Ploidy-regulated variation in biofilm-related phenotypes in natural isolates of saccharomyces cerevisiae

G3: Genes, Genomes, Genetics

Volumn 4, Issue 9, 2014, Pages 1773-1786

  Hope, Elyse A ^a   Dunham, Maitreya J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Biofilm; Flocculation; Natural isolates; Saccharomyces cerevisiae

Indexed keywords

AGAR; CRYSTAL VIOLET; POLYSTYRENE;

ARTICLE; BIOFILM; DIPLOIDY; FLOCCULATION; FUNGAL GENOME; HAPLOIDY; LIQUID CULTURE; PHENOTYPIC VARIATION; SACCHAROMYCES CEREVISIAE; CELL ADHESION; CELL MOTION; GENETICS; PHENOTYPE; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

BIOFILMS; CELL ADHESION; CELL MOVEMENT; DIPLOIDY; HAPLOIDY; PHENOTYPE; SACCHAROMYCES CEREVISIAE;

EID: 84907916694     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.114.013250     Document Type: Article

References (53)

1. Abramoff, M. D., P. J. Magalhaes, and S. J. Ram, 2004 Image processing with ImageJ. Biophotonics International 11: 36-42.
2. Bauer, F. F., P. Govender, and M. C. Bester, 2010 Yeast flocculation and its biotechnological relevance. Appl. Microbiol. Biotechnol. 88: 31-39.
3. Bayly, J. C., L. M. Douglas, I. S. Pretorius, F. F. Bauer, and A. M. Dranginis, 2005 Characteristics of Flo11-dependent flocculation in Saccharomyces cerevisiae. FEMS Yeast Res. 5: 1151-1156.
4. Beauvais, A., C. Loussert, M. C. Prevost, K. Verstrepen, and J. P. Latgé, 2009 Characterization of a biofilm-like extracellular matrix in FLO1- expressing Saccharomyces cerevisiae cells. FEMS Yeast Res. 9: 411-419.
5. Bergström, A., J. T. Simpson, F. Salinas, B. Barré, L. Parts et al., 2014 A high-definition view of functional genetic variation from natural yeast genomes. Mol. Biol. Evol. 31: 872-888.
6. Bony, M., D. Thines-Sempoux, P. Barre, and B. Blondin, 1997 Localization and cell surface anchoring of the Saccharomyces cerevisiae flocculation protein Flo1p. J. Bacteriol. 179: 4929-4936.
7. Brauer, M. J., C. M. Christianson, D. A. Pai, and M. J. Dunham, 2006 Mapping novel traits by array-assisted bulk segregant analysis in Saccharomyces cerevisiae. Genetics 173: 1813-1816.
8. Bruckner, S., and H. U. Mosch, 2012 Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 36: 25-58.
9. Cromie, G. A., K. E. Hyma, C. L. Ludlow, C. Garmendia-Torres, T. L. Gilbert et al., 2013 Genomic sequence diversity and population structure of Saccharomyces cerevisiae assessed by RAD-seq. G3 3: 2163-2171.
10. Cubillos, F. A., E. Billi, E. Zorgo, L. Parts, P. Fargier et al., 2011 Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol. Ecol. 20: 1401-1413.
11. Cubillos, F. A., L. Parts, F. Salinas, A. Bergström, E. Scovacricchi et al., 2013 High-resolution mapping of complex traits with a four-parent advanced intercross yeast population. Genetics 195: 1141-1155.
12. Cullen, P. J., and G. F. Sprague, Jr., 2000 Glucose depletion causes haploid invasive growth in yeast. Proc. Natl. Acad. Sci. USA 97: 13619-13624.
13. de Hoon, M. J. L., S. Imoto, J. Nolan, and S. Miyano, 2004 Open Source Clustering Software. Bioinformatics 20: 1453-1454.
14. Drees, B. L., V. Thorsson, G. W. Carter, A. W. Rives, M. Z. Raymond et al., 2005 Derivation of genetic interaction networks from quantitative phenotype data. Genome Biol. 6: R38.
15. Galitski, T., A. J. Saldanha, C. A. Styles, E. S. Lander, and G. R. Fink, 1999 Ploidy Regulation of Gene Expression. Science 285: 251-254.
16. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink, 1992 Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth regulation by starvation and RAS. Cell 68: 1077-1090.
17. Granek, J. A., and P. M. Magwene, 2010 Environmental and genetic determinants of colony morphology in yeast. PLoS Genet. 6: 1-12.
18. Granek, J. A., D. Murray, O. Kayrkci, and P. M. Magwene, 2013 The genetic architecture of biofilm formation in a clinical isolate of Saccharomyces cerevisiae. Genetics 193: 587-600.
19. Guo, B., C. A. Styles, Q. Feng, and G. R. Fink, 2000 A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc. Natl. Acad. Sci. USA 97: 12158-12163.
20. Halfmann, R., D. F. Jarosz, S. K. Jones, A. Chang, A. K. Lancaster et al., 2012 Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482: 363-368.
21. Hill, J. A., R. Ammar, D. Torti, C. Nislow, and L. E. Cowen, 2013 Genetic and genomic architecture of the evolution of resistance to antifungal drug combinations. PLoS Genet. 9: 1-22.
22. Holmes, D. L., A. K. Lancaster, S. Lindquist, and R. Halfmann, 2013 Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153: 153-165.
23. Jara, M., F. A. Cubillos, V. García, F. Salinas, O. Aguilera et al., 2014 Mapping genetic variants underlying differences in the central nitrogen metabolism in fermenter yeasts. PLoS ONE 9: e86533.
24. Johnston, J. R., and H. P. Reader, 1983 Genetic control of flocculation, pp. 205-224 in Yeast genetics: fundamental and applied aspects, edited by J. F. T. Spencer, D. M. Spencer, and A. R. W. Smith. Springer-Verlag, New York.
25. Kendall, M., 1938 A new measure of rank correlation. Biometrika 30: 81-89.
26. Liti, G.,D.M.Carter,A. M. Moses, J.Warringer, L. Parts et al., 2009 Population genomics of domestic and wild yeasts. Nature 458: 337-341.
27. Liu, H., C. A. Styles, and G. R. Fink, 1996 Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144: 967-978.
28. Lo, W. S., and A. M. Dranginis, 1996 FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin. J. Bacteriol. 178: 7144-7151.
29. Lo, W. S., and A. M. Dranginis, 1998 The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol. Biol. Cell 9: 161-171.
30. Lorenz, M. C., and J. Heitman, 1997 Yeast pseudohyphal growth is regulated by GPA2, a G protein a homolog. EMBO J. 16: 7008-7018.
31. Miki, B. L., N. H. Poon, and V. L. Seligy, 1982 Possible mechanism for flocculation interactions governed by gene FLO1 in Saccharomyces cerevisiae. J. Bacteriol. 150: 878-889.
32. O'Toole, G. A., and R. Kolter, 1998 Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28: 449-461.
33. O'Toole, G. A., H. B. Kaplan, and R. Kolter, 2000 Biofilm formation as microbial development. Annu. Rev. Microbiol. 54: 49-79.
34. Palecek, S. P., A. S. Parikh, and S. J. Kron, 2002 Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology 148: 893-907.
35. Reynolds, T. B., and G. R. Fink, 2001 Bakers' yeast, a model for fungal biofilm formation. Science 291: 878-881.
36. Roop, J. I., and R. B. Brem, 2013 Rare variants in hypermutable genes underlie common morphology and growth traits in wild Saccharomyces paradoxus. Genetics 195: 513-525.
37. Ruusuvuori, P., J. Lin, A. C. Scott, Z. Tan, S. Sorsa et al., 2014 Quantitative analysis of colony morphology in yeast. Biotechniques 56: 18-27.
38. Ryan, O., R. S. Shapiro, C. F. Kurat, D. Mayhew, A. Baryshnikova et al., 2012 Global gene deletion analysis exploring yeast filamentous growth. Science 337: 1353-1356.
39. Saldanha, A. J., 2004 Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
40. Sherman, F., 1998 An introduction to the genetics and molecular biology of the yeast Saccharomyces cerevisiae. Encyclopedia Mol. Biol. Mol. Med. 6: 302-325.
41. Sivakumar, G., D. R. Vail, J. Xu, D. M. Burner, J. O. Lay et al., 2010 Bioethanol and biodiesel: Alternative liquid fuels for future generations. Eng. Life Sci. 10: 8-18.
42. Skelly, D. A., G. E. Merrihew, M. Riffle, C. F. Connelly, E. O. Kerr et al., 2013 Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast. Genome Res. 23: 1496-1504.
43. Smukalla, S., M. Caldara, N. Pochet, A. Beauvais, S. Guadagnini et al., 2008 FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135: 726-737.
44. Storey, J. D., 2002 A direct approach to false discovery rates. J. R. Stat. Soc., B 64: 479-498.
45. Stovicek, V., L. Vachova, M. Kuthan, and Z. Palkova, 2010 General factors important for the formation of structured biofilm-like yeast colonies. Fungal Genet. Biol. 47: 1012-1022.
46. Vachova, L., V. Stovicek, O. Hlavacek, O. Chernyavskiy, L. Stepanek et al., 2011 Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. J. Cell Biol. 194: 679-687.
47. Verstrepen, K. J., and F. M. Klis, 2006 Flocculation, adhesion and biofilm formation in yeasts. Mol. Microbiol. 60: 5-15.
48. Verstrepen, K. J., G. Derdelinckx, H. Verachtert, and F. R. Delvaux, 2003 Yeast flocculation: what brewers should know. Appl. Microbiol. Biotechnol. 61: 197-205.
49. Verstrepen, K. J., T. B. Reynolds, and G. R. Fink, 2004 Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2: 533-540.
50. Voordeckers, K., D. De Maeyer, E. van der Zande, M. D. Vinces, W. Meert et al., 2012 Identification of a complex genetic network underlying Saccharomyces cerevisiae colony morphology. Mol. Microbiol. 86: 225- 239.
51. Warringer, J., E. Zorgo, F. A. Cubillos, A. Zia, A Gjuvsland et al., 2011 Trait variation in yeast is defined by population history. PLoS Genet. 7: e1002111.
52. Wilkening, S., G. Lin, E. S. Fritsch, M. M. Tekkedil, S. Anders et al.,. 2014 An Evaluation of High-Throughput Approaches to QTL Mapping in Saccharomyces cerevisiae. Genetics 196: 853-865.
53. Zorgo, E., K. Chwialkowska, A. B. Gjuvsland, E. Garre, P. Sunnerhagen et al., 2013 Ancient evolutionary trade-offs between yeast ploidy states. PLoS Genet. 9: e1003388.