Promoter Nucleosome Organization Shapes the Evolution of Gene Expression
Understanding why genes evolve at different rates is fundamental to evolutionary thinking. In species of the budding yeast, the rate at which genes diverge in expression correlates with the organization of their promoter nucleosomes: genes lacking a nucleosome-free region (denoted OPN for “Occupied Proximal Nucleosomes”) vary widely between the species, while the expression of those containing NFR (denoted DPN for “Depleted Proximal Nucleosomes”) remains largely conserved. To examine if early evolutionary dynamics contributes to this difference in divergence, we artificially selected for high expression of GFP–fused proteins. Surprisingly, selection was equally successful for OPN and DPN genes, with ∼80% of genes in each group stably increasing in expression by a similar amount. Notably, the two groups adapted by distinct mechanisms: DPN–selected strains duplicated large genomic regions, while OPN–selected strains favored trans mutations not involving duplications. When selection was removed, DPN (but not OPN) genes reverted rapidly to wild-type expression levels, consistent with their lower diversity between species. Our results suggest that promoter organization constrains the early evolutionary dynamics and in this way biases the path of long-term evolution.
Vyšlo v časopise:
Promoter Nucleosome Organization Shapes the Evolution of Gene Expression. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002579
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002579
Souhrn
Understanding why genes evolve at different rates is fundamental to evolutionary thinking. In species of the budding yeast, the rate at which genes diverge in expression correlates with the organization of their promoter nucleosomes: genes lacking a nucleosome-free region (denoted OPN for “Occupied Proximal Nucleosomes”) vary widely between the species, while the expression of those containing NFR (denoted DPN for “Depleted Proximal Nucleosomes”) remains largely conserved. To examine if early evolutionary dynamics contributes to this difference in divergence, we artificially selected for high expression of GFP–fused proteins. Surprisingly, selection was equally successful for OPN and DPN genes, with ∼80% of genes in each group stably increasing in expression by a similar amount. Notably, the two groups adapted by distinct mechanisms: DPN–selected strains duplicated large genomic regions, while OPN–selected strains favored trans mutations not involving duplications. When selection was removed, DPN (but not OPN) genes reverted rapidly to wild-type expression levels, consistent with their lower diversity between species. Our results suggest that promoter organization constrains the early evolutionary dynamics and in this way biases the path of long-term evolution.
Zdroje
1. BaldwinJM 1896 A New Factor in Evolution. The American Naturalist 30 441 451
2. SimpsonGG 1953 The Baldwin Effect. Evolution 7 110 117
3. WaddingtonCH 1953 The ‘Baldwin Effect’, ‘Genetic Assimilation’ and ‘Homeostasis’. Evolution 7 386 387
4. KirschnerMWGerhartGJ 2005 The Plausibility of Life New Haven, CT Yale Univ Press
5. West-EberhardMJ 2005 Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences of the United States of America 102 6543 6549
6. RutherfordSLLindquistS 1998 Hsp90 as a capacitor for morphological evolution. Nature 396 336 342
7. TawfikDS 2010 Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6 692 696
8. MiloRHouJHSpringerMBrennerMPKirschnerMW 2007 The relationship between evolutionary and physiological variation in hemoglobin. Proceedings of the National Academy of Sciences 104 16998 17003
9. CarrollSB 2000 Endless forms: the evolution of gene regulation and morphological diversity. Cell 101 577 580
10. KingMCWilsonAC 1975 Evolution at two levels in humans and chimpanzees. Science 188 107 116
11. SternDLOrgogozoV 2009 Is genetic evolution predictable? Science 323 746 751
12. WrayGA 2007 The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8 206 216
13. EnardWKhaitovichPKloseJZollnerSHeissigF 2002 Intra- and interspecific variation in primate gene expression patterns. Science 296 340 343
14. KhaitovichPHellmannIEnardWNowickKLeinweberM 2005 Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309 1850 1854
15. RanzJMCastillo-DavisCIMeiklejohnCDHartlDL 2003 Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300 1742 1745
16. RifkinSAKimJWhiteKP 2003 Evolution of gene expression in the Drosophila melanogaster subgroup. Nat Genet 33 138 144
17. SuAIWiltshireTBatalovSLappHChingKA 2004 A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101 6062 6067
18. TiroshIReikhavSLevyAABarkaiN 2009 A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324 659 662
19. TiroshIWeinbergerACarmiMBarkaiN 2006 A genetic signature of interspecies variations in gene expression. Nat Genet 38 830 834
20. TiroshIBarkaiN 2008 Two strategies for gene regulation by promoter nucleosomes. Genome Res 18 1084 1091
21. CairnsBR 2009 The logic of chromatin architecture and remodelling at promoters. Nature 461 193 198
22. TiroshIBarkaiNVerstrepenKJ 2009 Promoter architecture and the evolvability of gene expression. J Biol 8 95
23. LandryCRLemosBRifkinSADickinsonWJHartlDL 2007 Genetic properties influencing the evolvability of gene expression. Science 317 118 121
24. HuhWKFalvoJVGerkeLCCarrollASHowsonRW 2003 Global analysis of protein localization in budding yeast. Nature 425 686 691
25. VincesMDLegendreMCaldaraMHagiharaMVerstrepenKJ 2009 Unstable tandem repeats in promoters confer transcriptional evolvability. Science 324 1213 1216
26. BrownMGarvikBHartwellLKadykLSeeleyT 1991 Fidelity of mitotic chromosome transmission. Cold Spring Harb Symp Quant Biol 56 359 365
27. HartwellLHDutcherSKWoodJSGarvikB 1982 The Fidelity of Mitotic Chromosome Reproduction in S. Cerevisiae. Rec Adv Yeast Mol Biol 1 28 38
28. WittkoppPJHaerumBKClarkAG 2008 Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40 346 350
29. EmersonJJHsiehLCSungHMWangTYHuangCJ 2010 Natural selection on cis and trans regulation in yeasts. Genome Res 20 826 836
30. DunhamMJBadraneHFereaTAdamsJBrownPO 2002 Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 99 16144 16149
31. FereaTLBotsteinDBrownPORosenzweigRF 1999 Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci U S A 96 9721 9726
32. HughesTRRobertsCJDaiHJonesARMeyerMR 2000 Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 25 333 337
33. KoszulRCaburetSDujonBFischerG 2004 Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J 23 234 243
34. TiroshIReikhavSSigalNAssiaYBarkaiN 2010 Chromatin regulators as capacitors of interspecies variations in gene expression. Mol Syst Biol 6 435
35. McManusCJCoolonJDDuffMOEipper-MainsJGraveleyBR 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Research 20 816 825
36. LeeWTilloDBrayNMorseRHDavisRW 2007 A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39 1235 1244
37. KaplanNMooreIKFondufe-MittendorfYGossettAJTilloD 2009 The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458 362 366
38. TsuiKDubuisSGebbiaMMorseRHBarkaiN 2011 Evolution of nucleosome occupancy: conservation of global properties and divergence of gene-specific patterns. Mol Cell Biol 31 4348 4355
39. GietzRDSchiestlRH 2007 High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2 31 34
40. BalkayL FCS data reader for Matlab. http://www.mathworks.com/matlabcentral/fileexchange/9608-fcs-data-reader
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 3
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