Literature DB >> 23197825

Chromosomal duplication is a transient evolutionary solution to stress.

Avihu H Yona1, Yair S Manor, Rebecca H Herbst, Gal H Romano, Amir Mitchell, Martin Kupiec, Yitzhak Pilpel, Orna Dahan.   

Abstract

Aneuploidy, an abnormal number of chromosomes, is a widespread phenomenon found in unicellulars such as yeast, as well as in plants and in mammalians, especially in cancer. Aneuploidy is a genome-scale aberration that imposes a severe burden on the cell, yet under stressful conditions specific aneuploidies confer a selective advantage. This dual nature of aneuploidy raises the question of whether it can serve as a stable and sustainable evolutionary adaptation. To clarify this, we conducted a set of laboratory evolution experiments in yeast and followed the long-term dynamics of aneuploidy under diverse conditions. Here we show that chromosomal duplications are first acquired as a crude solution to stress, yet only as transient solutions that are eliminated and replaced by more efficient solutions obtained at the individual gene level. These transient dynamics of aneuploidy were repeatedly observed in our laboratory evolution experiments; chromosomal duplications gained under stress were eliminated not only when the stress was relieved, but even if it persisted. Furthermore, when stress was applied gradually rather than abruptly, alternative solutions appear to have emerged, but not aneuploidy. Our findings indicate that chromosomal duplication is a first evolutionary line of defense, that retains survivability under strong and abrupt selective pressures, yet it merely serves as a "quick fix," whereas more refined and sustainable solutions take over. Thus, in the perspective of genome evolution trajectory, aneuploidy is a useful yet short-lived intermediate that facilitates further adaptation.

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Year:  2012        PMID: 23197825      PMCID: PMC3529009          DOI: 10.1073/pnas.1211150109

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  30 in total

1.  Widespread aneuploidy revealed by DNA microarray expression profiling.

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Journal:  Nat Genet       Date:  2000-07       Impact factor: 38.330

Review 2.  Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation.

Authors:  Santiago F Elena; Richard E Lenski
Journal:  Nat Rev Genet       Date:  2003-06       Impact factor: 53.242

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

Authors:  Giulia Rancati; Norman Pavelka; Brian Fleharty; Aaron Noll; Rhonda Trimble; Kendra Walton; Anoja Perera; Karen Staehling-Hampton; Chris W Seidel; Rong Li
Journal:  Cell       Date:  2008-11-28       Impact factor: 41.582

Review 4.  Aneuploidy: cells losing their balance.

Authors:  Eduardo M Torres; Bret R Williams; Angelika Amon
Journal:  Genetics       Date:  2008-06       Impact factor: 4.562

5.  An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1.

Authors:  Anna Selmecki; Maryam Gerami-Nejad; Carsten Paulson; Anja Forche; Judith Berman
Journal:  Mol Microbiol       Date:  2008-03-20       Impact factor: 3.501

Review 6.  Causes and consequences of aneuploidy in cancer.

Authors:  David J Gordon; Benjamin Resio; David Pellman
Journal:  Nat Rev Genet       Date:  2012-01-24       Impact factor: 53.242

Review 7.  The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins.

Authors:  D A Parsell; S Lindquist
Journal:  Annu Rev Genet       Date:  1993       Impact factor: 16.830

8.  Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.

Authors:  E A Winzeler; D D Shoemaker; A Astromoff; H Liang; K Anderson; B Andre; R Bangham; R Benito; J D Boeke; H Bussey; A M Chu; C Connelly; K Davis; F Dietrich; S W Dow; M El Bakkoury; F Foury; S H Friend; E Gentalen; G Giaever; J H Hegemann; T Jones; M Laub; H Liao; N Liebundguth; D J Lockhart; A Lucau-Danila; M Lussier; N M'Rabet; P Menard; M Mittmann; C Pai; C Rebischung; J L Revuelta; L Riles; C J Roberts; P Ross-MacDonald; B Scherens; M Snyder; S Sookhai-Mahadeo; R K Storms; S Véronneau; M Voet; G Volckaert; T R Ward; R Wysocki; G S Yen; K Yu; K Zimmermann; P Philippsen; M Johnston; R W Davis
Journal:  Science       Date:  1999-08-06       Impact factor: 47.728

9.  Aneuploidy and isochromosome formation in drug-resistant Candida albicans.

Authors:  Anna Selmecki; Anja Forche; Judith Berman
Journal:  Science       Date:  2006-07-21       Impact factor: 47.728

10.  Effects of aneuploidy on cellular physiology and cell division in haploid yeast.

Authors:  Eduardo M Torres; Tanya Sokolsky; Cheryl M Tucker; Leon Y Chan; Monica Boselli; Maitreya J Dunham; Angelika Amon
Journal:  Science       Date:  2007-08-17       Impact factor: 47.728

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  146 in total

1.  Semi-supervised prediction of gene regulatory networks using machine learning algorithms.

Authors:  Nihir Patel; Jason T L Wang
Journal:  J Biosci       Date:  2015-10       Impact factor: 1.826

2.  Fate of a mutation in a fluctuating environment.

Authors:  Ivana Cvijović; Benjamin H Good; Elizabeth R Jerison; Michael M Desai
Journal:  Proc Natl Acad Sci U S A       Date:  2015-08-24       Impact factor: 11.205

3.  Gene Duplicability of Core Genes Is Highly Consistent across All Angiosperms.

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Journal:  Plant Cell       Date:  2016-01-07       Impact factor: 11.277

4.  Single nucleotide mapping of trait space reveals Pareto fronts that constrain adaptation.

Authors:  Yuping Li; Dmitri A Petrov; Gavin Sherlock
Journal:  Nat Ecol Evol       Date:  2019-10-14       Impact factor: 15.460

Review 5.  Too much to handle - how gaining chromosomes destabilizes the genome.

Authors:  Verena Passerini; Zuzana Storchová
Journal:  Cell Cycle       Date:  2016-09-16       Impact factor: 4.534

6.  Construction and Optimization of a Heterologous Pathway for Protocatechuate Catabolism in Escherichia coli Enables Bioconversion of Model Aromatic Compounds.

Authors:  Sonya M Clarkson; Richard J Giannone; Donna M Kridelbaugh; James G Elkins; Adam M Guss; Joshua K Michener
Journal:  Appl Environ Microbiol       Date:  2017-08-31       Impact factor: 4.792

Review 7.  The evolutionary significance of polyploidy.

Authors:  Yves Van de Peer; Eshchar Mizrachi; Kathleen Marchal
Journal:  Nat Rev Genet       Date:  2017-05-15       Impact factor: 53.242

8.  Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae.

Authors:  Jing Hou; Anne Friedrich; Jacky de Montigny; Joseph Schacherer
Journal:  Curr Biol       Date:  2014-05-08       Impact factor: 10.834

Review 9.  Aneuploidy, cell delamination and tumorigenesis in Drosophila epithelia.

Authors:  Andrés Dekanty; Marco Milán
Journal:  Cell Cycle       Date:  2013-02-19       Impact factor: 4.534

Review 10.  The functional basis of adaptive evolution in chemostats.

Authors:  David Gresham; Jungeui Hong
Journal:  FEMS Microbiol Rev       Date:  2014-12-04       Impact factor: 16.408

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