Skip to main content

Link of Zygotic Genome Activation and Cell Cycle Control

  • Protocol
  • First Online:
Zygotic Genome Activation

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1605))

Abstract

The activation of the zygotic genome and onset of transcription in blastula embryos is linked to changes in cell behavior and remodeling of the cell cycle and constitutes a transition from exclusive maternal to zygotic control of development. This step in development is referred to as mid-blastula transition and has served as a paradigm for the link between developmental program and cell behavior and morphology. Here, we discuss the mechanism and functional relationships between the zygotic genome activation and cell cycle control during mid-blastula transition with a focus on Drosophila embryos.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Hiiragi T, Solter D (2004) First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 430(6997):360–364. doi:10.1038/nature02595

    Article  CAS  PubMed  Google Scholar 

  2. O’Farrell PH, Stumpff J, Su TT (2004) Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol 14(1):R35–R45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. O’Farrell PH (2015) Growing an embryo from a single cell: a hurdle in animal life. Cold Spring Harb Perspect Biol 7(11):a019042. doi:10.1101/cshperspect.a019042

    Article  PubMed  CAS  Google Scholar 

  4. Boveri T (1893) An organism produced sexually without characteristics of the mother. Am Soc Nat 27(315):222–232

    Article  Google Scholar 

  5. Gerhart JC (1980) Mechanisms regulating pattern formation in the amphibian egg and early embryo. In: Goldberger R (ed) Biological regulation and development, vol 2. Springer, Boston, MA, pp 133–316

    Chapter  Google Scholar 

  6. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30(3):675–686

    Article  CAS  PubMed  Google Scholar 

  7. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30(3):687–696

    Article  CAS  PubMed  Google Scholar 

  8. Newport JW, Kirschner MW (1984) Regulation of the cell cycle during early Xenopus development. Cell 37(3):731–742

    Article  CAS  PubMed  Google Scholar 

  9. Farrell JA, O’Farrell PH (2014) From egg to gastrula: how the cell cycle is remodeled during the Drosophila mid-blastula transition. Annu Rev Genet 48:269–294. doi:10.1146/annurev-genet-111212-133531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Collart C, Owens ND, Bhaw-Rosun L, Cooper B, De Domenico E, Patrushev I, Sesay AK, Smith JN, Smith JC, Gilchrist MJ (2014) High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141(9):1927–1939. doi:10.1242/dev.102012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119(2):447–456

    CAS  PubMed  Google Scholar 

  12. Zamir E, Kam Z, Yarden A (1997) Transcription-dependent induction of G1 phase during the zebra fish midblastula transition. Mol Cell Biol 17(2):529–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Zhang M, Kothari P, Mullins M, Lampson MA (2014) Regulation of zygotic genome activation and DNA damage checkpoint acquisition at the mid-blastula transition. Cell Cycle 13(24):3828–3838. doi:10.4161/15384101.2014.967066

    Article  CAS  PubMed  Google Scholar 

  14. Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR, Fleming ES, Giraldez AJ (2013) Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503(7476):360–364. doi:10.1038/nature12632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Robertson S, Lin R (2015) The maternal-to-zygotic transition in C. elegans. Curr Top Dev Biol 113:1–42. doi:10.1016/bs.ctdb.2015.06.001

    Article  PubMed  Google Scholar 

  16. Guven-Ozkan T, Nishi Y, Robertson SM, Lin R (2008) Global transcriptional repression in C. elegans germline precursors by regulated sequestration of TAF-4. Cell 135(1):149–160. doi:10.1016/j.cell.2008.07.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100(1):64–119

    Article  CAS  PubMed  Google Scholar 

  18. Rose L, Gonczy P (2014) Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos. WormBook:1–43. doi:10.1895/wormbook.1.30.2

    Google Scholar 

  19. Foe VE, Alberts BM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61:31–70

    CAS  PubMed  Google Scholar 

  20. McCleland ML, O’Farrell PH (2008) RNAi of mitotic cyclins in Drosophila uncouples the nuclear and centrosome cycle. Curr Biol 18(4):245–254. doi:10.1016/j.cub.2008.01.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Shermoen AW, McCleland ML, O’Farrell PH (2010) Developmental control of late replication and S phase length. Curr Biol 20(23):2067–2077. doi:10.1016/j.cub.2010.10.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Farrell JA, Shermoen AW, Yuan K, O’Farrell PH (2012) Embryonic onset of late replication requires Cdc25 down-regulation. Genes Dev 26(7):714–725. doi:10.1101/gad.186429.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rabinowitz M (1941) Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J Morphol 69(1):1–49

    Article  Google Scholar 

  24. Axton JM, Shamanski FL, Young LM, Henderson DS, Boyd JB, Orr-Weaver TL (1994) The inhibitor of DNA replication encoded by the Drosophila gene plutonium is a small, ankyrin repeat protein. EMBO J 13(2):462–470

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Fenger DD, Carminati JL, Burney-Sigman DL, Kashevsky H, Dines JL, Elfring LK, Orr-Weaver TL (2000) PAN GU: a protein kinase that inhibits S phase and promotes mitosis in early Drosophila development. Development 127(22):4763–4774

    CAS  PubMed  Google Scholar 

  26. Lee LA, Van Hoewyk D, Orr-Weaver TL (2003) The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions. Genes Dev 17(23):2979–2991. doi:10.1101/gad.1132603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Laver JD, Marsolais AJ, Smibert CA, Lipshitz HD (2015) Regulation and function of maternal gene products during the maternal-to-zygotic transition in Drosophila. Curr Top Dev Biol 113:43–84. doi:10.1016/bs.ctdb.2015.06.007

    Article  PubMed  Google Scholar 

  28. Schubeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M (2002) Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32(3):438–442. doi:10.1038/ng1005

    Article  PubMed  CAS  Google Scholar 

  29. Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44(6):871–877

    Article  CAS  PubMed  Google Scholar 

  30. Merrill PT, Sweeton D, Wieschaus E (1988) Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104(3):495–509

    CAS  PubMed  Google Scholar 

  31. Ali-Murthy Z, Lott SE, Eisen MB, Kornberg TB (2013) An essential role for zygotic expression in the pre-cellular Drosophila embryo. PLoS Genet 9(4):e1003428. doi:10.1371/journal.pgen.1003428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, Langton L, Perrimon N, Sandler JE, Wan KH, Willingham A, Zhang Y, Zou Y, Andrews J, Bickel PJ, Brenner SE, Brent MR, Cherbas P, Gingeras TR, Hoskins RA, Kaufman TC, Oliver B, Celniker SE (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471(7339):473–479. doi:10.1038/nature09715

    Article  CAS  PubMed  Google Scholar 

  33. Lott SE, Villalta JE, Schroth GP, Luo S, Tonkin LA, Eisen MB (2011) Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq. PLoS Biol 9(2):e1000590. doi:10.1371/journal.pbio.1000590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Harrison MM, Eisen MB (2015) Transcriptional activation of the zygotic genome in Drosophila. Curr Top Dev Biol 113:85–112. doi:10.1016/bs.ctdb.2015.07.028

    Article  PubMed  Google Scholar 

  35. Lee MT, Bonneau AR, Giraldez AJ (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol 30:581–613. doi:10.1146/annurev-cellbio-100913-013027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5(5):e117. doi:10.1371/journal.pbio.0050117

    Article  PubMed  PubMed Central  Google Scholar 

  37. Tadros W, Houston SA, Bashirullah A, Cooperstock RL, Semotok JL, Reed BH, Lipshitz HD (2003) Regulation of maternal transcript destabilization during egg activation in Drosophila. Genetics 164(3):989–1001

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz HD (2007) SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 12(1):143–155. doi:10.1016/j.devcel.2006.10.005

    Article  CAS  PubMed  Google Scholar 

  39. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136(18):3033–3042. doi:10.1242/dev.033183

    Article  CAS  PubMed  Google Scholar 

  40. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA (2005) Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 15(4):284–294. doi:10.1016/j.cub.2005.01.048

    Article  CAS  PubMed  Google Scholar 

  41. Chen L, Dumelie JG, Li X, Cheng MH, Yang Z, Laver JD, Siddiqui NU, Westwood JT, Morris Q, Lipshitz HD, Smibert CA (2014) Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein. Genome Biol 15(1):R4. doi:10.1186/gb-2014-15-1-r4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Laver JD, Li X, Ray D, Cook KB, Hahn NA, Nabeel-Shah S, Kekis M, Luo H, Marsolais AJ, Fung KY, Hughes TR, Westwood JT, Sidhu SS, Morris Q, Lipshitz HD, Smibert CA (2015) Brain tumor is a sequence-specific RNA-binding protein that directs maternal mRNA clearance during the Drosophila maternal-to-zygotic transition. Genome Biol 16:94. doi:10.1186/s13059-015-0659-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Walser CB, Lipshitz HD (2011) Transcript clearance during the maternal-to-zygotic transition. Curr Opin Genet Dev 21(4):431–443. doi:10.1016/j.gde.2011.03.003

    Article  CAS  PubMed  Google Scholar 

  44. Bashirullah A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A, Fisher WW, Fu W, Hamilton JK, Etkin LD, Lipshitz HD (1999) Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J 18(9):2610–2620. doi:10.1093/emboj/18.9.2610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Bushati N, Stark A, Brennecke J, Cohen SM (2008) Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol 18(7):501–506. doi:10.1016/j.cub.2008.02.081

    Article  CAS  PubMed  Google Scholar 

  46. Fu S, Nien CY, Liang HL, Rushlow C (2014) Co-activation of microRNAs by Zelda is essential for early Drosophila development. Development 141(10):2108–2118. doi:10.1242/dev.108118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Huntzinger E, Izaurralde E (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 12(2):99–110. doi:10.1038/nrg2936

    Article  CAS  PubMed  Google Scholar 

  48. Li XY, Harrison MM, Villalta JE, Kaplan T, Eisen MB (2014) Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. Elife 3. doi:10.7554/eLife.03737

  49. Harrison MM, Li XY, Kaplan T, Botchan MR, Eisen MB (2011) Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet 7(10):e1002266. doi:10.1371/journal.pgen.1002266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM (2007) Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131(1):174–187. doi:10.1016/j.cell.2007.08.003

    Article  CAS  PubMed  Google Scholar 

  51. Saunders A, Core LJ, Sutcliffe C, Lis JT, Ashe HL (2013) Extensive polymerase pausing during Drosophila axis patterning enables high-level and pliable transcription. Genes Dev 27(10):1146–1158. doi:10.1101/gad.215459.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ferraro T, Lucas T, Clemot M, De Las Heras Chanes J, Desponds J, Coppey M, Walczak AM, Dostatni N (2016) New methods to image transcription in living fly embryos: the insights so far, and the prospects. Wiley Interdiscip Rev Dev Biol 5(3):296–310. doi:10.1002/wdev.221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Pritchard DK, Schubiger G (1996) Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev 10(9):1131–1142

    Article  CAS  PubMed  Google Scholar 

  54. Heyn P, Kircher M, Dahl A, Kelso J, Tomancak P, Kalinka AT, Neugebauer KM (2014) The earliest transcribed zygotic genes are short, newly evolved, and different across species. Cell Rep 6(2):285–292. doi:10.1016/j.celrep.2013.12.030

    Article  CAS  PubMed  Google Scholar 

  55. Chen K, Johnston J, Shao W, Meier S, Staber C, Zeitlinger J (2013) A global change in RNA polymerase II pausing during the Drosophila midblastula transition. Elife 2:e00861. doi:10.7554/eLife.00861

    PubMed  PubMed Central  Google Scholar 

  56. Sung HW, Spangenberg S, Vogt N, Grosshans J (2013) Number of nuclear divisions in the Drosophila blastoderm controlled by onset of zygotic transcription. Curr Biol 23(2):133–138. doi:10.1016/j.cub.2012.12.013

    Article  CAS  PubMed  Google Scholar 

  57. Sandler JE, Stathopoulos A (2016) Quantitative single-embryo profile of Drosophila genome activation and the dorsal-ventral patterning network. Genetics 202(4):1575–1584. doi:10.1534/genetics.116.186783

    Article  PubMed  PubMed Central  Google Scholar 

  58. ten Bosch JR, Benavides JA, Cline TW (2006) The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133(10):1967–1977. doi:10.1242/dev.02373

    Article  PubMed  CAS  Google Scholar 

  59. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA, Iyer VN, Hechmer A, Simirenko L, Stapleton M, Luengo Hendriks CL, Chu HC, Ogawa N, Inwood W, Sementchenko V, Beaton A, Weiszmann R, Celniker SE, Knowles DW, Gingeras T, Speed TP, Eisen MB, Biggin MD (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol 6(2):e27. doi:10.1371/journal.pbio.0060027

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Liang HL, Nien CY, Liu HY, Metzstein MM, Kirov N, Rushlow C (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456(7220):400–403. doi:10.1038/nature07388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Staudt N, Fellert S, Chung HR, Jackle H, Vorbruggen G (2006) Mutations of the Drosophila zinc finger-encoding gene vielfaltig impair mitotic cell divisions and cause improper chromosome segregation. Mol Biol Cell 17(5):2356–2365. doi:10.1091/mbc.E05-11-1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hamm DC, Bondra ER, Harrison MM (2015) Transcriptional activation is a conserved feature of the early embryonic factor Zelda that requires a cluster of four zinc fingers for DNA binding and a low-complexity activation domain. J Biol Chem 290(6):3508–3518. doi:10.1074/jbc.M114.602292

    Article  CAS  PubMed  Google Scholar 

  63. Foo SM, Sun Y, Lim B, Ziukaite R, O’Brien K, Nien CY, Kirov N, Shvartsman SY, Rushlow CA (2014) Zelda potentiates morphogen activity by increasing chromatin accessibility. Curr Biol 24(12):1341–1346. doi:10.1016/j.cub.2014.04.032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Schulz KN, Bondra ER, Moshe A, Villalta JE, Lieb JD, Kaplan T, McKay DJ, Harrison MM (2015) Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo. Genome Res 25(11):1715–1726. doi:10.1101/gr.192682.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, Adelman K, Levine M, Young RA (2007) RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 39(12):1512–1516. doi:10.1038/ng.2007.26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Boettiger AN, Levine M (2009) Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325(5939):471–473. doi:10.1126/science.1173976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Blythe SA, Wieschaus EF (2015) Zygotic genome activation triggers the DNA replication checkpoint at the midblastula transition. Cell 160(6):1169–1181. doi:10.1016/j.cell.2015.01.050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Rudolph T, Yonezawa M, Lein S, Heidrich K, Kubicek S, Schafer C, Phalke S, Walther M, Schmidt A, Jenuwein T, Reuter G (2007) Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3-3. Mol Cell 26(1):103–115. doi:10.1016/j.molcel.2007.02.025

    Article  CAS  PubMed  Google Scholar 

  69. Yuan K, O’Farrell PH (2016) TALE-light imaging reveals maternally guided, H3K9me2/3-independent emergence of functional heterochromatin in Drosophila embryos. Genes Dev. doi:10.1101/gad.272237.115

    Google Scholar 

  70. Lindeman LC, Andersen IS, Reiner AH, Li N, Aanes H, Ostrup O, Winata C, Mathavan S, Muller F, Alestrom P, Collas P (2011) Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell 21(6):993–1004. doi:10.1016/j.devcel.2011.10.008

    Article  CAS  PubMed  Google Scholar 

  71. Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A, Liu XS, Rinn J, Schier AF (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464(7290):922–926. doi:10.1038/nature08866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Amodeo AA, Jukam D, Straight AF, Skotheim JM (2015) Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition. Proc Natl Acad Sci U S A 112(10):E1086–E1095. doi:10.1073/pnas.1413990112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hontelez S, van Kruijsbergen I, Georgiou G, van Heeringen SJ, Bogdanovic O, Lister R, Veenstra GJ (2015) Embryonic transcription is controlled by maternally defined chromatin state. Nat Commun 6:10148. doi:10.1038/ncomms10148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ, Fudenberg G, Imakaev M, Mirny LA, Wu CT, Zhuang X (2016) Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 529(7586):418–422. doi:10.1038/nature16496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Zhao R, Nakamura T, Fu Y, Lazar Z, Spector DL (2011) Gene bookmarking accelerates the kinetics of post-mitotic transcriptional re-activation. Nat Cell Biol 13(11):1295–1304. doi:10.1038/ncb2341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Perez-Montero S, Carbonell A, Moran T, Vaquero A, Azorin F (2013) The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev Cell 26(6):578–590. doi:10.1016/j.devcel.2013.08.011

    Article  CAS  PubMed  Google Scholar 

  77. Li XY, Thomas S, Sabo PJ, Eisen MB, Stamatoyannopoulos JA, Biggin MD (2011) The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol 12(4):R34. doi:10.1186/gb-2011-12-4-r34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Thomas S, Li XY, Sabo PJ, Sandstrom R, Thurman RE, Canfield TK, Giste E, Fisher W, Hammonds A, Celniker SE, Biggin MD, Stamatoyannopoulos JA (2011) Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol 12(5):R43. doi:10.1186/gb-2011-12-5-r43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Zhang Y, Vastenhouw NL, Feng J, Fu K, Wang C, Ge Y, Pauli A, van Hummelen P, Schier AF, Liu XS (2014) Canonical nucleosome organization at promoters forms during genome activation. Genome Res 24(2):260–266. doi:10.1101/gr.157750.113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Juven-Gershon T, Kadonaga JT (2010) Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol 339(2):225–229. doi:10.1016/j.ydbio.2009.08.009

    Article  CAS  PubMed  Google Scholar 

  81. Zabidi MA, Arnold CD, Schernhuber K, Pagani M, Rath M, Frank O, Stark A (2015) Enhancer-core-promoter specificity separates developmental and housekeeping gene regulation. Nature 518(7540):556–559. doi:10.1038/nature13994

    Article  CAS  PubMed  Google Scholar 

  82. Collart C, Allen GE, Bradshaw CR, Smith JC, Zegerman P (2013) Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341(6148):893–896. doi:10.1126/science.1241530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Lehner CF, O’Farrell PH (1990) Drosophila cdc2 homologs: a functional homolog is coexpressed with a cognate variant. EMBO J 9(11):3573–3581

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Edgar BA, O’Farrell PH (1990) The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell 62(3):469–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Edgar BA, Sprenger F, Duronio RJ, Leopold P, O’Farrell PH (1994) Distinct molecular mechanism regulate cell cycle timing at successive stages of Drosophila embryogenesis. Genes Dev 8(4):440–452

    Article  CAS  PubMed  Google Scholar 

  86. Yuan K, O’Farrell PH (2015) Cyclin B3 is a mitotic cyclin that promotes the metaphase-anaphase transition. Curr Biol 25(6):811–816. doi:10.1016/j.cub.2015.01.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sigrist S, Ried G, Lehner CF (1995) Dmcdc2 kinase is required for both meiotic divisions during Drosophila spermatogenesis and is activated by the Twine/cdc25 phosphatase. Mech Dev 53(2):247–260

    Article  CAS  PubMed  Google Scholar 

  88. Glotzer M, Murray AW, Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349(6305):132–138. doi:10.1038/349132a0

    Article  CAS  PubMed  Google Scholar 

  89. Yuan K, Farrell JA, O’Farrell PH (2012) Different cyclin types collaborate to reverse the S-phase checkpoint and permit prompt mitosis. J Cell Biol 198(6):973–980. doi:10.1083/jcb.201205007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ji JY, Squirrell JM, Schubiger G (2004) Both cyclin B levels and DNA-replication checkpoint control the early embryonic mitoses in Drosophila. Development 131(2):401–411. doi:10.1242/dev.00944

    Article  CAS  PubMed  Google Scholar 

  91. Jin Z, Homola EM, Goldbach P, Choi Y, Brill JA, Campbell SD (2005) Drosophila Myt1 is a Cdk1 inhibitory kinase that regulates multiple aspects of cell cycle behavior during gametogenesis. Development 132(18):4075–4085. doi:10.1242/dev.01965

    Article  CAS  PubMed  Google Scholar 

  92. Price D, Rabinovitch S, O’Farrell PH, Campbell SD (2000) Drosophila wee1 has an essential role in the nuclear divisions of early embryogenesis. Genetics 155(1):159–166

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Stumpff J, Duncan T, Homola E, Campbell SD, Su TT (2004) Drosophila Wee1 kinase regulates Cdk1 and mitotic entry during embryogenesis. Curr Biol 14(23):2143–2148. doi:10.1016/j.cub.2004.11.050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Edgar BA, O’Farrell PH (1989) Genetic control of cell division patterns in the Drosophila embryo. Cell 57(1):177–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Blythe SA, Wieschaus EF (2015) Coordinating cell cycle remodeling with transcriptional activation at the Drosophila MBT. Curr Top Dev Biol 113:113–148. doi:10.1016/bs.ctdb.2015.06.002

    Article  PubMed  Google Scholar 

  96. Ayeni JO, Varadarajan R, Mukherjee O, Stuart DT, Sprenger F, Srayko M, Campbell SD (2014) Dual phosphorylation of cdk1 coordinates cell proliferation with key developmental processes in Drosophila. Genetics 196(1):197–210. doi:10.1534/genetics.113.156281

    Article  CAS  PubMed  Google Scholar 

  97. Farrell JA, O’Farrell PH (2013) Mechanism and regulation of Cdc25/Twine protein destruction in embryonic cell-cycle remodeling. Curr Biol 23(2):118–126. doi:10.1016/j.cub.2012.11.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Di Talia S, She R, Blythe SA, Lu X, Zhang QF, Wieschaus EF (2013) Posttranslational control of Cdc25 degradation terminates Drosophila’s early cell-cycle program. Curr Biol 23(2):127–132. doi:10.1016/j.cub.2012.11.029

    Article  CAS  PubMed  Google Scholar 

  99. Edgar BA, Lehner CF (1996) Developmental control of cell cycle regulators: a fly’s perspective. Science 274(5293):1646–1652

    Article  CAS  PubMed  Google Scholar 

  100. Alphey L, Jimenez J, White-Cooper H, Dawson I, Nurse P, Glover DM (1992) twine, a cdc25 homolog that functions in the male and female germline of Drosophila. Cell 69(6):977–988

    Article  CAS  PubMed  Google Scholar 

  101. Grosshans J, Wieschaus E (2000) A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101(5):523–531

    Article  CAS  PubMed  Google Scholar 

  102. Mata J, Curado S, Ephrussi A, Rorth P (2000) Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101(5):511–522

    Article  CAS  PubMed  Google Scholar 

  103. Rorth P, Szabo K, Texido G (2000) The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol Cell 6(1):23–30

    Article  CAS  PubMed  Google Scholar 

  104. Frazer C, Young PG (2012) Phosphorylation mediated regulation of Cdc25 activity, localization and stability. In: Huang C (ed) Protein phosphorylation in human health, Biochemistry, genetics and molecular biology. InTech, Rijeka, Croatia, pp 395–436. doi:10.5772/48315

    Google Scholar 

  105. Murphy JM, Nakatani Y, Jamieson SA, Dai W, Lucet IS, Mace PD (2015) Molecular mechanism of CCAAT-enhancer binding protein recruitment by the TRIB1 pseudokinase. Structure 23(11):2111–2121. doi:10.1016/j.str.2015.08.017

    Article  CAS  PubMed  Google Scholar 

  106. Edgar BA, Datar SA (1996) Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila’s early cell cycle program. Genes Dev 10(15):1966–1977

    Article  CAS  PubMed  Google Scholar 

  107. Chen F, Archambault V, Kar A, Lio P, D’Avino PP, Sinka R, Lilley K, Laue ED, Deak P, Capalbo L, Glover DM (2007) Multiple protein phosphatases are required for mitosis in Drosophila. Curr Biol 17(4):293–303. doi:10.1016/j.cub.2007.01.068

    Article  PubMed  CAS  Google Scholar 

  108. Blumenthal AB, Kriegstein HJ, Hogness DS (1974) The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol 38:205–223

    Article  CAS  PubMed  Google Scholar 

  109. Sibon OC, Stevenson VA, Theurkauf WE (1997) DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388(6637):93–97. doi:10.1038/40439

    Article  CAS  PubMed  Google Scholar 

  110. Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR, Uy GL, Goldberg ML, Sullivan W (1997) The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr Biol 7(6):418–426

    Article  CAS  PubMed  Google Scholar 

  111. Sibon OC, Laurencon A, Hawley R, Theurkauf WE (1999) The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr Biol 9(6):302–312

    Article  CAS  PubMed  Google Scholar 

  112. Shimuta K, Nakajo N, Uto K, Hayano Y, Okazaki K, Sagata N (2002) Chk1 is activated transiently and targets Cdc25A for degradation at the Xenopus midblastula transition. EMBO J 21(14):3694–3703. doi:10.1093/emboj/cdf357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Gawlinski P, Nikolay R, Goursot C, Lawo S, Chaurasia B, Herz HM, Kussler-Schneider Y, Ruppert T, Mayer M, Grosshans J (2007) The Drosophila mitotic inhibitor Fruhstart specifically binds to the hydrophobic patch of cyclins. EMBO Rep 8(5):490–496. doi:10.1038/sj.embor.7400948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Grosshans J, Muller HA, Wieschaus E (2003) Control of cleavage cycles in Drosophila embryos by fruhstart. Dev Cell 5(2):285–294

    Article  CAS  PubMed  Google Scholar 

  115. Lu X, Li JM, Elemento O, Tavazoie S, Wieschaus EF (2009) Coupling of zygotic transcription to mitotic control at the Drosophila mid-blastula transition. Development 136(12):2101–2110. doi:10.1242/dev.034421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Campbell SD, Sprenger F, Edgar BA, O’Farrell PH (1995) Drosophila Wee1 kinase rescues fission yeast from mitotic catastrophe and phosphorylates Drosophila Cdc2 in vitro. Mol Biol Cell 6(10):1333–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Bettencourt-Dias M, Giet R, Sinka R, Mazumdar A, Lock WG, Balloux F, Zafiropoulos PJ, Yamaguchi S, Winter S, Carthew RW, Cooper M, Jones D, Frenz L, Glover DM (2004) Genome-wide survey of protein kinases required for cell cycle progression. Nature 432(7020):980–987. doi:10.1038/nature03160

    Article  CAS  PubMed  Google Scholar 

  118. Fasulo B, Koyama C, Yu KR, Homola EM, Hsieh TS, Campbell SD, Sullivan W (2012) Chk1 and Wee1 kinases coordinate DNA replication, chromosome condensation, and anaphase entry. Mol Biol Cell 23(6):1047–1057. doi:10.1091/mbc.E11-10-0832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Royou A, McCusker D, Kellogg DR, Sullivan W (2008) Grapes(Chk1) prevents nuclear CDK1 activation by delaying cyclin B nuclear accumulation. J Cell Biol 183(1):63–75. doi:10.1083/jcb.200801153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Kang Q, Srividhya J, Ipe J, Pomerening JR (2014) Evidence toward a dual phosphatase mechanism that restricts Aurora A (Thr-295) phosphorylation during the early embryonic cell cycle. J Biol Chem 289(25):17480–17496. doi:10.1074/jbc.M113.527622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300(5625):1542–1548. doi:10.1126/science.1083430

    Article  CAS  PubMed  Google Scholar 

  122. Papoulas O, Monzo KF, Cantin GT, Ruse C, Yates JR 3rd, Ryu YH, Sisson JC (2010) dFMRP and Caprin, translational regulators of synaptic plasticity, control the cell cycle at the Drosophila mid-blastula transition. Development 137(24):4201–4209. doi:10.1242/dev.055046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Monzo K, Papoulas O, Cantin GT, Wang Y, Yates JR 3rd, Sisson JC (2006) Fragile X mental retardation protein controls trailer hitch expression and cleavage furrow formation in Drosophila embryos. Proc Natl Acad Sci U S A 103(48):18160–18165. doi:10.1073/pnas.0606508103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Nien CY, Liang HL, Butcher S, Sun Y, Fu S, Gocha T, Kirov N, Manak JR, Rushlow C (2011) Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLoS Genet 7(10):e1002339. doi:10.1371/journal.pgen.1002339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Benoit B, He CH, Zhang F, Votruba SM, Tadros W, Westwood JT, Smibert CA, Lipshitz HD, Theurkauf WE (2009) An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 136(6):923–932. doi:10.1242/dev.031815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Jevtic P, Levy DL (2015) Nuclear size scaling during Xenopus early development contributes to midblastula transition timing. Curr Biol 25(1):45–52. doi:10.1016/j.cub.2014.10.051

    Article  CAS  PubMed  Google Scholar 

  127. Vastag L, Jorgensen P, Peshkin L, Wei R, Rabinowitz JD, Kirschner MW (2011) Remodeling of the metabolome during early frog development. PLoS One 6(2):e16881. doi:10.1371/journal.pone.0016881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Edgar BA, Kiehle CP, Schubiger G (1986) Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44(2):365–372

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

BL was supported by China Scholarship Council. The work in JG’s laboratory was in part supported by the German Research Council (Deutsche Forschungsgemeinschaft (DFG) GR1945/3-1, SFB937/TP10).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jörg Grosshans .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media LLC

About this protocol

Cite this protocol

Liu, B., Grosshans, J. (2017). Link of Zygotic Genome Activation and Cell Cycle Control. In: Lee, K. (eds) Zygotic Genome Activation. Methods in Molecular Biology, vol 1605. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6988-3_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-6988-3_2

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-6986-9

  • Online ISBN: 978-1-4939-6988-3

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics