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Evolutionary Change within a Bipotential Switch Shaped the Sperm/Oocyte Decision in Hermaphroditic Nematodes


A subset of transcription factors like Gli2 and Oct1 are bipotential — they can activate or repress the same target, in response to changing signals from upstream genes. Some previous studies implied that the sex-determination protein TRA-1 might also be bipotential; here we confirm this hypothesis by identifying a co-factor, and use it to explore how the structure of a bipotential switch changes during evolution. First, null mutants reveal that C. briggsae TRR-1 is required for spermatogenesis, RNA interference implies that it works as part of the Tip60 Histone Acetyl Transferase complex, and RT-PCR data show that it promotes the expression of Cbr-fog-3, a gene needed for spermatogenesis. Second, epistasis tests reveal that TRR-1 works through TRA-1, both to activate Cbr-fog-3 and to control the sperm/oocyte decision. Since previous studies showed that TRA-1 can repress fog-3 as well, these observations demonstrate that it is bipotential. Third, TRR-1 also regulates the development of the male tail. Since Cbr-tra-2 Cbr-trr-1 double mutants resemble Cbr-tra-1 null mutants, these two regulatory branches control all tra-1 activity. Fourth, striking differences in the relationship between these two branches of the switch have arisen during recent evolution. C. briggsae trr-1 null mutants prevent hermaphrodite spermatogenesis, but not Cbr-fem null mutants, which disrupt the other half of the switch. On the other hand, C. elegans fem null mutants prevent spermatogenesis, but not Cel-trr-1 mutants. However, synthetic interactions confirm that both halves of the switch exist in each species. Thus, the relationship between the two halves of a bipotential switch can shift rapidly during evolution, so that the same phenotype is produce by alternative, complementary mechanisms.


Vyšlo v časopise: Evolutionary Change within a Bipotential Switch Shaped the Sperm/Oocyte Decision in Hermaphroditic Nematodes. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003850
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003850

Souhrn

A subset of transcription factors like Gli2 and Oct1 are bipotential — they can activate or repress the same target, in response to changing signals from upstream genes. Some previous studies implied that the sex-determination protein TRA-1 might also be bipotential; here we confirm this hypothesis by identifying a co-factor, and use it to explore how the structure of a bipotential switch changes during evolution. First, null mutants reveal that C. briggsae TRR-1 is required for spermatogenesis, RNA interference implies that it works as part of the Tip60 Histone Acetyl Transferase complex, and RT-PCR data show that it promotes the expression of Cbr-fog-3, a gene needed for spermatogenesis. Second, epistasis tests reveal that TRR-1 works through TRA-1, both to activate Cbr-fog-3 and to control the sperm/oocyte decision. Since previous studies showed that TRA-1 can repress fog-3 as well, these observations demonstrate that it is bipotential. Third, TRR-1 also regulates the development of the male tail. Since Cbr-tra-2 Cbr-trr-1 double mutants resemble Cbr-tra-1 null mutants, these two regulatory branches control all tra-1 activity. Fourth, striking differences in the relationship between these two branches of the switch have arisen during recent evolution. C. briggsae trr-1 null mutants prevent hermaphrodite spermatogenesis, but not Cbr-fem null mutants, which disrupt the other half of the switch. On the other hand, C. elegans fem null mutants prevent spermatogenesis, but not Cel-trr-1 mutants. However, synthetic interactions confirm that both halves of the switch exist in each species. Thus, the relationship between the two halves of a bipotential switch can shift rapidly during evolution, so that the same phenotype is produce by alternative, complementary mechanisms.


Zdroje

1. Zarkower D (2006) Somatic sex determination. In: Community TCeR, editor. Wormbook.

2. Ellis RE, Schedl T (2006) Sex-determination in the germ line. In: Community TCeR, editor. Wormbook.

3. EllisRE (2008) Chapter 2 Sex Determination in the Caenorhabditis elegans Germ Line. Curr Top Dev Biol 83: 41–64.

4. ChenPJ, EllisRE (2000) TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans. Development 127: 3119–3129.

5. ConradtB, HorvitzHR (1999) The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98: 317–327.

6. YiW, RossJM, ZarkowerD (2000) mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior. Development 127: 4469–4480.

7. StarostinaNG, LimJM, SchvarzsteinM, WellsL, SpenceAM, et al. (2007) A CUL-2 Ubiquitin Ligase Containing Three FEM Proteins Degrades TRA-1 to Regulate C. elegans Sex Determination. Dev Cell 13: 127–139.

8. ZarkowerD, HodgkinJ (1992) Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins. Cell 70: 237–249.

9. JiangJ (2006) Regulation of Hh/Gli signaling by dual ubiquitin pathways. Cell Cycle 5: 2457–2463.

10. AlexandreC, JacintoA, InghamPW (1996) Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev 10: 2003–2013.

11. MullerB, BaslerK (2000) The repressor and activator forms of Cubitus interruptus control Hedgehog target genes through common generic gli-binding sites. Development 127: 2999–3007.

12. Ruiz i AltabaA (1999) Gli proteins encode context-dependent positive and negative functions: implications for development and disease. Development 126: 3205–3216.

13. KoebernickK, PielerT (2002) Gli-type zinc finger proteins as bipotential transducers of Hedgehog signaling. Differentiation 70: 69–76.

14. SchvarzsteinM, SpenceAM (2006) The C. elegans sex-determining GLI protein TRA-1A is regulated by sex-specific proteolysis. Dev Cell 11: 733–740.

15. SchedlT, GrahamPL, BartonMK, KimbleJ (1989) Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans. Genetics 123: 755–769.

16. HodgkinJ (1987) A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans. Genes Dev 1: 731–745.

17. GuoY, LangS, EllisRE (2009) Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution. Curr Biol 19: 1853–1860.

18. ChoS, JinSW, CohenA, EllisRE (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14: 1207–1220.

19. KiontkeK, GavinNP, RaynesY, RoehrigC, PianoF, et al. (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci U S A 101: 9003–9008.

20. KiontkeKC, FelixMA, AilionM, RockmanMV, BraendleC, et al. (2011) A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11: 339.

21. BaldiC, ChoS, EllisRE (2009) Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326: 1002–1005.

22. HillRC, de CarvalhoCE, SalogiannisJ, SchlagerB, PilgrimD, et al. (2006) Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. Dev Cell 10: 531–538.

23. BartonMK, KimbleJ (1990) fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125: 29–39.

24. SchedlT, KimbleJ (1988) fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 119: 43–61.

25. EllisRE, KimbleJ (1995) The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139: 561–577.

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

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

28. MurrR, VaissiereT, SawanC, ShuklaV, HercegZ (2007) Orchestration of chromatin-based processes: mind the TRRAP. Oncogene 26: 5358–5372.

29. CeolCJ, HorvitzHR (2004) A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev Cell 6: 563–576.

30. KelleherDF, de CarvalhoCE, DotyAV, LaytonM, ChengAT, et al. (2008) Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae. Genetics 178: 1415–1429.

31. PilgrimD, McGregorA, JackleP, JohnsonT, HansenD (1995) The C. elegans sex-determining gene fem-2 encodes a putative protein phosphatase. Mol Biol Cell 6: 1159–1171.

32. HansenD, PilgrimD (1998) Molecular evolution of a sex determination protein. FEM-2 (pp2c) in Caenorhabditis. Genetics 149: 1353–1362.

33. PieknyAJ, WissmannA, MainsPE (2000) Embryonic morphogenesis in Caenorhabditis elegans integrates the activity of LET-502 Rho-binding kinase, MEL-11 myosin phosphatase, DAF-2 insulin receptor and FEM-2 PP2c phosphatase. Genetics 156: 1671–1689.

34. ChenPJ, ChoS, JinSW, EllisRE (2001) Specification of germ cell fates by FOG-3 has been conserved during nematode evolution. Genetics 158: 1513–1525.

35. HodgkinJA, BrennerS (1977) Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86: 275–287.

36. Prud'hommeB, GompelN, RokasA, KassnerVA, WilliamsTM, et al. (2006) Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440: 1050–1053.

37. WilliamsTM, SelegueJE, WernerT, GompelN, KoppA, et al. (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134: 610–623.

38. SeetharamanA, CumboP, BojanalaN, GuptaBP (2010) Conserved mechanism of Wnt signaling function in the specification of vulval precursor fates in C. elegans and C. briggsae. Dev Biol 346: 128–139.

39. BeadellAV, LiuQ, JohnsonDM, HaagES (2011) Independent recruitments of a translational regulator in the evolution of self-fertile nematodes. Proc Natl Acad Sci U S A 108: 19672–19677.

40. Pires-daSilvaA, SommerRJ (2004) Conservation of the global sex determination gene tra-1 in distantly related nematodes. Genes Dev 18: 1198–1208.

41. LumDH, KuwabaraPE, ZarkowerD, SpenceAM (2000) Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans. Genes Dev 14: 3153–3165.

42. ZarkowerD, De BonoM, AronoffR, HodgkinJ (1994) Regulatory rearrangements and smg-sensitive alleles of the C. elegans sex-determining gene tra-1. Dev Genet 15: 240–250.

43. HodgkinJ (1993) Molecular cloning and duplication of the nematode sex-determining gene tra-1. Genetics 133: 543–560.

44. AkimaruH, ChenY, DaiP, HouDX, NonakaM, et al. (1997) Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386: 735–738.

45. ZhouH, KimS, IshiiS, BoyerTG (2006) Mediator modulates Gli3-dependent Sonic hedgehog signaling. Mol Cell Biol 26: 8667–8682.

46. GroteP, ConradtB (2006) The PLZF-like protein TRA-4 cooperates with the Gli-like transcription factor TRA-1 to promote female development in C. elegans. Dev Cell 11: 561–573.

47. SzaboE, HargitaiB, RegosA, TihanyiB, BarnaJ, et al. (2009) TRA-1/GLI controls the expression of the Hox gene lin-39 during C. elegans vulval development. Dev Biol 330: 339–348.

48. CuiM, HanM (2007) Roles of chromatin factors in C. elegans development. WormBook 1–16.

49. DuveauF, FelixMA (2012) Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans. PLoS Biol 10: e1001230.

50. LiuT, RechtsteinerA, EgelhoferTA, VielleA, LatorreI, et al. (2011) Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 21: 227–236.

51. CanettieriG, Di MarcotullioL, GrecoA, ConiS, AntonucciL, et al. (2010) Histone deacetylase and Cullin3-REN(KCTD11) ubiquitin ligase interplay regulates Hedgehog signalling through Gli acetylation. Nat Cell Biol 12: 132–142.

52. TrueJR, HaagES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109–119.

53. ChandlerCH (2010) Cryptic intraspecific variation in sex determination in Caenorhabditis elegans revealed by mutations. Heredity (Edinb) 105: 473–482.

54. MillozJ, DuveauF, NuezI, FelixMA (2008) Intraspecific evolution of the intercellular signaling network underlying a robust developmental system. Genes Dev 22: 3064–3075.

55. TianH, SchlagerB, XiaoH, SommerRJ (2008) Wnt signaling induces vulva development in the nematode Pristionchus pacificus. Curr Biol 18: 142–146.

56. WangX, SommerRJ (2011) Antagonism of LIN-17/Frizzled and LIN-18/Ryk in nematode vulva induction reveals evolutionary alterations in core developmental pathways. PLoS Biol 9: e1001110.

57. HodgkinJ (1986) Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114: 15–52.

58. HillRC, HaagES (2009) A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway. Evol Dev 11: 333–342.

59. HaagES, AckermanAD (2005) Intraspecific variation in fem-3 and tra-2, two rapidly coevolving nematode sex-determining genes. Gene 349: 35–42.

60. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

61. YandellMD, EdgarLG, WoodWB (1994) Trimethylpsoralen induces small deletion mutations in Caenorhabditis elegans. Proc Natl Acad Sci U S A 91: 1381–1385.

62. KoboldtDC, StaischJ, ThillainathanB, HainesK, BairdSE, et al. (2010) A toolkit for rapid gene mapping in the nematode Caenorhabditis briggsae. BMC Genomics 11: 236.

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