Deciphering the Transcriptional-Regulatory Network of Flocculation in Schizosaccharomyces pombe

PLoS Genetics

Volumn 8, Issue 12, 2012, Pages

  Kwon, Eun Joo Gina ^a   Laderoute, Amy ^a   Chatfield Reed, Kate ^a   Vachon, Lianne ^a   Karagiannis, Jim ^b   Chua, Gordon ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CELL SURFACE PROTEIN; FLOCCULIN; GLYCEROL; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ADN2; TRANSCRIPTION FACTOR ADN3; TRANSCRIPTION FACTOR CBF11; TRANSCRIPTION FACTOR CBF12; TRANSCRIPTION FACTOR MBX2; TRANSCRIPTION FACTOR RFL1; TRANSCRIPTION FACTOR SRE2; TRANSCRIPTION FACTOR YOX1; UNCLASSIFIED DRUG;

ARTICLE; AUTOREGULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FLOCCULIN GENE; FUNGAL FLOCCULATION; FUNGAL PHENOMENA AND FUNCTIONS; GAS2 GENE; GENE; GENE EXPRESSION PROFILING; GSF2 GENE; MBX2 GENE; NONHUMAN; PFL1 GENE; PFL2 GENE; PFL9 GENE; POSITIVE FEEDBACK; PSU1 GENE; RFL1 GENE; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTIONAL REGULATORY NETWORK; UPREGULATION;

FLOCCULATION; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84872021865     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003104     Document Type: Article

References (79)

1. Goossens K, Willaert R, (2010) Flocculation protein structure and cell-cell adhesion mechanism in Saccharomyces cerevisiae. Biotechnol Lett 32: 1571-1585.
2. Soares EV, (2010) Flocculation in Saccharomyces cerevisiae: a review. J Appl Microbiol 110: 1-18.
3. Smukalla S, Caldara M, Pochet N, Beauvais A, Guadagnini S, et al. (2008) FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135: 726-737.
4. Verstrepen KJ, Klis FM, (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60: 5-15.
5. Stratford M, (1989) Evidence for two mechanisms of flocculation in Saccharomyces cerevisiae. Yeast 5 Spec No pp. S441-445.
6. Goossens KV, Stassen C, Stals I, Donohue DS, Devreese B, et al. (2011) The N-terminal domain of the Flo1 flocculation protein from Saccharomyces cerevisiae binds specifically to mannose carbohydrates. Eukaryot Cell 10: 110-117.
7. Tanaka N, Awai A, Bhuiyan MS, Fujita K, Fukui H, et al. (1999) Cell surface galactosylation is essential for nonsexual flocculation in Schizosaccharomyces pombe. J Bacteriol 181: 1356-1359.
8. Van Mulders SE, Christianen E, Saerens SM, Daenen L, Verbelen PJ, et al. (2009) Phenotypic diversity of Flo protein family-mediated adhesion in Saccharomyces cerevisiae. FEMS Yeast Res 9: 178-190.
9. Kobayashi O, Yoshimoto H, Sone H, (1999) Analysis of the genes activated by the FLO8 gene in Saccharomyces cerevisiae. Curr Genet 36: 256-261.
10. Teunissen AW, Steensma HY, (1995) Review: the dominant flocculation genes of Saccharomyces cerevisiae constitute a new subtelomeric gene family. Yeast 11: 1001-1013.
11. Verstrepen KJ, Derdelinckx G, Verachtert H, Delvaux FR, (2003) Yeast flocculation: what brewers should know. Appl Microbiol Biotechnol 61: 197-205.
12. Govender P, Domingo JL, Bester MC, Pretorius IS, Bauer FF, (2008) Controlled expression of the dominant flocculation genes FLO1, FLO5, and FLO11 in Saccharomyces cerevisiae. Appl Environ Microbiol 74: 6041-6052.
13. Purevdorj-Gage B, Orr ME, Stoodley P, Sheehan KB, Hyman LE, (2007) The role of FLO11 in Saccharomyces cerevisiae biofilm development in a laboratory based flow-cell system. FEMS Yeast Res 7: 372-379.
14. Guo B, Styles CA, Feng Q, Fink GR, (2000) A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 97: 12158-12163.
15. Lo WS, Dranginis AM, (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9: 161-171.
16. Bester MC, Pretorius IS, Bauer FF, (2006) The regulation of Saccharomyces cerevisiae FLO gene expression and Ca2+-dependent flocculation by Flo8p and Mss11p. Curr Genet 49: 375-383.
17. Liu H, Styles CA, Fink GR, (1996) Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144: 967-978.
18. Fichtner L, Schulze F, Braus GH, (2007) Differential Flo8p-dependent regulation of FLO1 and FLO11 for cell-cell and cell-substrate adherence of Sacc. cerevisiae S288c. Mol Microbiol 66: 1276-1289.
19. Shen H, Iha H, Yaguchi S, Tsurugi K, (2006) The mechanism by which overexpression of Gts1p induces flocculation in a FLO8-inactive strain of the yeast Saccharomyces cerevisiae. FEMS Yeast Res 6: 914-923.
20. Matsuzawa T, Morita T, Tanaka N, Tohda H, Takegawa K, (2011) Identification of a galactose-specific flocculin essential for non-sexual flocculation and filamentous growth in Schizosaccharomyces pombe. Mol Microbiol 82: 1531-1544.
21. Matsuzawa T, Yoritsune K, Takegawa K, (2012) MADS Box Transcription Factor Mbx2/Pvg4 Regulates Invasive Growth and Flocculation by Inducing gsf2+ Expression in Fission Yeast. Eukaryot Cell 11: 151-158.
22. Prevorovsky M, Grousl T, Stanurova J, Rynes J, Nellen W, et al. (2009) Cbf11 and Cbf12, the fission yeast CSL proteins, play opposing roles in cell adhesion and coordination of cell and nuclear division. Exp Cell Res 315: 1533-1547.
23. Linder T, Gustafsson CM, (2007) Molecular phylogenetics of ascomycotal adhesins-a novel family of putative cell-surface adhesive proteins in fission yeasts. Fungal Genet Biol 45: 485-497.
24. Linder T, Rasmussen NN, Samuelsen CO, Chatzidaki E, Baraznenok V, et al. (2008) Two conserved modules of Schizosaccharomyces pombe Mediator regulate distinct cellular pathways. Nucleic Acids Res 36: 2489-2504.
25. Kang WH, Park YH, Park HM, (2010) The LAMMER kinase homolog, Lkh1, regulates Tup transcriptional repressors through phosphorylation in Schizosaccharomyces pombe. J Biol Chem 285: 13797-13806.
26. Beskow A, Wright AP, (2006) Comparative analysis of regulatory transcription factors in Schizosaccharomyces pombe and budding yeasts. Yeast 23: 929-935.
27. Hertz-Fowler C, Peacock CS, Wood V, Aslett M, Kerhornou A, et al. (2004) GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 32: D339-343.
28. Andreishcheva EN, Kunkel JP, Gemmill TR, Trimble RB, (2004) Five genes involved in biosynthesis of the pyruvylated Galbeta1,3-epitope in Schizosaccharomyces pombe N-linked glycans. J Biol Chem 279: 35644-35655.
29. Dodgson J, Avula H, Hoe KL, Kim DU, Park HO, et al. (2009) Functional genomics of adhesion, invasion, and mycelial formation in Schizosaccharomyces pombe. Eukaryot Cell 8: 1298-1306.
30. Bailey TL, Williams N, Misleh C, Li WW, (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34: W369-373.
31. Chen X, Hughes TR, Morris Q, (2007) RankMotif++: a motif-search algorithm that accounts for relative ranks of K-mers in binding transcription factors. Bioinformatics 23: i72-79.
32. Nurrish SJ, Treisman R, (1995) DNA binding specificity determinants in MADS-box transcription factors. Mol Cell Biol 15: 4076-4085.
33. Pollock R, Treisman R, (1991) Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev 5: 2327-2341.
34. Todd RB, Andrianopoulos A, (1997) Evolution of a fungal regulatory gene family: the Zn(II)2Cys6 binuclear cluster DNA binding motif. Fungal Genet Biol 21: 388-405.
35. Prevorovsky M, Atkinson SR, Ptackova M, McLean JR, Gould K, et al. (2011) N-termini of fungal CSL transcription factors are disordered, enriched in regulatory motifs and inhibit DNA binding in fission yeast. PLoS ONE 6: e23650 doi:10.1371/journal.pone.0023650.
36. Aligianni S, Lackner DH, Klier S, Rustici G, Wilhelm BT, et al. (2009) The fission yeast homeodomain protein Yox1p binds to MBF and confines MBF-dependent cell-cycle transcription to G1-S via negative feedback. PLoS Genet 5: e1000626 doi:10.1371/journal.pgen.1000626.
37. Hughes AL, Todd BL, Espenshade PJ, (2005) SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120: 831-842.
38. Chang YW, Howard SC, Herman PK, (2004) The Ras/PKA signaling pathway directly targets the Srb9 protein, a component of the general RNA polymerase II transcription apparatus. Mol Cell 15: 107-116.
39. Prevorovsky M, Puta F, Folk P, (2007) Fungal CSL transcription factors. BMC Genomics 8: 233.
40. Artavanis-Tsakonas S, Rand MD, Lake RJ, (1999) Notch signaling: cell fate control and signal integration in development. Science 284: 770-776.
41. Gomez-Escoda B, Ivanova T, Calvo IA, Alves-Rodrigues I, Hidalgo E, et al. (2011) Yox1 links MBF-dependent transcription to completion of DNA synthesis. EMBO Rep 12: 84-89.
42. Bachewich C, Nantel A, Whiteway M, (2005) Cell cycle arrest during S or M phase generates polarized growth via distinct signals in Candida albicans. Mol Microbiol 57: 942-959.
43. Bachewich C, Whiteway M, (2005) Cyclin Cln3p links G1 progression to hyphal and pseudohyphal development in Candida albicans. Eukaryot Cell 4: 95-102.
44. Bensen ES, Clemente-Blanco A, Finley KR, Correa-Bordes J, Berman J, (2005) The mitotic cyclins Clb2p and Clb4p affect morphogenesis in Candida albicans. Mol Biol Cell 16: 3387-3400.
45. Chapa y Lazo B, Bates S, Sudbery P, (2005) The G1 cyclin Cln3 regulates morphogenesis in Candida albicans. Eukaryot Cell 4: 90-94.
46. Chou H, Glory A, Bachewich C, (2011) Orthologues of the anaphase-promoting complex/cyclosome coactivators Cdc20p and Cdh1p are important for mitotic progression and morphogenesis in Candida albicans. Eukaryot Cell 10: 696-709.
47. Hussein B, Huang H, Glory A, Osmani A, Kaminskyj S, et al. (2011) G1/S transcription factor orthologues Swi4p and Swi6p are important but not essential for cell proliferation and influence hyphal development in the fungal pathogen Candida albicans. Eukaryot Cell 10: 384-397.
48. Jin R, Dobry CJ, McCown PJ, Kumar A, (2008) Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol Biol Cell 19: 284-296.
49. Ofir A, Hofmann K, Weindling E, Gildor T, Barker KS, et al. (2012) Role of a Candida albicans Nrm1/Whi5 homologue in cell cycle gene expression and DNA replication stress response. Mol Microbiol 84: 778-794.
50. Horton JD, Goldstein JL, Brown MS, (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109: 1125-1131.
51. Strauss CJ, van Wyk PWJ, Lodolo EJ, Botes PJ, Pohl CH, et al. (2007) Mitochondrial Associated Yeast Flocculation-The Effect of Acetylsalicylic Acid. Journal of the Institute of Brewing 113: 42-47.
52. Iung AR, Coulon J, Kiss F, Ekome JN, Vallner J, et al. (1999) Mitochondrial function in cell wall glycoprotein synthesis in Saccharomyces cerevisiae NCYC 625 (Wild type) and [rho(0)] mutants. Appl Environ Microbiol 65: 5398-5402.
53. Dekker N, Speijer D, Grun CH, van den Berg M, de Haan A, et al. (2004) Role of the alpha-glucanase Agn1p in fission-yeast cell separation. Mol Biol Cell 15: 3903-3914.
54. Dekker N, van Rijssel J, Distel B, Hochstenbach F, (2007) Role of the alpha-glucanase Agn2p in ascus-wall endolysis following sporulation in fission yeast. Yeast 24: 279-288.
55. Omi K, Sonoda H, Nagata K, Sugita K, (1999) Cloning and characterization of psu1(+), a new essential fission yeast gene involved in cell wall synthesis. Biochem Biophys Res Commun 262: 368-374.
56. de Medina-Redondo M, Arnaiz-Pita Y, Clavaud C, Fontaine T, del Rey F, et al. (2010) beta(1,3)-glucanosyl-transferase activity is essential for cell wall integrity and viability of Schizosaccharomyces pombe. PLoS ONE 5: e14046 doi:10.1371/journal.pone.0014046.
57. Stratford M, Carter AT, (1993) Yeast flocculation: lectin synthesis and activation. Yeast 9: 371-378.
58. Zhang N, Gardner DC, Oliver SG, Stateva LI, (1999) Down-regulation of the expression of PKC1 and SRB1/PSA1/VIG9, two genes involved in cell wall integrity in Saccharomyces cerevisiae, causes flocculation. Microbiology 145 (Pt 2):: 309-316.
59. Imazu H, Sakurai H, (2005) Saccharomyces cerevisiae heat shock transcription factor regulates cell wall remodeling in response to heat shock. Eukaryot Cell 4: 1050-1056.
60. Sopko R, Huang D, Preston N, Chua G, Papp B, et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21: 319-330.
61. Alonso-Nunez ML, An H, Martin-Cuadrado AB, Mehta S, Petit C, et al. (2005) Ace2p controls the expression of genes required for cell separation in Schizosaccharomyces pombe. Mol Biol Cell 16: 2003-2017.
62. Dekker N, de Haan A, Hochstenbach F, (2006) Transcription regulation of the alpha-glucanase gene agn1 by cell separation transcription factor Ace2p in fission yeast. FEBS Lett 580: 3099-3106.
63. Petit CS, Mehta S, Roberts RH, Gould KL, (2005) Ace2p contributes to fission yeast septin ring assembly by regulating mid2+ expression. J Cell Sci 118: 5731-5742.
64. Rustici G, Mata J, Kivinen K, Lio P, Penkett CJ, et al. (2004) Periodic gene expression program of the fission yeast cell cycle. Nat Genet 36: 809-817.
65. Conlan RS, Tzamarias D, (2001) Sfl1 functions via the co-repressor Ssn6-Tup1 and the cAMP-dependent protein kinase Tpk2. J Mol Biol 309: 1007-1015.
66. Song W, Carlson M, (1998) Srb/mediator proteins interact functionally and physically with transcriptional repressor Sfl1. EMBO J 17: 5757-5765.
67. Alon U, (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
68. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.
69. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
70. Sheff MA, Thorn KS, (2004) Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21: 661-670.
71. Forsburg SL, Sherman DA, (1997) General purpose tagging vectors for fission yeast. Gene 191: 191-195.
72. Chua G, (2009) Identification of transcription factor targets by phenotypic activation and microarray expression profiling in yeast. Methods Mol Biol 548: 19-35.
73. Smyth GK, Speed T, (2003) Normalization of cDNA microarray data. Methods 31: 265-273.
74. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
75. Eisen MB, Spellman PT, Brown PO, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
76. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
77. Buck MJ, Nobel AB, Lieb JD, (2005) ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6: R97.
78. Workman CT, Yin Y, Corcoran DL, Ideker T, Stormo GD, et al. (2005) enoLOGOS: a versatile web tool for energy normalized sequence logos. Nucleic Acids Res 33: W389-392.
79. Amoah-Buahin E, Bone N, Armstrong J, (2005) Hyphal Growth in the Fission Yeast Schizosaccharomyces pombe. Eukaryot Cell 4: 1287-1297.