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Schizosaccharomyces pombe rsv1 Transcription Factor and its Putative Homologues Preserved their Functional Homology and are Evolutionarily Conserved

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Abstract

Environmental glucose is an important regulator of biological processes, as it can launch different cell processes depending on its concentration. Thus, low glucose concentration can induce entry into quiescence, which ensures long-term viability for the cells or in other cases mycelial growth in the dimorphic species, which, in turn, provides the cells with fresh nutrients. Several genes, such as the genes of cAMP cascade, are involved in glucose sensing and response. Since this signal transduction pathway seemed to be an evolutionarily conserved process, we assumed that its genes were also conserved and preserved their functional homology. To obtain evidence, Schizosaccharomyces pombe rsv1 and its orthologous genes were investigated using in silico and experimental approaches. Our results supported that the Rsv1 zinc-finger transcription factors of Schizosaccharomyces japonicus and Schizosaccharomyces octosporus and the Candida albicans cas5p were really functional homologues of the S. pombe Rsv1. Namely, the homologous proteins were able to restore mutant phenotype of the S. pombe rsv1-deleted cells. Bioinformatic anaysis revealed that the most conserved parts of the proteins always contained the C2H2 domains and the complementation abilities of the counterpart genes were not uniform regarding the investigated features, which can be in connection with the conserved regions outside C2H2.

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References

  1. Alfa C, Fantes P, Hyams J, Warbrich ME (eds) (1993) Experiments with fission yeast: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  2. Balazs A, Batta G, Miklos I, Acs-Szabo L, Vazquez de Aldana CR, Sipiczki M (2012) Conserved regulators of the cell separation process in Schizosaccharomyces. Fungal Genet Biol 49(3):235–249

    Article  CAS  PubMed  Google Scholar 

  3. Bockmühl DP, Krishnamurthy S, Gerads M, Sonneborn A, Ernst JF (2001) Distinct and redundant roles of the two protein kinase A isoforms Tpk1p and Tpk2p in morphogenesis and growth of Candida albicans. Mol Microbiol 42(5):1243–1257

    Article  PubMed  Google Scholar 

  4. Brown V, Sexton JA, Johnston M (2006) A Glucose sensor in Candida albicans. Eukaryot Cell 5(10):1726–1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bruno VM, Kalachikov S, Subaran R, Nobile CJ, Kyratsous C, Mitchell AP (2006) Control of the c. albicans cell wall damage response by transcriptional regulator cas5. PLoS Pathog 2(3):e21

    Article  PubMed  PubMed Central  Google Scholar 

  6. Buu LM, Chen YC (2014) Impact of glucose levels on expression of hypha-associated secreted aspartyl proteinases in Candida albicans. J Biomed Sci 21:22–31

    Article  PubMed  PubMed Central  Google Scholar 

  7. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cullen PJ, Sprague GF Jr (2000) Glucose depletion causes haploid invasive growth in yeast. PNAS 97(25):13619–13624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Giacometti R, Kronberg F, Biondi RM, Passeron S (2011) Candida albicans Tpk1p and Tpk2p isoforms differentially regulate pseudohyphal development, biofilm structure, cell aggregation and adhesins expression. Yeast 28:293–308

    Article  CAS  PubMed  Google Scholar 

  10. Gupta DR, Paul SK, Oowatari Y, Matsuo Y, Kawamukai M (2011) Complex Formation, Phosphorylation, and Localization of Protein Kinase A of Schizosaccharomyces pombe upon Glucose Starvation. Biosci Biotechnol Biochem 75(8):1456–1465

    Article  CAS  PubMed  Google Scholar 

  11. Hao Z, Furunobu A, Nagata A, Okayama H (1997) A zinc finger protein required for stationary phase viability in fission yeast. J Cell Sci 110:2557–2566

    CAS  PubMed  Google Scholar 

  12. Heiland S, Radovanovic N, Hofer M, Winderickx J and Lichtenberg H (2000) Multiple Hexose Transporters of Schizosaccharomyces pombe J of Bact 182(8):2153–2162

  13. Herman PK Stationary phase in yeast. Curr Opin Microbiol 5(6):602–7

  14. Homann OR, Dea J, Noble SM, Johnson AD (2009) A Phenotypic Profile of the Candida albicans Regulatory Network. PLoS Genet 5(12):e1000783

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hoffman CS (2005) Except in every detail: comparing and contrasting G protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eukaryot Cell 4:495–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hoffman CS (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans 33(01):257–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hudson DA, Sciascia QL, Sanders RJ, Norris GE, Edwards P J B, Sullivan PA, Farley PC (2004) Identification of the dialysable serum inducer of germ-tube formation in Candida albicans. Microbiology 150:3041–3049

    Article  CAS  PubMed  Google Scholar 

  18. Hrmová M, Drobnica L (1981) Induction of mycelial type of development in Candida albicans by low glucose concentration. Mycopathologia 76(2):83–96

    Article  PubMed  Google Scholar 

  19. Kraakman L, Lemaire K, Ma P, Teunissen A WRH, Donaton MCV, Van Dijck P, Winderickx J, de Winde JH, Thevelein JM (2000) The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154(2):609–622

    Google Scholar 

  20. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, Chen D, Langford C, Vetrie D, Bähler J (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4:27–42

    Article  PubMed  PubMed Central  Google Scholar 

  21. Liu J, Jia Y, Li J, Chu Z (2015) Transcriptional profiling analysis of individual kinase-deletion strains of fission yeast in response to nitrogen starvation. Mol Genet Genomics 290:1067–1083

    Article  CAS  PubMed  Google Scholar 

  22. Maidan MM, De Rop L, Serneels J, Exler S, Rupp S, Tournu H, Thevelein JM, Van Dijck P (2005) The G protein-coupled receptor Gpr1 and the G alpha protein Gpa2 act through the cAMP-protein kinase. A pathway to induce morphogenesis in Candida albicans. Mol Biol Cell 16(4):1971–1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mata J, Bahler J (2007) Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol 8(10):R217

    Article  PubMed  PubMed Central  Google Scholar 

  24. Maundrell K (1993) Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123:127–130

    Article  CAS  PubMed  Google Scholar 

  25. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD:NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226

    Article  PubMed  Google Scholar 

  26. Mitchison JM (1970) Physiological and cytological methods for Schizosaccharomyces pombe. Methods Cell Physiol 4:131–165

  27. Miwa T, Takagi Y, Shinozaki M, Yun CW, Schell WA, Perfect JR, Kumagai H, Tamaki H (2004) Gpr1, a putative G-protein-coupled receptor, regulates morphogenesis and hypha formation in the pathogenic fungus Candida albicans. Eukaryot Cell 3(4):919–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ozcan S, Johnston M (1999) Function and regulation of yeast hexose transporters. Microbiol Mol Biol Rev 63(3):554–569

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Pan X, Lei B, Zhou N, Feng B, Yao W, Zhao X, Yu Y, Lu H (2012) “Identification of novel genes involved in DNA damage response by screening a genome-wide Schizosaccharomyces pombe deletion library”. BMC Genomics 13:662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Papp L, Sipiczki M., Miklos I (2016) Expression pattern and phenotypic characterization of the mutant strain reveals target genes and processes regulated by pka1 in the dimorphic fission yeast Schizosaccharomyces japonicus. Curr Genet (in press) DOI:10.1007/s00294-016-0651-x

    PubMed  Google Scholar 

  31. Pletnev P, Osterman I, Sergiev P, Bogdanov A, Dontsova O (2015) Survival guide: Escherichia coli in the stationary phase, Acta Naturae 7(4): 22–33

  32. Prentice HL (1992) High efficiency transformation of Schizosaccharomyces pombe by electroporation. Nucleic Acids Res 20:621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rhind et al (2011) “Comparative Functional Genomics of the Fission Yeasts”. Science 332(6032):930–936

  34. Robertson LS, Fink GR (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci USA 95(23):13783–13787

  35. Sabina J, Brown V (2009) Glucose sensing network in Candida albicans: a sweet spot for fungal morphogenesis. Eukaryot Cell 8(9):1314–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Santangelo GM (2006) Glucose Signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70(1):253–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sipiczki M, Ferenczy L (1977) Protoplast fusion of Schizosaccharomyces pombe auxotrophic mutants of identical mating-type. Mol Gen Genet 151:77–78

    Article  CAS  PubMed  Google Scholar 

  38. Sipiczki M, Takeo K, Grallert A (1998) Growth polarity transitions in adimorphic fission yeast. Microbiology 144(12):3475–3485

    Article  CAS  PubMed  Google Scholar 

  39. Wang Y, Pierce M, Schneper L, Güldal CG, Zhang X, Tavazoie S, Broach JR (2004) Ras and Gpa2 Mediate One Branch of a Redundant Glucose Signaling Pathway in Yeast. PLoS Biol 2(5):e128

    Article  PubMed  PubMed Central  Google Scholar 

  40. Welton RM, Hoffman CS (2000) Glucose monitoring in fission yeast via the gpa2 G, the git5 G, and the git3 putative glucose receptor. Genetics 156:513–521

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Yun CW, Tamaki H, Nakayama R, Yamamoto K, Kumagai H (1997) G-protein coupled receptor from yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 240(2):287–292

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Hungarian National Research, Development and Innovation Office (OTKA K106172), and the European Union, co-financed by the European Social Fund (SROP-4.2.2.B-15/1/KONV-2015-0001). We thank Ilona Lakatos for technical assistance and Dr Tamas Emri (Dept. of Biotechnology and Microbiology, University of Debrecen) for providing the Candida albicans genomic DNA.

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Correspondence to Ida Miklos.

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Pataki, E., Sipiczki, M. & Miklos, I. Schizosaccharomyces pombe rsv1 Transcription Factor and its Putative Homologues Preserved their Functional Homology and are Evolutionarily Conserved. Curr Microbiol 74, 710–717 (2017). https://doi.org/10.1007/s00284-017-1227-9

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  • DOI: https://doi.org/10.1007/s00284-017-1227-9

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