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An Essential Role for Zygotic Expression in the Pre-Cellular Drosophila Embryo
The Drosophila embryo proceeds through thirteen mitotic divisions as a syncytium. Its nuclei distribute in the embryo's interior during the first six divisions, dividing synchronously with a cycle time of less than ten minutes. After seven divisions (nuclear cycle 8), the syncytial blastoderm forms as the nuclei approach the embryo surface and slow their cycle time; subsequent divisions proceed in waves that initiate at the poles. Because genetic studies have not identified zygotic mutants that affect the early divisions and because transcription has not been detected before cycle 8, the early, pre-blastoderm embryo has been considered to rely entirely on maternal contributions and to be transcriptionally silent. Our studies identified several abnormal phenotypes in live engrailed (en) mutant embryos prior to cycle 8, as well as a small group of genes that are transcribed in embryos prior to cycle 7. Nuclei in en embryos divide asynchronously, an abnormality that was detected as early as nuclear cycle 2–3. Anti-En antibody detected nuclear En protein in embryos at cycle 2, and expression of an En:GFP fusion protein encoded in the paternal genome was also detected in cycle 2 nuclei. These findings demonstrate that the Drosophila embryo is functionally competent for gene expression prior to the onset of its rapid nuclear divisions and that the embryo requires functions that are expressed in the zygote in order to faithfully prosecute its early, pre-cellularization mitotic cycles.
Vyšlo v časopise: An Essential Role for Zygotic Expression in the Pre-Cellular Drosophila Embryo. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003428
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003428Souhrn
The Drosophila embryo proceeds through thirteen mitotic divisions as a syncytium. Its nuclei distribute in the embryo's interior during the first six divisions, dividing synchronously with a cycle time of less than ten minutes. After seven divisions (nuclear cycle 8), the syncytial blastoderm forms as the nuclei approach the embryo surface and slow their cycle time; subsequent divisions proceed in waves that initiate at the poles. Because genetic studies have not identified zygotic mutants that affect the early divisions and because transcription has not been detected before cycle 8, the early, pre-blastoderm embryo has been considered to rely entirely on maternal contributions and to be transcriptionally silent. Our studies identified several abnormal phenotypes in live engrailed (en) mutant embryos prior to cycle 8, as well as a small group of genes that are transcribed in embryos prior to cycle 7. Nuclei in en embryos divide asynchronously, an abnormality that was detected as early as nuclear cycle 2–3. Anti-En antibody detected nuclear En protein in embryos at cycle 2, and expression of an En:GFP fusion protein encoded in the paternal genome was also detected in cycle 2 nuclei. These findings demonstrate that the Drosophila embryo is functionally competent for gene expression prior to the onset of its rapid nuclear divisions and that the embryo requires functions that are expressed in the zygote in order to faithfully prosecute its early, pre-cellularization mitotic cycles.
Zdroje
1. PritchardDK, SchubigerG (1996) Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev 10 : 1131–1142.
2. ten BoschJR, BenavidesJA, ClineTW (2006) The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133 : 1967–1977.
3. AndersonKV, LengyelJA (1981) Changing rates of DNA and RNA synthesis in Drosophila embryos. Dev Biol 82 : 127–138.
4. EdgarBA, SchubigerG (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44 : 871–877.
5. ZalokarM (1976) Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol 49 : 425–437.
6. De RenzisS, ElementoO, TavazoieS, WieschausEF (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5: e117–e117 doi:10.1371/journal.pbio.0050117.
7. HarrisonMM, BotchanMR, ClineTW (2010) Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes. Dev Biol 345 : 248–255.
8. EricksonJW, ClineTW (1998) Key aspects of the primary sex determination mechanism are conserved across the genus Drosophila. Development 125 : 3259–3268.
9. KarrTL, AliZ, DreesB, KornbergT (1985) The engrailed locus of D. melanogaster provides an essential zygotic function in precellular embryos. Cell 43 : 591–601.
10. JiJY, SquirrellJM, SchubigerG (2004) Both cyclin B levels and DNA-replication checkpoint control the early embryonic mitoses in Drosophila. Development 131 : 401–411.
11. FoeVE, AlbertsBM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61 : 31–70.
12. SchupbachT, WieschausE (1989) Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121 : 101–117.
13. MerrillPT, SweetonD, WieschausE (1988) Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104 : 495–509.
14. WieschausE, SweetonD (1988) Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development 104 : 483–493.
15. KaneDA, KimmelCB (1993) The zebrafish midblastula transition. Development 119 : 447–456.
16. NewportJ, KirschnerM (1982) A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30 : 675–686.
17. RinaldiAM, MonroyA (1969) Polyribosome formation and RNA synthesis in the early post-fertilization stages of the sea urchin egg. Dev Biol 19 : 73–86.
18. BrownDD (1964) RNA Synthesis during Amphibian Development. J Exp Zool 157 : 101–117.
19. NakakuraN, MiuraT, YamanaK, ItoA, ShiokawaK (1987) Synthesis of heterogeneous mRNA-like RNA and low-molecular-weight RNA before the midblastula transition in embryos of Xenopus laevis. Dev Biol 123 : 421–429.
20. YangJ, TanC, DarkenRS, WilsonPA, KleinPS (2002) Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129 : 5743–5752.
21. MathavanS, LeeSG, MakA, MillerLD, MurthyKR, et al. (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1: e29 doi:10.1371/journal.pgen.0010029.
22. SchenkelH, SchnetterW (1979) Transcription During Early Embryogenesis of Leptinotarasa (Coleoptera). W Roux's Archiv 186 : 179–188.
23. GustavsonE, GoldsboroughAS, AliZ, KornbergTB (1996) The Drosophila engrailed and invected genes: partners in regulation, expression and function. Genetics 142 : 893–906.
24. RoyouA, FieldC, SissonJC, SullivanW, KaressR (2004) Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol Biol Cell 15 : 838–850.
25. MackayTF, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482 : 173–178.
26. 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 doi:10.1371/journal.pbio.1000590.
27. EricksonJW, ClineTW (1993) A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev 7 : 1688–1702.
28. HamataniT, CarterMG, SharovAA, KoMS (2004) Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 6 : 117–131.
29. WieschausE (1996) Embryonic transcription and the control of developmental pathways. Genetics 142 : 5–10.
30. KunerJM, NakanishiM, AliZ, DreesB, GustavsonE, et al. (1985) Molecular cloning of engrailed: a gene involved in the development of pattern in Drosophila melanogaster. Cell 42 : 309–316.
31. BiedlerJK, HuW, TaeH, TuZ (2012) Identification of early zygotic genes in the yellow fever mosquito Aedes aegypti and discovery of a motif involved in early zygotic genome activation. PLoS ONE 7: e33933 doi:10.1371/journal.pone.0033933.
32. ArdehaliMB, LisJT (2009) Tracking rates of transcription and splicing in vivo. Nat Struct Mol Biol 16 : 1123–1124.
33. KornbergT (1981) engrailed: A gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci, USA 78 : 1095–1099.
34. EmeryG, HuttererA, BerdnikD, MayerB, Wirtz-PeitzF, et al. (2005) Asymmetric Rab 11 endosomes regulate delta recycling and specify cell fate in the Drosophila nervous system. Cell 122 : 763–773.
35. VenkenKJ, CarlsonJW, SchulzeKL, PanH, HeY, et al. (2009) Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods 6 : 431–434.
36. PatelNH, Martin-BlancoE, ColemanKG, PooleSJ, EllisMC, et al. (1989) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 955–968.
37. AshburnerM, DrysdaleR (1994) FlyBase–the Drosophila genetic database. Development 120 : 2077–2079.
38. TweedieS, AshburnerM, FallsK, LeylandP, McQuiltonP, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37: D555–559.
39. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
40. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 : 1105–1111.
41. 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.
42. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 : 2078–2079.
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