1932

Abstract

Many, if not most, embryos begin development with extremely short cell cycles that exhibit unusually rapid DNA replication and no gap phases. The commitment to the cell cycle in the early embryo appears to preclude many other cellular processes that only emerge as the cell cycle slows just prior to gastrulation at a major embryonic transition known as the mid-blastula transition (MBT). As reviewed here, genetic and molecular studies in have identified changes that extend S phase and introduce a postreplicative gap phase, G2, to slow the cell cycle. Although many mysteries remain about the upstream regulators of these changes, we review the core mechanisms of the change in cell cycle regulation and discuss advances in our understanding of how these might be timed and triggered. Finally, we consider how the elements of this program may be conserved or changed in other organisms.

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2014-11-23
2024-10-06
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Literature Cited

  1. Ali-Murthy Z, Lott SE, Eisen MB, Kornberg TB. 1.  2013. An essential role for zygotic expression in the pre-cellular Drosophila embryo. PLOS Genet. 9:4e1003428 [Google Scholar]
  2. Alphey L, Jimenez J, White-Cooper H, Dawson I, Nurse P, Glover DM. 2.  1992. Twine, a cdc25 homolog that functions in the male and female germline of Drosophila. Cell 69:6977–88 [Google Scholar]
  3. Benoit B, He CH, Zhang F, Votruba SM, Tadros W. 3.  et al. 2009. An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 136:6923–32 [Google Scholar]
  4. Bissen ST, Weisblat DA. 4.  1987. Early differences between alternate N blast cells in leech embryo. J. Neurobiol. 18:3251–69 [Google Scholar]
  5. Bissen ST, Weisblat DA. 5.  1989. The durations and compositions of cell cycles in embryos of the leech, Helobdella triserialis. Development 106:1105–18 [Google Scholar]
  6. Blumenthal AB, Kriegstein HJ, Hogness DS. 6.  1974. The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb. Symp. Quant. Biol. 38:205–23 [Google Scholar]
  7. Boos D, Sanchez-Pulido L, Rappas M, Pearl LH, Oliver AW. 7.  et al. 2011. Regulation of DNA replication through Sld3-Dpb11 interaction is conserved from yeast to humans. Curr. Biol. 21:131152–57 [Google Scholar]
  8. Brown DD, Wensink PC, Jordan E. 8.  1971. Purification and some characteristics of 5S DNA from Xenopus laevis. Proc. Natl. Acad. Sci. USA 68:123175–79 [Google Scholar]
  9. Brown JL, Sonoda S, Ueda H, Scott MP, Wu C. 9.  1991. Repression of the Drosophila fushi tarazu (ftz) segmentation gene. EMBO J. 10:3665–74 [Google Scholar]
  10. Calvi BR, Lilly MA, Spradling AC. 10.  1998. Cell cycle control of chorion gene amplification. Genes Dev. 12:5734–44 [Google Scholar]
  11. Collart C, Allen GE, Bradshaw CR, Smith JC, Zegerman P. 11.  2013. Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341:6148893–96 [Google Scholar]
  12. Courtot C, Fankhauser C, Simanis V, Lehner CF. 12.  1992. The Drosophila cdc25 homolog twine is required for meiosis. Development 116:2405–16 [Google Scholar]
  13. Dalle Nogare DE, Pauerstein PT, Lane ME. 13.  2009. G2 acquisition by transcription-independent mechanism at the zebrafish midblastula transition. Dev. Biol. 326:1131–42 [Google Scholar]
  14. de Nooij JC, Letendre MA, Hariharan IK. 14.  1996. A cyclin-dependent kinase inhibitor, Dacapo, is necessary for timely exit from the cell cycle during Drosophila embryogenesis. Cell 87:71237–47 [Google Scholar]
  15. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF. 15.  2007. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLOS Biol. 5:5e117 [Google Scholar]
  16. Deshpande G, Stukey J, Schedl P. 16.  1995. Scute (sis-b) function in Drosophila sex determination. Mol. Cell. Biol. 15:84430–40 [Google Scholar]
  17. Di Talia S, She R, Blythe SA, Lu X, Zhang QF, Wieschaus EF. 17.  2013. Posttranslational control of Cdc25 degradation terminates Drosophila's early cell-cycle program. Curr. Biol. 23:2127–32 [Google Scholar]
  18. Dumollard R, Hebras C, Besnardeau L, McDougall A. 18.  2013. β-Catenin patterns the cell cycle during maternal-to-zygotic transition in urochordate embryos. Dev. Biol. 384:2331–42 [Google Scholar]
  19. Dunphy WG, Kumagai A. 19.  1991. The cdc25 protein contains an intrinsic phosphatase activity. Cell 67:1189–96 [Google Scholar]
  20. Duronio RJ, O'Farrell PH. 20.  1995. Developmental control of the G1 to S transition in Drosophila: Cyclin E is a limiting downstream target of E2F. Genes Dev. 9:121456–68 [Google Scholar]
  21. Dyson N. 21.  1994. PRB, p107 and the regulation of the E2F transcription factor. J. Cell Sci. Suppl. 18:81–87 [Google Scholar]
  22. Edgar BA, Datar SA. 22.  1996. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev. 10:151966–77 [Google Scholar]
  23. Edgar BA, Kiehle CP, Schubiger G. 23.  1986. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44:2365–72 [Google Scholar]
  24. Edgar BA, Lehman DA, O'Farrell PH. 24.  1994. Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development 120:113131–43 [Google Scholar]
  25. Edgar BA, O'Farrell PH. 25.  1989. Genetic control of cell division patterns in the Drosophila embryo. Cell 57:1177–87 [Google Scholar]
  26. Edgar BA, O'Farrell PH. 26.  1990. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell 62:3469–80 [Google Scholar]
  27. Edgar BA, Schubiger G. 27.  1986. Parameters controlling transcriptional activation during early Drosophila development. Cell 44:6871–77 [Google Scholar]
  28. Edgar BA, Sprenger F, Duronio RJ, Leopold P, O'Farrell PH. 28.  1994. Distinct molecular mechanisms regulate cell cycle timing at successive stages of Drosophila embryogenesis. Genes Dev. 8:4440–52 [Google Scholar]
  29. Erickson JW, Cline TW. 29.  1993. A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev 7:91688–702 [Google Scholar]
  30. Erickson JW, Cline TW. 30.  1998. Key aspects of the primary sex determination mechanism are conserved across the genus Drosophila. Development 125:163259–68 [Google Scholar]
  31. Farrell JA, O'Farrell PH. 31.  2013. Mechanism and regulation of Cdc25/Twine protein destruction in embryonic cell-cycle remodeling. Curr. Biol. 23:2118–26 [Google Scholar]
  32. Farrell JA, Shermoen AW, Yuan K, O'Farrell PH. 32.  2012. Embryonic onset of late replication requires Cdc25 down-regulation. Genes Dev. 26:7714–25 [Google Scholar]
  33. Ferrell JE, Wu M, Gerhart JC, Martin GS. 33.  1991. Cell cycle tyrosine phosphorylation of p34cdc2 and a microtubule-associated protein kinase homolog in Xenopus oocytes and eggs. Mol. Cell. Biol. 11:41965–71 [Google Scholar]
  34. Foe VE. 34.  1989. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107:11–22 [Google Scholar]
  35. Foe VE, Alberts BM. 35.  1983. Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61:31–70 [Google Scholar]
  36. Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR. 36.  et al. 1997. The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr. Biol. 7:6418–26 [Google Scholar]
  37. Follette PJ, Duronio RJ, O'Farrell PH. 37.  1998. Fluctuations in cyclin E levels are required for multiple rounds of endocycle S phase in Drosophila. Curr. Biol. 8:4235–38 [Google Scholar]
  38. Follette PJ, O'Farrell PH. 38.  1997. Cdks and the Drosophila cell cycle. Curr. Opin. Genet. Dev. 7:117–22 [Google Scholar]
  39. Frederick DL, Andrews MT. 39.  1994. Cell cycle remodeling requires cell-cell interactions in developing Xenopus embryos. J. Exp. Zool. 270:4410–16 [Google Scholar]
  40. Fu S, Nien CY, Liang HL, Rushlow C. 40.  2014. Co-activation of microRNAs by Zelda is essential for early Drosophila development. Development 141:102108–18 [Google Scholar]
  41. Gawliński P, Nikolay R, Goursot C, Lawo S, Chaurasia B. 41.  et al. 2007. The Drosophila mitotic inhibitor Frühstart specifically binds to the hydrophobic patch of cyclins. EMBO Rep. 8:5490–96 [Google Scholar]
  42. Gerhart JC. 42.  1980. Mechanisms regulating pattern formation in the amphibian egg and early embryo. Biological Regulation and Development 2 Molecular Organization and Cell Function RF Goldberger 133–316 New York: Plenum Press, 2nd ed.. [Google Scholar]
  43. Gould KL, Nurse P. 43.  1989. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342:624539–45 [Google Scholar]
  44. Graham CF, Morgan RW. 44.  1966. Changes in the cell cycle during early amphibian development. Dev. Biol. 14:3439–60 [Google Scholar]
  45. Gross PR, Cousineau GH. 45.  1964. Macromolecule synthesis and the influence of actinomycin on early development. Exp. Cell Res. 33:368–95 [Google Scholar]
  46. Grosshans J, Müller HAJ, Wieschaus E. 46.  2003. Control of cleavage cycles in Drosophila embryos by frühstart. Dev. Cell 5:2285–94 [Google Scholar]
  47. Grosshans J, Wieschaus E. 47.  2000. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 101:5523–31 [Google Scholar]
  48. Harrison MM, Li X-Y, Kaplan T, Botchan MR, Eisen MB. 48.  2011. Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLOS Genet. 7:10e1002266 [Google Scholar]
  49. Hayashi S. 49.  1996. A Cdc2 dependent checkpoint maintains diploidy in Drosophila. Development 122:41051–58 [Google Scholar]
  50. Howe JA, Howell M, Hunt T, Newport JW. 50.  1995. Identification of a developmental timer regulating the stability of embryonic cyclin A and a new somatic A-type cyclin at gastrulation. Genes Dev. 9:101164–76 [Google Scholar]
  51. Iwao Y, Uchida Y, Ueno S, Yoshizaki N, Masui Y. 51.  2005. Midblastula transition (MBT) of the cell cycles in the yolk and pigment granule-free translucent blastomeres obtained from centrifuged Xenopus embryos. Dev. Growth Differ. 47:5283–94 [Google Scholar]
  52. Jin Z, Homola EM, Goldbach P, Choi Y, Brill JA, Campbell SD. 52.  2005. Drosophila Myt1 is a Cdk1 inhibitory kinase that regulates multiple aspects of cell cycle behavior during gametogenesis. Development 132:184075–85 [Google Scholar]
  53. Kafatos FC, Mitsialis SA, Spoerel N, Mariani B, Lingappa JR, Delidakis C. 53.  1985. Studies on the developmentally regulated expression and amplification of insect chorion genes. Cold Spring Harb. Symp. Quant. Biol. 50:537–47 [Google Scholar]
  54. Kane DA, Hammerschmidt M, Mullins MC, Maischein HM, Brand M. 54.  et al. 1996. The zebrafish epiboly mutants. Development 123:47–55 [Google Scholar]
  55. Kane DA, Kimmel CB. 55.  1993. The zebrafish midblastula transition. Development 119:2447–56 [Google Scholar]
  56. Kimelman D, Kirschner M, Scherson T. 56.  1987. The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48:3399–407 [Google Scholar]
  57. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 57.  1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:3253–310 [Google Scholar]
  58. Knoblich JA, Sauer K, Jones L, Richardson H, Saint R, Lehner CF. 58.  1994. Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77:1107–20 [Google Scholar]
  59. Lane ME, Sauer K, Wallace K, Jan YN, Lehner CF, Vaessin H. 59.  1996. Dacapo, a cyclin-dependent kinase inhibitor, stops cell proliferation during Drosophila development. Cell 87:71225–35 [Google Scholar]
  60. Laugsch M, Schierenberg E. 60.  2004. Differences in maternal supply and early development of closely related nematode species. Int. J. Dev. Biol. 48:7655–62 [Google Scholar]
  61. Leptin M. 61.  2005. Gastrulation movements: the logic and the nuts and bolts. Curr. Opin. Cell Biol. 8:3305–20 [Google Scholar]
  62. Liang H-L, Nien C-Y, Liu H-Y, Metzstein MM, Kirov N, Rushlow C. 62.  2008. The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456:7220400–3 [Google Scholar]
  63. Lohe AR, Hilliker AJ, Roberts PA. 63.  1993. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134:41149–74 [Google Scholar]
  64. Lott SE, Villalta JE, Schroth GP, Luo S, Tonkin LA, Eisen MB. 64.  2011. Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq. PLOS Biol. 9:2e1000590 [Google Scholar]
  65. Lu X, Li JM, Elemento O, Tavazoie S, Wieschaus EF. 65.  2009. Coupling of zygotic transcription to mitotic control at the Drosophila mid-blastula transition. Development 136:122101–10 [Google Scholar]
  66. Mac Auley A, Werb Z, Mirkes PE. 66.  1993. Characterization of the unusually rapid cell cycles during rat gastrulation. J. Embryol. Exp. Morphol. 117:3873–83 [Google Scholar]
  67. Manes C. 67.  1973. The participation of the embryonic genome during early cleavage in the rabbit. Dev. Biol. 32:2453–59 [Google Scholar]
  68. Mata J, Curado S, Ephrussi A, Rørth P. 68.  2000. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating String/CDC25 proteolysis. Cell 101:5511–22 [Google Scholar]
  69. McCleland ML, O'Farrell PH. 69.  2008. RNAi of mitotic cyclins in Drosophila uncouples the nuclear and centrosome cycle. Curr. Biol. 18:4245–54 [Google Scholar]
  70. McCleland ML, Shermoen AW, O'Farrell PH. 70.  2009. DNA replication times the cell cycle and contributes to the mid-blastula transition in Drosophila embryos. J. Cell Biol. 187:17–14 [Google Scholar]
  71. McGarry TJ, Kirschner MW. 71.  1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93:61043–53 [Google Scholar]
  72. McKnight SL, Miller OL. 72.  1977. Electron microscopic analysis of chromatin replication in the cellular blastoderm Drosophila melanogaster embryo. Cell 12:3795–804 [Google Scholar]
  73. McKnight SL, Miller OL. 73.  1979. Post-replicative nonribosomal transcription units in D. melanogaster embryos. Cell 17:3551–63 [Google Scholar]
  74. Merrill PT, Sweeton D, Wieschaus E. 74.  1988. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104:3495–509 [Google Scholar]
  75. Morgan D. 75.  1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13:1261–91 [Google Scholar]
  76. Morgan DO. 76.  2007. The Cell Cycle London: New Science Ltd, 1st ed.. [Google Scholar]
  77. Nabel-Rosen H, Toledano-Katchalski H, Volohonsky G, Volk T. 77.  2005. Cell divisions in the Drosophila embryonic mesoderm are repressed via posttranscriptional regulation of string/cdc25 by HOW. Curr. Biol. 15:4295–302 [Google Scholar]
  78. Newport J, Kirschner M. 78.  1982. A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:3675–86 [Google Scholar]
  79. Newport J, Kirschner M. 79.  1982. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:3687–96 [Google Scholar]
  80. Nien C-Y, Liang H-L, Butcher S, Sun Y, Fu S. 80.  et al. 2011. Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLOS Genet. 7:10e1002339 [Google Scholar]
  81. Nothias JY, Majumder S, Kaneko KJ. 81.  1995. Regulation of gene expression at the beginning of mammalian development. J. Biol. Chem. 270:3822077–80 [Google Scholar]
  82. O'Farrell PH. 82.  2004. How metazoans reach their full size: the natural history of bigness. Cell Growth: Control of Cell Size MN Hall, M Raff, G Thomas 1–22 New York: Cold Spring Harbor Press [Google Scholar]
  83. O'Farrell PH, Stumpff J, Su TT. 83.  2004. Embryonic cleavage cycles: How is a mouse like a fly?. Curr. Biol. 14:1R35–R45 [Google Scholar]
  84. Parkhurst SM, Lipshitz HD, Ish-Horowicz D. 84.  1993. achaete-scute feminizing activities and Drosophila sex determination. Development 117:2737–49 [Google Scholar]
  85. Price D, Rabinovitch S, O'Farrell PH, Campbell SD. 85.  2000. Drosophila wee1 has an essential role in the nuclear divisions of early embryogenesis. Genetics 155:1159–66 [Google Scholar]
  86. Pritchard DK, Schubiger G. 86.  1996. Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev. 10:91131–42 [Google Scholar]
  87. Quinn LM, Herr A, McGarry TJ, Richardson H. 87.  2001. The Drosophila Geminin homolog: roles for Geminin in limiting DNA replication, in anaphase and in neurogenesis. Genes Dev. 15:202741–54 [Google Scholar]
  88. Rabinowitz M. 88.  1941. Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J. Morphol. 69:11–49 [Google Scholar]
  89. Rose LS, Wieschaus E. 89.  1992. The Drosophila cellularization gene nullo produces a blastoderm-specific transcript whose levels respond to the nucleocytoplasmic ratio. Genes Dev. 6:71255–68 [Google Scholar]
  90. Russell P, Nurse P. 90.  1986. Cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45:1145–53 [Google Scholar]
  91. Satija R, Bradley RK. 91.  2012. The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo. Genome Res. 22:4656–65 [Google Scholar]
  92. Seher TC, Leptin M. 92.  2000. Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr. Biol. 10:11623–29 [Google Scholar]
  93. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA. 93.  2005. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr. Biol. 15:4284–94 [Google Scholar]
  94. Shermoen AW, McCleland ML, O'Farrell PH. 94.  2010. Developmental control of late replication and S phase length. Curr. Biol. 20:232067–77 [Google Scholar]
  95. Shermoen AW, O'Farrell PH. 95.  1991. Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell 67:2303–10 [Google Scholar]
  96. Shimuta K, Nakajo N, Uto K, Hayano Y, Okazaki K, Sagata N. 96.  2002. Chk1 is activated transiently and targets Cdc25A for degradation at the Xenopus midblastula transition. EMBO J. 21:143694–703 [Google Scholar]
  97. Sibon OC, Laurençon A, Hawley R, Theurkauf WE. 97.  1999. The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9:6302–12 [Google Scholar]
  98. Sibon OC, Stevenson VA, Theurkauf WE. 98.  1997. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388:663793–97 [Google Scholar]
  99. Simpson L, Wieschaus E. 99.  1990. Zygotic activity of the nullo locus is required to stabilize the actin-myosin network during cellularization in Drosophila. Development 110:3851–63 [Google Scholar]
  100. Smibert CA, Wilson JE, Kerr K, Macdonald PM. 100.  1996. Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev. 10:202600–9 [Google Scholar]
  101. Smith AV, Orr-Weaver TL. 101.  1991. The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development 112:4997–1008 [Google Scholar]
  102. Snow MHL. 102.  1977. Gastrulation in the mouse: growth and regionalization of the epiblast. J. Embryol. Exp. Morphol. 42:1293–303 [Google Scholar]
  103. Spradling AC. 103.  1981. The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27:193–201 [Google Scholar]
  104. Stiffler LA, Ji JY, Trautmann S, Trusty C, Schubiger G. 104.  1999. Cyclin A and B functions in the early Drosophila embryo. Development 126:235505–13 [Google Scholar]
  105. Stumpff J, Duncan T, Homola E, Campbell SD, Su TT. 105.  2004. Drosophila Wee1 kinase regulates Cdk1 and mitotic entry during embryogenesis. Curr. Biol. 14:232143–48 [Google Scholar]
  106. Su TT, Campbell SD, O'Farrell PH. 106.  1999. Drosophila grapes/CHK1 mutants are defective in cyclin proteolysis and coordination of mitotic events. Curr. Biol. 9:16919–22 [Google Scholar]
  107. Su TT, Sprenger F, DiGregorio PJ, Campbell SD, O'Farrell PH. 107.  1998. Exit from mitosis in Drosophila syncytial embryos requires proteolysis and cyclin degradation, and is associated with localized dephosphorylation. Genes Dev. 12:101495–503 [Google Scholar]
  108. Sullivan W, Fogarty P, Theurkauf W. 108.  1993. Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development 118:41245–54 [Google Scholar]
  109. Sung H-W, Spangenberg S, Vogt N, Grosshans J. 109.  2013. Number of nuclear divisions in the Drosophila blastoderm controlled by onset of zygotic transcription. Curr. Biol. 23:2133–38 [Google Scholar]
  110. Sweeton D, Parks S, Costa M, Wieschaus E. 110.  1991. Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations. Development 112:3775–89 [Google Scholar]
  111. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L. 111.  et al. 2007. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev. Cell 12:1143–55 [Google Scholar]
  112. Takai H, Tominaga K, Motoyama N, Minamishima YA, Nagahama H. 112.  et al. 2000. Aberrant cell cycle checkpoint function and early embryonic death in Chk1−/− mice. Genes Dev. 14:121439–47 [Google Scholar]
  113. ten Bosch JR, Benavides JA, Cline TW. 113.  2006. The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133:101967–77 [Google Scholar]
  114. Thomson AM, Gillespie PJ, Blow JJ. 114.  2010. Replication factory activation can be decoupled from the replication timing program by modulating Cdk levels. J. Cell Biol. 188:2209–21 [Google Scholar]
  115. Uto K, Inoue D, Shimuta K, Nakajo N, Sagata N. 115.  2004. Chk1, but not Chk2, inhibits Cdc25 phosphatases by a novel common mechanism. EMBO J. 23:163386–96 [Google Scholar]
  116. Wieschaus E. 116.  1996. Embryonic transcription and the control of developmental pathways. Genetics 142:15–10 [Google Scholar]
  117. Wieschaus E, Sweeton D. 117.  1988. Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development 104:3483–93 [Google Scholar]
  118. Wilson EB. 118.  1925. The Cell in Development and Heredity New York: Macmillan, 3rd ed.. [Google Scholar]
  119. Xu Z, Chen H, Ling J, Yu D, Struffi P. 119.  et al. 2014. Impacts of the ubiquitous factor Zelda on Bicoid-dependent DNA binding and transcription in Drosophila. Genes Dev 28:6608–21 [Google Scholar]
  120. Yasuda GK, Baker J, Schubiger G. 120.  1991. Temporal regulation of gene expression in the blastoderm Drosophila embryo. Genes Dev. 5:101800–12 [Google Scholar]
  121. Yasuda GK, Schubiger G. 121.  1992. Temporal regulation in the early embryo: Is MBT too good to be true?. Trends Genet. 8:4124–27 [Google Scholar]
  122. Yuan K, Farrell JA, O'Farrell PH. 122.  2012. Different cyclin types collaborate to reverse the S-phase checkpoint and permit prompt mitosis. J. Cell Biol. 198:6973–80 [Google Scholar]
  123. Yuan K, Shermoen AW, O'Farrell PH. 123.  2014. Illuminating DNA replication during Drosophila development using TALE-lights. Curr. Biol. 24:4R144–45 [Google Scholar]
  124. Zalokar M. 124.  1976. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev. Biol. 49:2425–37 [Google Scholar]
  125. Zamir E, Kam Z, Yarden A. 125.  1997. Transcription-dependent induction of G1 phase during the zebrafish midblastula transition. Mol. Cell. Biol. 17:2529–36 [Google Scholar]
  126. Zhurov V, Terzin T, Grbić M. 126.  2007. (In)discrete charm of the polyembryony: evolution of embryo cloning. Cell. Mol. Life Sci. 64:212790–98 [Google Scholar]
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