winderickx J 2011 Differential roles for the low-affinity phosphate transporters Pho87 and Pho90 in Saccharomyces cerevisiae. Biochem. J. 434 243–251

    Article  CAS  PubMed  Google Scholar 

  • Giots F, Donaton MCV and Thevelein JM 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

    Article  CAS  PubMed  Google Scholar 

  • Gras DE, Persinoti GF, Peres NTA, Martinez-Rossi NM, Tahira AC, Reis EM, Prade RA and Rossi A 2013 Fungal Genetics and Biology. Fungal Genet. Biol. 60 140–149

    Article  CAS  PubMed  Google Scholar 

  • Gras DE, Silveira HCS, Martinez-Rossi NM and Rossi A 2007 Identification of genes displaying differential expression in the nuc-2 mutant strain of the mold Neurospora crassa grown under phosphate starvation. FEMS Microbiol. Lett. 269 196–200

    Article  CAS  PubMed  Google Scholar 

  • Henry TC, Power JE, Kerwin CL, Mohammed A, Weissman JS, Cameron DM and Wykoff DD 2011 Systematic screen of Schizosaccharomyces pombe deletion collection uncovers parallel evolution of the phosphate signal transduction pathway in yeasts. Eukaryot. Cell 10 198–206

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Homann OR, Dea J, Noble SM and Johnson AD 2009 A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5 e1000783

    Article  PubMed Central  PubMed  Google Scholar 

  • Inglis DO, Arnaud MB, Binkley J, Shah P, Skrzypek MS, Wymore F, Binkley G, Miyasato SR, Simison M and Sherlock G 2012 The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nuc. Acid. Res. 40 D667–674

  • Kaffman A, Rank NM, O'Neill EM, Huang LS and O'Shea EK 1998 The receptor Msn5 exports the phosphorylated transcription factor Pho4 out of the nucleus. Nature 396 482–486

    Article  CAS  PubMed  Google Scholar 

  • Kang S and Metzenberg RL 1990 Molecular analysis of nuc-1+, a gene controlling phosphorus acquisition in Neurospora crassa. Mol. Cell Biol. 10 5839–5848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kerwin CL and Wykoff DD 2009 Candida glabrata PHO4 is necessary and sufficient for Pho2-independent transcription of phosphate starvation genes. Genetics 182 471–479

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kerwin CL and Wykoff DD 2012 De novo generation of a phosphate starvation-regulated promoter in Candida glabrata. FEMS Yeast Res. 12 980–989

    Article  CAS  PubMed  Google Scholar 

  • Komeili A 1999 Roles of phosphorylation sites in regulating activity of the transcription factor Pho4. Science 284 977–980

    Article  CAS  PubMed  Google Scholar 

  • Kornberg A, Rao NN and Ault-Riché D 1999 Inorganic polyphosphate a molecule of many functions. Annu. Rev. Biochem. 68 89–125

    Article  CAS  PubMed  Google Scholar 

  • Kulaev I and Kulakovskaya T 2000 Polyphosphate and phosphate pump. Annu. Rev. Microbiol. 54 709–734

    Article  CAS  PubMed  Google Scholar 

  • Leal J, Squina FM, Martinez-Rossi NM and Rossi A 2007 The transcription of the gene for iso-orotate decarboxylase IDCase, an enzyme of the thymidine salvage pathway, is downregulated in the pregc mutant strain of Neurospora crassa grown under phosphate starvation. Can. J. Microbiol. 53 1011–1015

    Article  CAS  PubMed  Google Scholar 

  • Lee MV, Topper SE, Hubler SL, Hose J, Wenger CD, Coon JJ and Gasch AP 2011 A dynamic model of proteome changes reveals new roles for transcript alteration in yeast. Mol. Syst. Biol. 7 514

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee PS, Greenwell PW, Dominska M, Gawel M, Hamilton M and Petes TD 2009 A fine-structure map of spontaneous mitotic crossovers in the yeast Saccharomyces cerevisiae. PLoS Genet. 5 e1000410

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee YS, Mulugu S, York JD and O'Shea EK 2007 Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 316 109–112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lenburg M and O'Shea E 1996 Signaling phosphate starvation. Trends Biochem. Sci. 21 383–387

    Article  CAS  PubMed  Google Scholar 

  • Levy S, Kafri M, Carmi M and Barkai N 2011 The competitive advantage of a dual-transporter system. Science 334 1408–1412

    Article  CAS  PubMed  Google Scholar 

  • Lichko LP, Kulakovskaya TV, Kulakovskaya EV and Kulaev IS 2008 Inactivation of PPX1 and PPN1 genes encoding exopolyphosphatases of Saccharomyces cerevisiae does not prevent utilization of polyphosphates as phosphate reserve. Biochemistry (Mosc.) 73 985–989

    Article  CAS  Google Scholar 

  • Liu C 2000 Regulation of the yeast transcriptional factor PHO2 activity by phosphorylation. J. Biol. Chem. 275 31972–31978

    Article  CAS  PubMed  Google Scholar 

  • Lundh F, Mouillon J-M, Samyn D, Stadler K, Popova Y, Lagerstedt JO, Thevelein JM and Persson BL 2009 Molecular mechanisms controlling phosphate-induced downregulation of the yeast Pho84 phosphate transporter. Biochemistry 48 4497–4505

    Article  CAS  PubMed  Google Scholar 

  • Maundrell K, Nurse P, Schönholzer F and Schweingruber ME 1985 Cloning and characterization of two genes restoring acid phosphatase activity in pho1− mutants of Schizosaccharomyces pombe. Gene 39 223–230

    Article  CAS  PubMed  Google Scholar 

  • Metzenberg RL 1979 Implications of some genetic control mechanisms in Neurospora. Microbiol. Rev. 43 361–383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miyakawa Y 2000 Identification of a Candida albicans homologue of the PHO85 gene, a negative regulator of the PHO system in Saccharomyces cerevisiae. Yeast 16 1045–1051

    Article  CAS  PubMed  Google Scholar 

  • Mouillon J-M and Persson BL 2006 New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae. FEMS Yeast Res. 6 171–176

    Article  CAS  PubMed  Google Scholar 

  • Mulugu S, Bai W, Fridy PC, Bastidas RJ, Otto JC, Dollins DE, Haystead TA, Ribeiro AA and York JD 2007 A conserved family of enzymes that phosphorylate inositol hexakisphosphate. Science 316 106–109

    Article  CAS  PubMed  Google Scholar 

  • Neurospora crassa Sequencing Project 2014 Broad Institute of Harvard and MIT ( http://www.broadinstitute.org/ )

  • Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR and Johnson AD 2012 A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148 126–138

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Odom AR, Stahlberg A, Wente SR and York JD 2000 A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287 2026–2029

    Article  CAS  PubMed  Google Scholar 

  • Ogawa N, DeRisi J and Brown PO 2000 New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol. Biol. Cell 11 4309–4321

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orkwis BR, Davies DL, Kerwin CL, Sanglard D and Wykoff DD 2010 Novel acid phosphatase in Candida glabrata suggests selective pressure and niche specialization in the phosphate signal transduction pathway. Genetics 186 885–895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oshima Y 1997 The phosphatase system in Saccharomyces cerevisiae. Genes Genet. Syst. 72 323–334

    Article  CAS  PubMed  Google Scholar 

  • Peleg Y and Metzenberg RL 1994 Analysis of the DNA-binding and dimerization activities of Neurospora crassa transcription factor NUC-1. Mol. Cell Biol. 14 7816–7826

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peleg Y, Addison R, Aramayo R and Metzenberg RL 1996 Translocation of Neurospora crassa transcription factor NUC-1 into the nucleus is induced by phosphorus limitation. Fungal Genet. Biol. 20 185–191

    Article  CAS  PubMed  Google Scholar 

  • Persson BL, Lagerstedt JO, Pratt JR, Pattison-Granberg J, Lundh K, Shokrollahzadeh S and Lundh F 2003 Regulation of phosphate acquisition in Saccharomyces cerevisiae. Curr. Genet. 43 225–244

    Article  CAS  PubMed  Google Scholar 

  • Persson BL, Petersson J, Fristedt U, Weinander R, Berhe A and Pattison J 1999 Phosphate permeases of Saccharomyces cerevisiae structure, function and regulation. Biochim. Biophys. Acta 1422 255–272

    Article  CAS  PubMed  Google Scholar 

  • Poleg Y, Aramayo R, Kang S, Hall JG and Metzenberg RL 1996 NUC-2, a component of the phosphate-regulated signal transduction pathway in Neurospora crassa, is an ankyrin repeat protein. Mol. Gen. Genet. 252 709–716

    CAS  PubMed  Google Scholar 

  • Popova Y, Thayumanavan P, Lonati E, Agrochão M and Thevelein JM 2010 Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc. Natl. Acad. Sci. USA 107 2890–2895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Romanowski K, Zaborin A, Valuckaite V, Rolfes RJ, Babrowski T, Bethel C, Olivas A, Zaborina O and Alverdy JC 2012 Candida albicans isolates from the gut of critically ill patients respond to phosphate limitation by expressing filaments and a lethal phenotype. PLoS ONE 7 e30119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roomans GM, Blasco F and Borst-Pauwels GW 1977 Cotransport of phosphate and sodium by yeast. Biochim. Biophys. Acta 467 65–71

    Article  CAS  PubMed  Google Scholar 

  • Saiardi A, Nagata E, Luo HR, Sawa A, Luo X, Snowman AM and Snyder SH 2001 Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc. Natl. Acad. Sci. USA 98 2306–2311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saito H 2010 Regulation of cross-talk in yeast MAPK signaling pathways. Curr. Opin. Microbiol. 13 677–683

    Article  CAS  PubMed  Google Scholar 

  • Samyn DR, Ruiz-Pávon L, Andersson MR, Popova Y, Thevelein JM and Persson BL 2012 Mutational analysis of putative phosphate- and proton-binding sites in the Saccharomyces cerevisiae Pho84 phosphate:H+ transceptor and its effect on signalling to the PKA and PHO pathways. Biochem. J. 445 413–422

    Article  CAS  PubMed  Google Scholar 

  • Schwaninger R, Dumermuth E and Schweingruber ME 1990 Effects of seven different mutations in the pho1 gene on enzymatic activity, glycosylation and secretion of acid phosphatase in Schizosaccharomyces pombe. Mol. Gen. Genet. 221 403–410

    Article  CAS  PubMed  Google Scholar 

  • Schweingruber ME, Edenharter E, Zurlinden A and Stockmaier KM 1992 Regulation of pho1-encoded acid phosphatase of Schizosaccharomyces pombe by adenine and phosphate. Curr. Genet. 22 289–292

    Article  CAS  PubMed  Google Scholar 

  • Secco D, Wang C, Shou H and Whelan J 2012 Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Lett. 586 289–295

    Article  CAS  PubMed  Google Scholar 

  • Sethuraman A, Rao NN and Kornberg A 2001 The endopolyphosphatase gene: essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98 8542–8547

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shao D 1998 A cysteine residue in helixII of the bHLH domain is essential for homodimerization of the yeast transcription factor Pho4p. Nuc. Acid. Res. 26 710–714

    Article  CAS  Google Scholar 

  • Shapiro RS, Sellam A, Tebbji F, Whiteway M, Nantel A and Cowen LE 2012 Pho85, Pcl1, and Hms1 signaling governs Candida albicans morphogenesis induced by high temperature or Hsp90 compromise. Curr. Biol. 22 461–470

    Article  CAS  PubMed  Google Scholar 

  • Smith RF, Blasi D and Dayton SL 1973 Phosphatase activity among Candida species and other yeasts isolated from clinical material. Appl. Microbiol. 26 364–367

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vogel K, Hörz W and Hinnen A 1989 The two positively acting regulatory proteins PHO2 and PHO4 physically interact with PHO5 upstream activation regions. Mol. Cell Biol. 9 2050–2057

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wood V, Harris MA, McDowall MD, Rutherford K, Vaughan BW, Staines DM, Aslett M, Lock A, Bähler J, Kersey PJ and Oliver SG 2012 PomBase: a comprehensive online resource for fission yeast. Nuc. Acid. Res. 40 D695–699

  • Wurst H, Shiba T and Kornberg A 1995 The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 177 898–906

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wykoff DD and O'Shea EK 2001 Phosphate transport and sensing in Saccharomyces cerevisiae. Genetics 159 1491–1499

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wykoff DD, Rizvi AH, Raser JM, Margolin B and O'Shea EK 2007 Positive feedback regulates switching of phosphate transporters in S. cerevisiae. Mol. Cell 27 1005–1013

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Correspondence to Himanshu Sinha.

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Corresponding editor: Luis M Corrochano

[Tomar P and Sinha H 2014 Conservation of PHO pathway in ascomycetes and the role of Pho84. J. Biosci. 39 1–12] DOI 10.1007/s12038-014-9435-y

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Tomar, P., Sinha, H. Conservation of PHO pathway in ascomycetes and the role of Pho84. J Biosci 39, 525–536 (2014). https://doi.org/10.1007/s12038-014-9435-y

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