Sex-Specific Embryonic Gene Expression in Species with Newly Evolved Sex Chromosomes


Sex chromosome dosage differences between females and males are a significant form of natural genetic variation in many species. Like many species with chromosomal sex determination, Drosophila females have two X chromosomes, while males have one X and one Y. Fusions of sex chromosomes with autosomes have occurred along the lineage leading to D. pseudoobscura and D. miranda. The resulting neo-sex chromosomes are gradually evolving the properties of sex chromosomes, and neo-X chromosomes are becoming targets for the molecular mechanisms that compensate for differences in X chromosome dose between sexes. We have previously shown that D. melanogaster possess at least two dosage compensation mechanisms: the well- characterized MSL-mediated dosage compensation active in most somatic tissues, and another system active during early embryogenesis prior to the onset of MSL-mediated dosage compensation. To better understand the developmental constraints on sex chromosome gene expression and evolution, we sequenced mRNA from individual male and female embryos of D. pseudoobscura and D. miranda, from ∼0.5 to 8 hours of development. Autosomal expression levels are highly conserved between these species. But, unlike D. melanogaster, we observe a general lack of dosage compensation in D. pseudoobscura and D. miranda prior to the onset of MSL-mediated dosage compensation. Thus, either there has been a lineage-specific gain or loss in early dosage compensation mechanism(s) or increasing X chromosome dose may strain dosage compensation systems and make them less effective. The extent of female bias on the X chromosomes decreases through developmental time with the establishment of MSL-mediated dosage compensation, but may do so more slowly in D. miranda than D. pseudoobscura. These results also prompt a number of questions about whether species with more sex-linked genes have more sex-specific phenotypes, and how much transcript level variance is tolerable during critical stages of development.


Vyšlo v časopise: Sex-Specific Embryonic Gene Expression in Species with Newly Evolved Sex Chromosomes. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004159
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004159

Souhrn

Sex chromosome dosage differences between females and males are a significant form of natural genetic variation in many species. Like many species with chromosomal sex determination, Drosophila females have two X chromosomes, while males have one X and one Y. Fusions of sex chromosomes with autosomes have occurred along the lineage leading to D. pseudoobscura and D. miranda. The resulting neo-sex chromosomes are gradually evolving the properties of sex chromosomes, and neo-X chromosomes are becoming targets for the molecular mechanisms that compensate for differences in X chromosome dose between sexes. We have previously shown that D. melanogaster possess at least two dosage compensation mechanisms: the well- characterized MSL-mediated dosage compensation active in most somatic tissues, and another system active during early embryogenesis prior to the onset of MSL-mediated dosage compensation. To better understand the developmental constraints on sex chromosome gene expression and evolution, we sequenced mRNA from individual male and female embryos of D. pseudoobscura and D. miranda, from ∼0.5 to 8 hours of development. Autosomal expression levels are highly conserved between these species. But, unlike D. melanogaster, we observe a general lack of dosage compensation in D. pseudoobscura and D. miranda prior to the onset of MSL-mediated dosage compensation. Thus, either there has been a lineage-specific gain or loss in early dosage compensation mechanism(s) or increasing X chromosome dose may strain dosage compensation systems and make them less effective. The extent of female bias on the X chromosomes decreases through developmental time with the establishment of MSL-mediated dosage compensation, but may do so more slowly in D. miranda than D. pseudoobscura. These results also prompt a number of questions about whether species with more sex-linked genes have more sex-specific phenotypes, and how much transcript level variance is tolerable during critical stages of development.


Zdroje

1. CharlesworthB (1996) The evolution of chromosomal sex determination and dosage compensation. Curr Biol 6: 149–162.

2. VicosoB, BachtrogD (2009) Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Res 17: 585–602.

3. StraubT, BeckerPB (2007) Dosage compensation: the beginning and end of generalization. Nat Rev Genet 8: 47–57.

4. StraubT, BeckerPB (2011) Transcription modulation chromosome-wide: universal features and principles of dosage compensation in worms and flies. Curr Opin Genet Dev 21: 147–153.

5. DistecheCM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46: 537–560.

6. ArnoldAP, ItohY, MelamedE (2008) A bird's-eye view of sex chromosome dosage compensation. Annu Rev Genomics Hum Genet 9: 109–127.

7. WolfJB, BrykJ (2011) General lack of global dosage compensation in ZZ/ZW systems? Broadening the perspective with RNA-seq. BMC Genomics 12: 91.

8. GelbartME, KurodaMI (2009) Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136: 1399–1410.

9. GeorgievP, ChlamydasS, AkhtarA (2011) Drosophila dosage compensation: males are from Mars, females are from Venus. Fly (Austin) 5: 147–154.

10. ConradT, AkhtarA (2011) Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat Rev Genet 13: 123–134.

11. ten BoschJR, BenavidesJA, ClineTW (2006) The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133: 1967–1977.

12. Ali-MurthyZ, LottSE, EisenMB, KornbergTB (2013) An essential role for zygotic expression in the pre-cellular Drosophila embryo. PLoS Genet 9: e1003428.

13. RastelliL, RichmanR, KurodaMI (1995) The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev 53: 223–233.

14. FrankeA, DernburgA, BashawGJ, BakerBS (1996) Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development 122: 2751–2760.

15. LottSE, VillaltaJE, SchrothGP, LuoS, TonkinLA, et al. (2011) Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq. PLoS Biol 9: e1000590.

16. BernsteinM, ClineTW (1994) Differential effects of Sex-lethal mutations on dosage compensation early in Drosophila development. Genetics 136: 1051–1061.

17. GergenJP (1987) Dosage Compensation in Drosophila: Evidence That daughterless and Sex-lethal Control X Chromosome Activity at the Blastoderm Stage of Embryogenesis. Genetics 117: 477–485.

18. LucchesiJC (1978) Gene dosage compensation and the evolution of sex chromosomes. Science 202: 711–716.

19. BachtrogD (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14: 113–124.

20. MarinI, FrankeA, BashawGJ, BakerBS (1996) The dosage compensation system of Drosophila is co-opted by newly evolved X chromosomes. Nature 383: 160–163.

21. SturgillD, ZhangY, ParisiM, OliverB (2007) Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 238–241.

22. CarvalhoAB, ClarkAG (2005) Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307: 108–110.

23. DobzhanskyT (1935) Drosophila Miranda, a New Species. Genetics 20: 377–391.

24. BachtrogD, CharlesworthB (2002) Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416: 323–326.

25. SteinemannM, SteinemannS (1998) Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica 102–103: 409–420.

26. SteinemannM, SteinemannS, LottspeichF (1993) How Y chromosomes become genetically inert. Proc Natl Acad Sci U S A 90: 5737–5741.

27. BachtrogD (2003) Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet 34: 215–219.

28. BachtrogD, HomE, WongKM, MasideX, de JongP (2008) Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol 9: R30.

29. KaiserVB, ZhouQ, BachtrogD (2011) Nonrandom gene loss from the Drosophila miranda neo-Y chromosome. Genome Biol Evol 3: 1329–1337.

30. ZhouQ, BachtrogD (2012) Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337: 341–345.

31. BoneJR, KurodaMI (1996) Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila. Genetics 144: 705–713.

32. SteinemannM, SteinemannS, TurnerBM (1996) Evolution of dosage compensation. Chromosome Res 4: 185–190.

33. AlekseyenkoAA, EllisonCE, GorchakovAA, ZhouQ, KaiserVB, et al. (2013) Conservation and de novo acquisition of dosage compensation on newly evolved sex chromosomes in Drosophila. Genes Dev 27: 853–858.

34. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

35. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

36. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511–515.

37. HaddrillPR, ZengK, CharlesworthB (2011) Determinants of synonymous and nonsynonymous variability in three species of Drosophila. Mol Biol Evol 28: 1731–1743.

38. JensenJD, BachtrogD (2011) Characterizing the influence of effective population size on the rate of adaptation: Gillespie's Darwin domain. Genome Biol Evol 3: 687–701.

39. AlekseyenkoAA, PengS, LarschanE, GorchakovAA, LeeOK, et al. (2008) A sequence motif within chromatin entry sites directs MSL establishment on the Drosophila X chromosome. Cell 134: 599–609.

40. StraubT, GrimaudC, GilfillanGD, MitterwegerA, BeckerPB (2008) The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet 4: e1000302.

41. Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, et al.. (2013) The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. arXiv:13097072v1 [q-bioGN].

42. MeiklejohnCD, PresgravesDC (2012) Little evidence for demasculinization of the Drosophila X chromosome among genes expressed in the male germline. Genome Biol Evol 4: 1007–1016.

43. GuptaV, ParisiM, SturgillD, NuttallR, DoctoleroM, et al. (2006) Global analysis of X-chromosome dosage compensation. J Biol 5: 3.

44. MaloneJH, ChoDY, MattiuzzoNR, ArtieriCG, JiangL, et al. (2012) Mediation of Drosophila autosomal dosage effects and compensation by network interactions. Genome Biol 13: r28.

45. StenbergP, LundbergLE, JohanssonAM, RydenP, SvenssonMJ, et al. (2009) Buffering of segmental and chromosomal aneuploidies in Drosophila melanogaster. PLoS Genet 5: e1000465.

46. ZhangY, MaloneJH, PowellSK, PeriwalV, SpanaE, et al. (2010) Expression in aneuploid Drosophila S2 cells. PLoS Biol 8: e1000320.

47. LindsleyDL, SandlerL, BakerBS, CarpenterAT, DenellRE, et al. (1972) Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71: 157–184.

48. McAnallyAA, YampolskyLY (2010) Widespread transcriptional autosomal dosage compensation in Drosophila correlates with gene expression level. Genome Biol Evol 2: 44–52.

49. OliverB (2007) Sex, dose, and equality. PLoS Biol 5: e340.

50. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.

51. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.

52. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498.

53. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.

54. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

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