Aneuploidy Underlies Rapid Adaptive Evolution of Yeast Cells Deprived of a Conserved Cytokinesis Motor

Cell

Volumn 135, Issue 5, 2008, Pages 879-893

  Rancati, Giulia ^a   Pavelka, Norman ^a   Fleharty, Brian ^a   Noll, Aaron ^a   Trimble, Rhonda ^a   Walton, Kendra ^a   Perera, Anoja ^a   Staehling Hampton, Karen ^a   Seidel, Chris W ^a   Li, Rong ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

CELLBIO; EVO_ECOL; SYSBIO

Indexed keywords

MYOSIN II; TRANSCRIPTOME;

ANEUPLOIDY; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELL CYCLE REGULATION; CELL DIVISION; CELL GROWTH; CHROMOSOME; CYTOKINESIS; DNA SEQUENCE; GENE; GENE CONTROL; GENE EXPRESSION; GENETIC VARIABILITY; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MUTATION; MYO 1; NONHUMAN; PHENOTYPE; POINT MUTATION; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM; STOICHIOMETRY; TRANSCRIPTOMICS; YEAST;

EID: 56349088536     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.09.039     Document Type: Article

References (48)

1. Adams A.E., and Pringle J.R. Staining of actin with fluorochrome-conjugated phalloidin. Methods Enzymol. 194 (1991) 729-731
2. Al-Shahrour F., Minguez P., Tarraga J., Montaner D., Alloza E., Vaquerizas J.M., Conde L., Blaschke C., Vera J., and Dopazo J. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res. 34 (2006) W472-W476
3. Aury J.M., Jaillon O., Duret L., Noel B., Jubin C., Porcel B.M., Segurens B., Daubin V., Anthouard V., Aiach N., et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444 (2006) 171-178
4. Balasubramanian M.K., Bi E., and Glotzer M. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14 (2004) R806-R818
5. Brunet F.G., Crollius H.R., Paris M., Aury J.M., Gibert P., Jaillon O., Laudet V., and Robinson-Rechavi M. Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol. Biol. Evol. 23 (2006) 1808-1816
6. Buscemi G., Saracino F., Masnada D., and Carbone M.L. The Saccharomyces cerevisiae SDA1 gene is required for actin cytoskeleton organization and cell cycle progression. J. Cell Sci. 113 (2000) 1199-1211
7. Camahort R., Li B., Florens L., Swanson S.K., Washburn M.P., and Gerton J.L. Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26 (2007) 853-865
8. Carter A.J., and Wagner G.P. Evolution of functionally conserved enhancers can be accelerated in large populations: a population-genetic model. Proc. Biol. Sci. 269 (2002) 953-960
9. Darwin C. On the Origin of Species by Means of Natural Selection, 1 edn (1859), John Murray, London
10. Dehal P., and Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3 (2005) e314 10.1371/journal.pbio.0030314
11. Dunham M.J., Badrane H., Ferea T., Adams J., Brown P.O., Rosenzweig F., and Botstein D. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99 (2002) 16144-16149
12. Eggert U.S., Kiger A.A., Richter C., Perlman Z.E., Perrimon N., Mitchison T.J., and Field C.M. Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets. PLoS Biol. 2 (2004) e379 10.1371/journal.pbio.0020379
13. Eggert U.S., Mitchison T.J., and Field C.M. Animal cytokinesis: From parts list to mechanisms. Annu. Rev. Biochem. 75 (2006) 543-566
14. Elena S.F., and Lenski R.E. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4 (2003) 457-469
15. Gillespie J.H. The status of the neutral theory: The neutral theory of molecular evolution. Science 224 (1984) 732-733
16. Hu Z., Killion P.J., and Iyer V.R. Genetic reconstruction of a functional transcriptional regulatory network. Nat. Genet. 39 (2007) 683-687
17. Hughes T.R., Roberts C.J., Dai H., Jones A.R., Meyer M.R., Slade D., Burchard J., Dow S., Ward T.R., Kidd M.J., et al. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25 (2000) 333-337
18. Ihaka R., and Gentleman R. R: A language for data analysis and graphics. J. Comput. Graph. Statist. 5 (1996) 299-314
19. Kanada M., Nagasaki A., and Uyeda T.Q. Adhesion-dependent and contractile ring-independent equatorial furrowing during cytokinesis in mammalian cells. Mol. Biol. Cell 16 (2005) 3865-3872
20. Kirschner M., and Gerhart J. Evolvability. Proc. Natl. Acad. Sci. USA 95 (1998) 8420-8427
21. Kitano H. Biological robustness. Nat. Rev. Genet. 5 (2004) 826-837
22. Levin D.E. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69 (2005) 262-291
23. McClellan A.J., Xia Y., Deutschbauer A.M., Davis R.W., Gerstein M., and Frydman J. Diverse cellular functions of the hsp90 molecular chaperone uncovered using systems approaches. Cell 131 (2007) 121-135
24. Murray A.W., Schultes N.P., and Szostak J.W. Chromosome length controls mitotic chromosome segregation in yeast. Cell 45 (1986) 529-536
25. Nagasaki A., de Hostos E.L., and Uyeda T.Q.P. Genetic and morphological evidence for two parallel pathways of cell-cycle-coupled cytokinesis in Dictyostelium. J. Cell Sci. 115 (2002) 2241-2251
26. Ng P.C., and Henikoff S. Predicting deleterious amino acid substitutions. Genome Res. 11 (2001) 863-874
27. Oeffinger M., and Tollervey D. Yeast Nop15p is an RNA-binding protein required for pre-rRNA processing and cytokinesis. EMBO J. 22 (2003) 6573-6583
28. Ohta T. Near-neutrality in evolution of genes and gene regulation. Proc. Natl. Acad. Sci. USA 99 (2002) 16134-16137
29. Otto S.P. The evolutionary consequences of polyploidy. Cell 131 (2007) 452-462
30. Otto S.P., and Whitton J. Polyploid incidence and evolution. Annu. Rev. Genet. 34 (2000) 401-437
31. Pinkel D., and Albertson D.G. Comparative genomic hybridization. Annu. Rev. Genomics Hum. Genet. 6 (2005) 331-354
32. Roe S.M., Prodromou C., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J. Med. Chem. 42 (1999) 260-266
33. Rutherford S.L., and Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 396 (1998) 336-342
34. Schmidt M., Bowers B., Varma A., Roh D.H., and Cabib E. In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J. Cell Sci. 115 (2002) 293-302
35. Shafaatian R., Payton M.A., and Reid J.D. PWP2, a member of the WD-repeat family of proteins, is an essential Saccharomyces cerevisiae gene involved in cell separation. Mol. Gen. Genet. 252 (1996) 101-114
36. Sherman F., Fink G., Lawrence C., and Cold Spring Harbor Laboratory. Methods in Yeast Genetics (1974), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
37. Spence J.M., Mills W., Mann K., Huxley C., and Farr C.J. Increased missegregation and chromosome loss with decreasing chromosome size in vertebrate cells. Chromosoma 115 (2006) 60-74
38. Squirrell J.M., Eggers Z.T., Luedke N., Saari B., Grimson A., Lyons G.E., Anderson P., and White J.G. CAR-1, a protein that localizes with the mRNA decapping component DCAP-1, is required for cytokinesis and ER organization in Caenorhabditis elegans embryos. Mol. Biol. Cell 17 (2006) 336-344
39. Storchova Z., and Pellman D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell Biol. 5 (2004) 45-54
40. Storchova Z., Breneman A., Cande J., Dunn J., Burbank K., O'Toole E., and Pellman D. Genome-wide genetic analysis of polyploidy in yeast. Nature 443 (2006) 541-547
41. Tolliday N., Pitcher M., and Li R. Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II. Mol. Biol. Cell 14 (2003) 798-809
42. Torres E.M., Sokolsky T., Tucker C.M., Chan L.Y., Boselli M., Dunham M.J., and Amon A. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317 (2007) 916-924
43. Wagner A. Robustness and Evolvability in Living Systems. 1 edn Volume 1 (2005), Princeton University Press, Princeton, NJ
44. Wagner G.P., and Altenberg L. Perspective: complex adaptations and the evolution of evolvability. Evolution Int. J. Org. Evolution 50 (1996) 967-976
45. Weinreich D.M., and Chao L. Rapid evolutionary escape by large populations from local fitness peaks is likely in nature. Evolution Int. J. Org. Evolution 59 (2005) 1175-1182
46. Whistler J.L., and Rine J. Ras2 and Ras1 protein phosphorylation in Saccharomyces cerevisiae. J. Biol. Chem. 272 (1997) 18790-18800
47. Wilker E.W., van Vugt M.A., Artim S.A., Huang P.H., Petersen C.P., Reinhardt H.C., Feng Y., Sharp P.A., Sonenberg N., White F.M., et al. 14-3-3sigma controls mitotic translation to facilitate cytokinesis. Nature 446 (2007) 329-332
48. Wolfe K.H., and Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387 (1997) 708-713