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ORFs in Drosophila Are Important to Organismal Fitness and Evolved Rapidly from Previously Non-coding Sequences


How non-coding DNA gives rise to new protein-coding genes (de novo genes) is not well understood. Recent work has revealed the origins and functions of a few de novo genes, but common principles governing the evolution or biological roles of these genes are unknown. To better define these principles, we performed a parallel analysis of the evolution and function of six putatively protein-coding de novo genes described in Drosophila melanogaster. Reconstruction of the transcriptional history of de novo genes shows that two de novo genes emerged from novel long non-coding RNAs that arose at least 5 MY prior to evolution of an open reading frame. In contrast, four other de novo genes evolved a translated open reading frame and transcription within the same evolutionary interval suggesting that nascent open reading frames (proto-ORFs), while not required, can contribute to the emergence of a new de novo gene. However, none of the genes arose from proto-ORFs that existed long before expression evolved. Sequence and structural evolution of de novo genes was rapid compared to nearby genes and the structural complexity of de novo genes steadily increases over evolutionary time. Despite the fact that these genes are transcribed at a higher level in males than females, and are most strongly expressed in testes, RNAi experiments show that most of these genes are essential in both sexes during metamorphosis. This lethality suggests that protein coding de novo genes in Drosophila quickly become functionally important.


Vyšlo v časopise: ORFs in Drosophila Are Important to Organismal Fitness and Evolved Rapidly from Previously Non-coding Sequences. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003860
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003860

Souhrn

How non-coding DNA gives rise to new protein-coding genes (de novo genes) is not well understood. Recent work has revealed the origins and functions of a few de novo genes, but common principles governing the evolution or biological roles of these genes are unknown. To better define these principles, we performed a parallel analysis of the evolution and function of six putatively protein-coding de novo genes described in Drosophila melanogaster. Reconstruction of the transcriptional history of de novo genes shows that two de novo genes emerged from novel long non-coding RNAs that arose at least 5 MY prior to evolution of an open reading frame. In contrast, four other de novo genes evolved a translated open reading frame and transcription within the same evolutionary interval suggesting that nascent open reading frames (proto-ORFs), while not required, can contribute to the emergence of a new de novo gene. However, none of the genes arose from proto-ORFs that existed long before expression evolved. Sequence and structural evolution of de novo genes was rapid compared to nearby genes and the structural complexity of de novo genes steadily increases over evolutionary time. Despite the fact that these genes are transcribed at a higher level in males than females, and are most strongly expressed in testes, RNAi experiments show that most of these genes are essential in both sexes during metamorphosis. This lethality suggests that protein coding de novo genes in Drosophila quickly become functionally important.


Zdroje

1. OhnoS, WolfU, AtkinNB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59: 169–187.

2. Ohno S (1970) Evolution by gene duplication. LondonNew York: Allen & Unwin; Springer-Verlag. 160 p.

3. JacobF (1977) Evolution and tinkering. Science 196: 1161–1166.

4. LevineMT, JonesCD, KernAD, LindforsHA, BegunDJ (2006) Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression. Proceedings of the National Academy of Sciences 103: 9935–9939.

5. BegunDJ (2005) Recently Evolved Genes Identified From Drosophila yakuba and D. erecta Accessory Gland Expressed Sequence Tags. Genetic 172: 1675–1681.

6. BegunDJ, LindforsHA, KernAD, JonesCD (2006) Evidence for de Novo Evolution of Testis-Expressed Genes in the Drosophila yakuba/Drosophila erecta Clade. Genetics 176: 1131–1137.

7. ClarkAG, EisenMB, SmithDR, BergmanCM, OliverB, et al. (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203–218 doi:10.1038/nature06341

8. YandellM (2005) A computational and experimental approach to validating annotations and gene predictions in the Drosophila melanogaster genome. Proceedings of the National Academy of Sciences 102: 1566–1571 doi:10.1073/pnas.0409421102

9. CaiJ, ZhaoR, JiangH, WangW (2008) De Novo Origination of a New Protein-Coding Gene in Saccharomyces cerevisiae. Genetics 179: 487–496.

10. Toll-RieraM, BoschN, BelloraN, CasteloR, ArmengolL, et al. (2008) Origin of Primate Orphan Genes: A Comparative Genomics Approach. Molecular Biology and Evolution 26: 603–612 doi:10.1093/molbev/msn281

11. KnowlesDG, McLysaghtA (2009) Recent de novo origin of human protein-coding genes. Genome Research 109: 1752–1759.

12. XieC, ZhangYE, ChenJ-Y, LiuC-J, ZhouW-Z, et al. (2012) Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs. PLoS Genet 8: e1002942 doi:10.1371/journal.pgen.1002942

13. HeinenTJAJ, StaubachF, HämingD, TautzD (2009) Emergence of a new gene from an intergenic region. Current Biology 19: 1527–1531.

14. CarvunisA-R, RollandT, WapinskiI, CalderwoodMA, YildirimMA, et al. (2012) Proto-genes and de novo gene birth. Nature 487: 370–374 doi:10.1038/nature11184

15. LadoukakisE, PereiraV, MagnyEG, Eyre-WalkerA, CousoJP (2011) Hundreds of putatively functional small open reading frames in Drosophila. Genome Biology 12: R118.

16. LiD, DongY, JiangY, JiangH, CaiJ, et al. (2010) A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand. Cell Research 20: 408–420.

17. ChenS, ZhangYE, LongM (2010) New Genes in Drosophila Quickly Become Essential. Science 330: 1682–1685.

18. Mummery-WidmerJL, YamazakiM, StoegerT, NovatchkovaM, BhaleraoS, et al. (2009) Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 458: 987–992.

19. LiC-Y, ZhangY, WangZ, ZhangY, CaoC, et al. (2010) A human-specific de novo protein-coding gene associated with human brain functions. PLoS computational biology 6: e1000734.

20. ZhouQ, ZhangG, ZhangY, XuS, ZhaoR, et al. (2008) On the origin of new genes in Drosophila. Genome Res 18: 1446–1455 doi:10.1101/gr.076588.108

21. BrunnerE, AhrensCH, MohantyS, BaetschmannH, LoevenichS, et al. (2007) A high-quality catalog of the Drosophila melanogaster proteome. Nature Biotechnology 25: 576–583.

22. VizcainoJA, CoteR, ReisingerF, BarsnesH, FosterJM, et al. (2009) The Proteomics Identifications database: 2010 update. Nucleic Acids Research 38: D736–D742 doi:10.1093/nar/gkp964

23. Toorn HWP vanden, MohammedS, GouwJW, Breukelen Bvan, HeckAJR (2008) Targeted SCX Based Peptide Fractionation for Optimal Sequencing by Collision Induced, and Electron Transfer Dissociation. Journal of Proteomics & Bioinformatics 01: 379–388 doi:10.4172/jpb.1000047

24. Van den ToornHWP, MuñozJ, MohammedS, RaijmakersR, HeckAJR, et al. (2011) RockerBox: Analysis and Filtering of Massive Proteomics Search Results. Journal of Proteome Research 10: 1420–1424 doi:10.1021/pr1010185

25. GraveleyBR, BrooksAN, CarlsonJW, DuffMO, LandolinJM, et al. (2010) The developmental transcriptome of Drosophila melanogaster. Nature 471: 473–479.

26. Blair SS. (2000) Imaginal Discs. In: Drosophila protocols. Sullivan W, Ashburner M, Hawley RS, editors. Cold Spring Harbor Laboratory Press. pp. 159–173.

27. JiangJ, BensonE, BausekN, DoggettK, White-CooperH (2007) Tombola, a tesmin/TSO1-family protein, regulates transcriptional activation in the Drosophila male germline and physically interacts with always early. Development 134: 1549–1559.

28. KaessmannH (2010) Origins, evolution, and phenotypic impact of new genes. Genome Research 20: 1313–1326.

29. DietzlG, ChenD, SchnorrerF, SuK-C, BarinovaY, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151–156.

30. SunS, TingC-T, WuC-I (2004) The normal function of a speciation gene, Odysseus, and its hybrid sterility effect. Science 305: 81–83 doi:10.1126/science.1093904

31. CooperJL, TillBJ, HenikoffS (2008) Fly-TILL: reverse genetics using a living point mutation resource. Fly 2: 300–302.

32. NagyE, MaquatLE (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends in biochemical sciences 23: 198–199.

33. GatfieldD, UnterholznerL, CiccarelliFD, BorkP, IzaurraldeE (2003) Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. The EMBO Journal 22: 3960–3970.

34. LangleyCH, StevensK, CardenoC, LeeYCG, SchriderDR, et al. (2012) Genomic Variation in Natural Populations of Drosophila melanogaster. Genetics 192: 533–598 doi:10.1534/genetics.112.142018

35. HutterS, VilellaAJ, RozasJ (2006) Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinformatics 7: 409.

36. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

37. FuYX, LiWH (1993) Statistical tests of neutrality of mutations. Genetics 133: 693–709.

38. LeeYCG, ReinhardtJA (2012) Widespread polymorphism in the positions of stop codons in Drosophila melanogaster. Genome Biol Evol 4: 533–549 doi:10.1093/gbe/evr113

39. White-CooperH, BausekN (2010) Evolution and spermatogenesis. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 1465–1480 doi:10.1098/rstb.2009.0323

40. KleeneKC (2001) A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 106: 3–23.

41. KleeneKC (2005) Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. Dev Biol 277: 16–26 doi:10.1016/j.ydbio.2004.09.031

42. TautzD, Domazet-LošoT (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692–702 doi:10.1038/nrg3053

43. OrrHA (1998) The Population Genetics of Adaptation: The Distribution of Factors Fixed during Adaptive Evolution. Evolution 52: 935 doi:10.2307/2411226

44. UncklessRL, OrrHA (2009) The Population Genetics of Adaptation: Multiple Substitutions on a Smooth Fitness Landscape. Genetics 183: 1079–1086 doi:10.1534/genetics.109.106757

45. MuraliT, PacificoS, YuJ, GuestS, RobertsGG3rd, et al. (2011) DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucleic Acids Research 39: D736–743.

46. SellaG, PetrovDA, PrzeworskiM, AndolfattoP (2009) Pervasive Natural Selection in the Drosophila Genome? PLoS Genetics 5: e1000495 doi:10.1371/journal.pgen.1000495

47. WrayGA (2007) The evolutionary significance of cis-regulatory mutations. Nature Reviews Genetics 8: 206–216 doi:10.1038/nrg2063

48. ChiaromonteF, YapVB, MillerW (2002) Scoring pairwise genomic sequence alignments. Pacific Symposium on Biocomputing 115–126.

49. FujitaPA, RheadB, ZweigAS, HinrichsAS, KarolchikD, et al. (2010) The UCSC Genome Browser database: update 2011. Nucleic Acids Research 39: D876–D882.

50. TweedieS, AshburnerM, FallsK, LeylandP, McQuiltonP, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37: D555–559 doi:10.1093/nar/gkn788

51. RiceP, LongdenI, BleasbyA (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276–277.

52. DarlingACE, MauB, BlattnerFR, PernaNT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Research 14: 1394–1403.

53. DarlingAE, MauB, PernaNT (2010) progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement. PLoS ONE 5: e11147.

54. StoletzkiN, Eyre-WalkerA (2011) Estimation of the neutrality index. Mol Biol Evol 28: 63–70 doi:10.1093/molbev/msq249

55. McDonaldJH, KreitmanM (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351: 652–654.

56. Korber B, Rodrigo AG, Learn GH (2000) HIV Signature and Sequence Variation Analysis. Computational Analysis of HIV Molecular Sequences, Chapter 4. Dordrecht, Netherlands: Kluwer Academic Publishers. pp. 55–72. Available: http://www.hiv.lanl.gov.

57. ChintapalliVR, WangJ, DowJAT (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nature Genetics 39: 715–720.

58. DainesB, WangH, WangL, LiY, HanY, et al. (2011) The Drosophila melanogaster transcriptome by paired-end RNA sequencing. Genome Research 21: 315–324.

59. ZhaoJ, KlyneG, BensonE, GudmannsdottirE, White-CooperH, et al. (2010) FlyTED: the Drosophila Testis Gene Expression Database. Nucleic Acids Res 38: D710–715 doi:10.1093/nar/gkp1006

60. FindlayGD, YiX, MacCossMJ, SwansonWJ (2008) Proteomics Reveals Novel Drosophila Seminal Fluid Proteins Transferred at Mating. PLoS Biology 6: e178 doi:10.1371/journal.pbio.0060178

61. FindlayGD, MacCossMJ, SwansonWJ (2009) Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res 19: 886–896 doi:10.1101/gr.089391.108

62. DorusS, BusbySA, GerikeU, ShabanowitzJ, HuntDF, et al. (2006) Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat Genet 38: 1440–1445 doi:10.1038/ng1915

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