Comparative RNAi Screens in and Reveal the Impact of Developmental System Drift on Gene Function

English version České info

Although two related species may have extremely similar phenotypes, the genetic networks underpinning this conserved biology may have diverged substantially since they last shared a common ancestor. This is termed Developmental System Drift (DSD) and reflects the plasticity of genetic networks. One consequence of DSD is that some orthologous genes will have evolved different in vivo functions in two such phenotypically similar, related species and will therefore have different loss of function phenotypes. Here we report an RNAi screen in C. elegans and C. briggsae to identify such cases. We screened 1333 genes in both species and identified 91 orthologues that have different RNAi phenotypes. Intriguingly, we find that recently evolved genes of unknown function have the fastest evolving in vivo functions and, in several cases, we identify the molecular events driving these changes. We thus find that DSD has a major impact on the evolution of gene function and we anticipate that the C. briggsae RNAi library reported here will drive future studies on comparative functional genomics screens in these nematodes.

Vyšlo v časopise: Comparative RNAi Screens in and Reveal the Impact of Developmental System Drift on Gene Function. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004077
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004077

Souhrn

Zdroje

1. LanderES, LintonLM, BirrenB, NusbaumC, ZodyMC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.

2. WangX, ChamberlinHM (2004) Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nature genetics 36: 231–232.

3. GompelN, Prud'hommeB, WittkoppPJ, KassnerVa, CarrollSB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481–487.

4. ChanYF, MarksME, JonesFC, VillarrealG, ShapiroMD, et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science (New York, NY) 327: 302–305.

5. TrueJR, HaagES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evolution & development 3: 109–119.

6. FelixMA, DuveauF (2012) Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biol 10: 59.

7. ZhaoZ, BoyleTJ, BaoZ, MurrayJI, MericleB, et al. (2008) Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Developmental biology 314: 93–99.

8. CutterAD (2008) Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol Biol Evol 25: 778–786.

9. SteinLD, BaoZ, BlasiarD, BlumenthalT, BrentMR, et al. (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS biology 1: E45.

10. BairdSE, SutherlinME, EmmonsSW (1992) Reproductive Isolation in Rhabditidae (Nematoda: Secernentea); Mechanisms That Isolate Six Species of Three Genera. Evolution 46: 585–594.

11. ZhaoZ, FlibotteS, MurrayJI, BlickD, BoyleTJ, et al. (2010) New tools for investigating the comparative biology of Caenorhabditis briggsae and C. elegans. Genetics 184: 853–863.

12. LinKT, Broitman-MaduroG, HungWW, CervantesS, MaduroMF (2009) Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans. Dev Biol 325: 296–306.

13. FraseraG, KamathRS, ZipperlenP, Martinez-CamposM, SohrmannM, et al. (2000) Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325–330.

14. KamathRS, FraserAG, DongY, PoulinG, DurbinR, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231–237.

15. SonnichsenB, KoskiLB, WalshA, MarschallP, NeumannB, et al. (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462–469.

16. GonczyP, EcheverriC, OegemaK, CoulsonA, JonesSJ, et al. (2000) Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408: 331–336.

17. FireA, XuS, MontgomeryMK, KostasSA, DriverSE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.

18. TimmonsL, FireA (1998) Specific interference by ingested dsRNA. Nature 395: 854.

19. KamathR, Martinez-CamposM (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: 1–10.

20. BerglundAC, SjolundE, OstlundG, SonnhammerEL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36: D263–266.

21. KuzniarA, van HamRC, PongorS, LeunissenJA (2008) The quest for orthologs: finding the corresponding gene across genomes. Trends Genet 24: 539–551.

22. LiH, CoghlanA, RuanJ, CoinLJ, HericheJK, et al. (2006) TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res 34: D572–580.

23. WinstonWM, SutherlinM, WrightAJ, FeinbergEH, HunterCP (2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proceedings of the National Academy of Sciences of the United States of America 104: 10565–10570.

24. NuezI, FélixM-A (2012) Evolution of Susceptibility to Ingested Double-Stranded RNAs in Caenorhabditis Nematodes. PLoS ONE 7: e29811.

25. WinstonWM, MolodowitchC, HunterCP (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science 295: 2456–2459.

26. TischlerJ, LehnerB, ChenN, FraserAG (2006) Combinatorial RNA interference in Caenorhabditis elegans reveals that redundancy between gene duplicates can be maintained for more than 80 million years of evolution. Genome Biology 7: 1–13.

27. TsongAE, TuchBB, LiH, JohnsonAD (2006) Evolution of alternative transcriptional circuits with identical logic. Nature 443: 415–420.

28. Domazet-LosoT, BrajkovicJ, TautzD (2007) A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends Genet 23: 533–539.

29. DaiH, ChenY, ChenS, MaoQ, KennedyD, et al. (2008) The evolution of courtship behaviors through the origination of a new gene in Drosophila. Proc Natl Acad Sci U S A 105: 7478–7483.

30. HobertO (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. BioTechniques 32: 728–730.

31. BeadellAV, LiuQ, JohnsonDM, HaagES (2011) Independent recruitments of a translational regulator in the evolution of self-fertile nematodes. Proceedings of the National Academy of Sciences of the United States of America 108: 1–6.

32. LiuQ, StumpfC, ThomasC, WickensM, HaagES (2012) Context-dependent function of a conserved translational regulatory module. Development 139: 1509–1521.

33. BarriereA, GordonKL, RuvinskyI (2011) Distinct functional constraints partition sequence conservation in a cis-regulatory element. PLoS Genet 7: e1002095.

34. BarriereA, GordonKL, RuvinskyI (2012) Coevolution within and between regulatory loci can preserve promoter function despite evolutionary rate acceleration. PLoS Genet 8: e1002961.

35. PetersK, McDowallJ, RoseAM (1991) Mutations in the bli-4 (I) locus of Caenorhabditis elegans disrupt both adult cuticle and early larval development. Genetics 129: 95–102.

36. PageAP, McCormackG, BirnieAJ (2006) Biosynthesis and enzymology of the Caenorhabditis elegans cuticle: identification and characterization of a novel serine protease inhibitor. International journal for parasitology 36: 681–689.

37. LongmanD, McGarveyT, McCrackenS, JohnstoneIL, BlencoweBJ, et al. (2001) Multiple interactions between SRm160 and SR family proteins in enhancer-dependent splicing and development of C. elegans. Curr Biol 11: 1923–1933.

38. KawanoT, FujitaM, SakamotoH (2000) Unique and redundant functions of SR proteins, a conserved family of splicing factors, in Caenorhabditis elegans development. Mech Dev 95: 67–76.

39. FelixMA (2007) Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis. Curr Biol 17: 103–114.

40. PenigaultJB, FelixMA (2011) Evolution of a system sensitive to stochastic noise: P3.p cell fate in Caenorhabditis. Dev Biol 357: 419–427.

41. HoyosE, KimK, MillozJ, BarkoulasM, PenigaultJB, et al. (2011) Quantitative variation in autocrine signaling and pathway crosstalk in the Caenorhabditis vulval network. Curr Biol 21: 527–538.

42. BakerCR, BoothLN, SorrellsTR, JohnsonAD (2012) Protein modularity, cooperative binding, and hybrid regulatory states underlie transcriptional network diversification. Cell 151: 80–95.

43. CliffordR, LeeMH, NayakS, OhmachiM, GiorginiF, et al. (2000) FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127: 5265–5276.

44. NayakS, GoreeJ, SchedlT (2005) fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis. PLoS Biol 3: e6.

45. GuoY, LangS, EllisRE (2009) Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Current biology : CB 19: 1853–1860.

46. HittingerCT, CarrollSB (2007) Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449: 677–681.

47. FontanaW, SchusterP (1998) Continuity in evolution: on the nature of transitions. Science 280: 1451–1455.

48. SchusterP, FontanaW (1999) Chance and necessity in evolution: lessons from RNA. Physica D: Nonlinear Phenomena 133: 427–452.

49. PfafflMW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic acids research 29: e45.

50. HarrisTW, AntoshechkinI, BieriT, BlasiarD, ChanJ, et al. (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 38: D463–467.

51. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.

52. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.