Phylogenomic Analysis Reveals Dynamic Evolutionary History of the Drosophila Heterochromatin Protein 1 (HP1) Gene Family
Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin.
Vyšlo v časopise:
Phylogenomic Analysis Reveals Dynamic Evolutionary History of the Drosophila Heterochromatin Protein 1 (HP1) Gene Family. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002729
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002729
Souhrn
Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin.
Zdroje
1. KellisMPattersonNEndrizziMBirrenBLanderES 2003 Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423 241 254
2. ClarkAGEisenMBSmithDRBergmanCMOliverB 2007 Evolution of genes and genomes on the Drosophila phylogeny. Nature 450 203 218
3. SmithCDShuSMungallCJKarpenGH 2007 The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316 1586 1591
4. MoritzKBRothGE 1976 Complexity of germline and somatic DNA in Ascaris. Nature 259 55 57
5. VermaakDBayesJJMalikHS 2009 A surrogate approach to study the evolution of noncoding DNA elements that organize eukaryotic genomes. J Hered 100 624 636
6. WangGMaAChowCMHorsleyDBrownNR 2000 Conservation of heterochromatin protein 1 function. Mol Cell Biol 20 6970 6983
7. CenciGCiapponiLGattiM 2005 The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 114 135 145
8. RongYS 2008 Telomere capping in Drosophila: dealing with chromosome ends that most resemble DNA breaks. Chromosoma 117 235 242
9. KlattenhoffCXiHLiCLeeSXuJ 2009 The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138 1137 1149
10. BayesJJMalikHS 2009 Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326 1538 1541
11. BrideauNJFloresHAWangJMaheshwariSWangX 2006 Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 1292 1295
12. KellumRAlbertsBM 1995 Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J Cell Sci 108 ( Pt 4) 1419 1431
13. VolpeAMHorowitzHGraferCMJacksonSMBergCA 2001 Drosophila rhino encodes a female-specific chromo-domain protein that affects chromosome structure and egg polarity. Genetics 159 1117 1134
14. VermaakDHenikoffSMalikHS 2005 Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila. PLoS Genet doi:10.1371/journal.pgen.0010009
15. LomberkGWallrathLUrrutiaR 2006 The Heterochromatin Protein 1 family. Genome Biol 7 228
16. SmothersJFHenikoffS 2001 The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins. Mol Cell Biol 21 2555 2569
17. EisenJA 1998 Phylogenomics: improving functional predictions for uncharacterized genes by evolutionary analysis. Genome Res 8 163 167
18. JamesTCElginSC 1986 Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6 3862 3872
19. JamesTCEissenbergJCCraigCDietrichVHobsonA 1989 Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol 50 170 180
20. ParoRHognessDS 1991 The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A 88 263 267
21. AaslandRStewartAF 1995 The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucleic Acids Res 23 3168 3173
22. BannisterAJZegermanPPartridgeJFMiskaEAThomasJO 2001 Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 120 124
23. SmothersJFHenikoffS 2000 The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr Biol 10 27 30
24. MeehanRRKaoCFPenningsS 2003 HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain. EMBO J 22 3164 3174
25. MuchardtCGuillemeMSeelerJSTroucheDDejeanA 2002 Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1alpha. EMBO Rep 3 975 981
26. LozovskayaERNurminskyDIPetrovDAHartlDL 1999 Genome size as a mutation-selection-drift process. Genes Genet Syst 74 201 207
27. VermaakDMalikHS 2009 Multiple roles for heterochromatin protein 1 genes in Drosophila. Annu Rev Genet 43 467 492
28. SwansonWJVacquierVD 2002 The rapid evolution of reproductive proteins. Nat Rev Genet 3 137 144
29. MeiklejohnCDParschJRanzJMHartlDL 2003 Rapid evolution of male-biased gene expression in Drosophila. Proc Natl Acad Sci U S A 100 9894 9899
30. ChenSZhangYELongM 2010 New genes in Drosophila quickly become essential. Science 330 1682 1685
31. VishnoiAKryazhimskiySBazykinGAHannenhalliSPlotkinJB 2010 Young proteins experience more variable selection pressures than old proteins. Genome Res 20 1574 1581
32. ShieldsDCSharpPMHigginsDGWrightF 1988 “Silent” sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5 704 716
33. Langley CH, Stevens K, Cardeno C, Lee YCG, Schrider DR, et al. (In Review) Genomic variation in natural populations of Drosophila melanogaster
34. DemuthJPDe BieTStajichJECristianiniNHahnMW 2006 The evolution of mammalian gene families. PLoS ONE 1 doi:10.1371/journal.pone.0000085 e85
35. YasuharaJCWakimotoBT 2006 Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet 22 330 338
36. BoscoGCampbellPLeiva-NetoJTMarkowTA 2007 Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177 1277 1290
37. SchaefferSWBhutkarAMcAllisterBFMatsudaMMatzkinLM 2008 Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 179 1601 1655
38. LarracuenteAMNoorMAClarkAG 2010 Translocation of Y-linked genes to the dot chromosome in Drosophila pseudoobscura. Mol Biol Evol 27 1612 1620
39. WhiteMJD 1973 Animal Cytology and Evolution. Cambridge: Cambridge University Press
40. CarvalhoABClarkAG 2005 Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307 108 110
41. MaloneCDBrenneckeJDusMStarkAMcCombieWR 2009 Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137 522 535
42. AdamsMDCelnikerSEHoltRAEvansCAGocayneJD 2000 The genome sequence of Drosophila melanogaster. Science 287 2185 2195
43. LachnerMO'CarrollDReaSMechtlerKJenuweinT 2001 Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 116 120
44. FilionGJvan BemmelJGBraunschweigUTalhoutWKindJ 2010 Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143 212 224
45. GallachMChandrasekaranCBetranE 2010 Analyses of nuclearly encoded mitochondrial genes suggest gene duplication as a mechanism for resolving intralocus sexually antagonistic conflict in Drosophila. Genome Biol Evol 2 835 850
46. KusanoAStaberCGanetzkyB 2002 Segregation distortion induced by wild-type RanGAP in Drosophila. Proc Natl Acad Sci U S A 99 6866 6870
47. PhadnisNHsiehEMalikHS 2011 Birth, death and replacement of karyopherins in Drosophila. Mol Biol Evol
48. HuisingaKLElginSC 2009 Small RNA-directed heterochromatin formation in the context of development: what flies might learn from fission yeast. Biochim Biophys Acta 1789 3 16
49. BriscoeAJrTomkielJE 2000 Chromosomal position effects reveal different cis-acting requirements for rDNA transcription and sex chromosome pairing in Drosophila melanogaster. Genetics 155 1195 1211
50. HoltzmanSMillerDEismanRKuwayamaHNiimiT 2010 Transgenic tools for members of the genus Drosophila with sequenced genomes. Fly (Austin) 4 349 362
51. HornCSchmidBGPogodaFSWimmerEA 2002 Fluorescent transformation markers for insect transgenesis. Insect Biochem Mol Biol 32 1221 1235
52. AltschulSFGishWMillerWMyersEWLipmanDJ 1990 Basic local alignment search tool. J Mol Biol 215 403 410
53. EissenbergJC 2001 Molecular biology of the chromo domain: an ancient chromatin module comes of age. Gene 275 19 29
54. GreilFde WitEBussemakerHJvan SteenselB 2007 HP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila. EMBO J 26 741 751
55. DohenyJGMottusRGrigliattiTA 2008 Telomeric position effect–a third silencing mechanism in eukaryotes. PLoS ONE 3 doi:10.1371/journal.pone.0003864 e3864
56. JoppichCScholzSKorgeGSchwendemannA 2009 Umbrea, a chromo shadow domain protein in Drosophila melanogaster heterochromatin, interacts with Hip, HP1 and HOAP. Chromosome Res 17 19 36
57. DrummondAJRambautA 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 214
58. DrummondAJHoSYPhillipsMJRambautA 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 doi:10.1371/journal.pbio.0040088 e88
59. ShapiroBRambautADrummondAJ 2006 Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23 7 9
60. BegunDJHollowayAKStevensKHillierLWPohYP 2007 Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5 doi:10.1371/journal.pbio.0050310 e310
61. NeiM 1987 Molecular evolutionary genetics. New York: Columbia University Press
62. WrightF 1990 The ‘effective number of codons’ used in a gene. Gene 87 23 29
63. LibradoPRozasJ 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 1451 1452
64. YangZ 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591
65. McDonaldJHKreitmanM 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 652 654
66. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
67. Prud'hommeBGompelNRokasAKassnerVAWilliamsTM 2006 Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440 1050 1053
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 6
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