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PMID: 19041751 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor.

Cell ·Vol. 135 ·No. 5 ·2008-11-28 ·Pages 879-93

Rancati G, Pavelka N, Fleharty B, Noll A, Trimble R, Walton K, Perera A, Staehling-Hampton K, Seidel CW, Li R

Abstract

The ability to evolve is a fundamental feature of biological systems, but the mechanisms underlying this capacity and the evolutionary dynamics of conserved core processes remain elusive. We show that yeast cells deleted of MYO1, encoding the only myosin II normally required for cytokinesis, rapidly evolved divergent pathways to restore growth and cytokinesis. The evolved cytokinesis phenotypes correlated with specific changes in the transcriptome. Polyploidy and aneuploidy were common genetic alterations in the best evolved strains, and aneuploidy could account for gene expression changes due directly to altered chromosome stoichiometry as well as to downstream effects. The phenotypic effect of aneuploidy could be recapitulated with increased copy numbers of specific regulatory genes in myo1Delta cells. These results demonstrate the evolvability of even a well-conserved process and suggest that changes in chromosome stoichiometry provide a source of heritable variation driving the emergence of adaptive phenotypes when the cell division machinery is strongly perturbed.

MeSH Terms
Aneuploidy Cytokinesis Directed Molecular Evolution Gene Deletion Genome, Fungal Myosin Heavy Chains/genetics Polyploidy Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins/genetics
Chemicals
MYO1 protein, S cerevisiae Saccharomyces cerevisiae Proteins Myosin Heavy Chains
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Rancati Giulia
Stowers Institute for Medical Research, 1000 E. 50th Street, Kansas City, MO 64110, USA.
Pavelka Norman
Fleharty Brian
Noll Aaron
Trimble Rhonda
Walton Kendra
Perera Anoja
Staehling-Hampton Karen
Seidel Chris W
Li Rong
References (44)
44 references, click to expand
  1. 14-3-3sigma controls mitotic translation to facilitate cytokinesis.
    Nature. 2007 Mar 15;446(7133):329-32 PMID: 17361185
  2. The evolutionary consequences of polyploidy.
    Cell. 2007 Nov 2;131(3):452-62 PMID: 17981114
  3. Near-neutrality in evolution of genes and gene regulation.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16134-7 PMID: 12461171
  4. Two rounds of whole genome duplication in the ancestral vertebrate.
    PLoS Biol. 2005 Oct;3(10):e314 PMID: 16128622
  5. 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. 2003 Feb;14(2):798-809 PMID: 12589071
  6. PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY.
    Evolution. 1996 Jun;50(3):967-976 PMID: 28565291
  7. Increased missegregation and chromosome loss with decreasing chromosome size in vertebrate cells.
    Chromosoma. 2006 Feb;115(1):60-74 PMID: 16267674
  8. Predicting deleterious amino acid substitutions.
    Genome Res. 2001 May;11(5):863-74 PMID: 11337480
  9. Yeast Nop15p is an RNA-binding protein required for pre-rRNA processing and cytokinesis.
    EMBO J. 2003 Dec 15;22(24):6573-83 PMID: 14657029
  10. Genome-wide genetic analysis of polyploidy in yeast.
    Nature. 2006 Oct 5;443(7111):541-7 PMID: 17024086
  11. Effects of aneuploidy on cellular physiology and cell division in haploid yeast.
    Science. 2007 Aug 17;317(5840):916-24 PMID: 17702937
  12. Gene loss and evolutionary rates following whole-genome duplication in teleost fishes.
    Mol Biol Evol. 2006 Sep;23(9):1808-16 PMID: 16809621
  13. Adhesion-dependent and contractile ring-independent equatorial furrowing during cytokinesis in mammalian cells.
    Mol Biol Cell. 2005 Aug;16(8):3865-72 PMID: 15944220
  14. Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore.
    Mol Cell. 2007 Jun 22;26(6):853-65 PMID: 17569568
  15. Genetic and morphological evidence for two parallel pathways of cell-cycle-coupled cytokinesis in Dictyostelium.
    J Cell Sci. 2002 May 15;115(Pt 10):2241-51 PMID: 11973364
  16. In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other.
    J Cell Sci. 2002 Jan 15;115(Pt 2):293-302 PMID: 11839781
  17. BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W472-6 PMID: 16845052
  18. Hsp90 as a capacitor for morphological evolution.
    Nature. 1998 Nov 26;396(6709):336-42 PMID: 9845070
  19. Rapid evolutionary escape by large populations from local fitness peaks is likely in nature.
    Evolution. 2005 Jun;59(6):1175-82 PMID: 16050095
  20. Genetic reconstruction of a functional transcriptional regulatory network.
    Nat Genet. 2007 May;39(5):683-7 PMID: 17417638
  21. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin.
    J Med Chem. 1999 Jan 28;42(2):260-6 PMID: 9925731
  22. The Saccharomyces cerevisiae SDA1 gene is required for actin cytoskeleton organization and cell cycle progression.
    J Cell Sci. 2000 Apr;113 ( Pt 7):1199-211 PMID: 10704371
  23. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia.
    Nature. 2006 Nov 9;444(7116):171-8 PMID: 17086204
  24. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation.
    Nat Rev Genet. 2003 Jun;4(6):457-69 PMID: 12776215
  25. Widespread aneuploidy revealed by DNA microarray expression profiling.
    Nat Genet. 2000 Jul;25(3):333-7 PMID: 10888885
  26. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16144-9 PMID: 12446845
  27. 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. 2006 Jan;17(1):336-44 PMID: 16267265
  28. Evolution of functionally conserved enhancers can be accelerated in large populations: a population-genetic model.
    Proc Biol Sci. 2002 May 7;269(1494):953-60 PMID: 12028779
  29. Molecular evidence for an ancient duplication of the entire yeast genome.
    Nature. 1997 Jun 12;387(6634):708-13 PMID: 9192896
  30. Comparative genomic hybridization.
    Annu Rev Genomics Hum Genet. 2005;6:331-54 PMID: 16124865
  31. Chromosome length controls mitotic chromosome segregation in yeast.
    Cell. 1986 May 23;45(4):529-36 PMID: 3518944
  32. Biological robustness.
    Nat Rev Genet. 2004 Nov;5(11):826-37 PMID: 15520792
  33. The status of the neutral theory: the neutral theory of molecular evolution.
    Science. 1984 May 18;224(4650):732-3 PMID: 17780612
  34. PWP2, a member of the WD-repeat family of proteins, is an essential Saccharomyces cerevisiae gene involved in cell separation.
    Mol Gen Genet. 1996 Aug 27;252(1-2):101-14 PMID: 8804409
  35. Ras2 and Ras1 protein phosphorylation in Saccharomyces cerevisiae.
    J Biol Chem. 1997 Jul 25;272(30):18790-800 PMID: 9228053
  36. Polyploid incidence and evolution.
    Annu Rev Genet. 2000;34:401-437 PMID: 11092833
  37. Evolvability.
    Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8420-7 PMID: 9671692
  38. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches.
    Cell. 2007 Oct 5;131(1):121-35 PMID: 17923092
  39. Cell wall integrity signaling in Saccharomyces cerevisiae.
    Microbiol Mol Biol Rev. 2005 Jun;69(2):262-91 PMID: 15944456
  40. From polyploidy to aneuploidy, genome instability and cancer.
    Nat Rev Mol Cell Biol. 2004 Jan;5(1):45-54 PMID: 14708009
  41. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells.
    Curr Biol. 2004 Sep 21;14(18):R806-18 PMID: 15380095
  42. Animal cytokinesis: from parts list to mechanisms.
    Annu Rev Biochem. 2006;75:543-66 PMID: 16756502
  43. Staining of actin with fluorochrome-conjugated phalloidin.
    Methods Enzymol. 1991;194:729-31 PMID: 2005819
  44. Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets.
    PLoS Biol. 2004 Dec;2(12):e379 PMID: 15547975
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2008.09.039
Published
2008-11-28
Pages
879-93
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2776776
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059964 · United States
NIGMS NIH HHS · R01 GM059964-09A1 · United States
NIGMS NIH HHS · GM0558864 · United States
Corrections
CommentIn
PMID: 19041741
External Links
PubMed source DOI: 10.1016/j.cell.2008.09.039 PMC Full Text View journal details
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