1932

Abstract

Embryogenesis depends on a highly coordinated cascade of genetically encoded events. In animals, maternal factors contributed by the egg cytoplasm initially control development, whereas the zygotic nuclear genome is quiescent. Subsequently, the genome is activated, embryonic gene products are mobilized, and maternal factors are cleared. This transfer of developmental control is called the maternal-to-zygotic transition (MZT). In this review, we discuss recent advances toward understanding the scope, timing, and mechanisms that underlie zygotic genome activation at the MZT in animals. We describe high-throughput techniques to measure the embryonic transcriptome and explore how regulation of the cell cycle, chromatin, and transcription factors together elicits specific patterns of embryonic gene expression. Finally, we illustrate the interplay between zygotic transcription and maternal clearance and show how these two activities combine to reprogram two terminally differentiated gametes into a totipotent embryo.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100913-013027
2014-10-06
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/30/1/annurev-cellbio-100913-013027.html?itemId=/content/journals/10.1146/annurev-cellbio-100913-013027&mimeType=html&fmt=ahah

Literature Cited

  1. Aanes H, Ostrup O, Andersen IS, Moen LF, Mathavan S. et al. 2013. Differential transcript isoform usage pre- and post-zygotic genome activation in zebrafish. BMC Genomics 14:331 [Google Scholar]
  2. Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG. et al. 2011. Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res. 21:81328–38 [Google Scholar]
  3. Adenot PG, Mercier Y, Renard JP, Thompson EM. 1997. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124:224615–25 [Google Scholar]
  4. Akkers RC, van Heeringen SJ, Jacobi UG, Janssen-Megens EM, Françoijs KJ. et al. 2009. A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev. Cell 17:3425–34 [Google Scholar]
  5. Ali-Murthy Z, Lott SE, Eisen MB, Kornberg TB. 2013. An essential role for zygotic expression in the pre-cellular Drosophila embryo. PLOS Genet. 9:4e1003428 [Google Scholar]
  6. Andersen IS, Reiner AH, Aanes H, Aleström P, Collas P. 2012. Developmental features of DNA methylation during activation of the embryonic zebrafish genome. Genome Biol. 13:7R65 [Google Scholar]
  7. Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K. et al. 2010. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLOS Biol. 8:8e1000453 [Google Scholar]
  8. Aoki F, Hara KT, Schultz RM. 2003. Acquisition of transcriptional competence in the 1-cell mouse embryo: requirement for recruitment of maternal mRNAs. Mol. Reprod. Dev. 64:3270–74 [Google Scholar]
  9. Aoki F, Worrad DM, Schultz RM. 1997. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181:2296–307 [Google Scholar]
  10. Audic Y, Omilli F, Osborne HB. 1997. Postfertilization deadenylation of mRNAs in Xenopus laevis embryos is sufficient to cause their degradation at the blastula stage. Mol. Cell. Biol. 17:1209–18 [Google Scholar]
  11. Barckmann B, Simonelig M. 2013. Control of maternal mRNA stability in germ cells and early embryos. Biochim. Biophys. Acta Gene Regul. Mech. 1829:6–7714–24 [Google Scholar]
  12. Baroux C, Autran D, Gillmor CS, Grimanelli D, Grossniklaus U. 2008. The maternal to zygotic transition in animals and plants. Cold Spring Harb. Symp. Quant. Biol. 73:89–100 [Google Scholar]
  13. Bashirullah A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A. et al. 1999. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J. 18:92610–20 [Google Scholar]
  14. Baugh LR, Hill AA, Slonim DK, Brown EL, Hunter CP. 2003. Composition and dynamics of the Caenorhabditis elegans early embryonic transcriptome. Development 130:5889–900 [Google Scholar]
  15. Bártfai R, Balduf C, Hilton T, Rathmann Y, Hadzhiev Y. et al. 2004. TBP2, a vertebrate-specific member of the TBP family, is required in embryonic development of zebrafish. Curr. Biol. 14:7593–98 [Google Scholar]
  16. Bazzini AA, Lee MT, Giraldez AJ. 2012. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336:6078233–37 [Google Scholar]
  17. Benoit B, He CH, Zhang F, Votruba SM, Tadros W. 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]
  18. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ. et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:2315–26 [Google Scholar]
  19. Biedler JK, Hu W, Tae H, Tu Z. 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 7:3e33933 [Google Scholar]
  20. Blankenship JT, Wieschaus E. 2001. Two new roles for the Drosophila AP patterning system in early morphogenesis. Development 128:245129–38 [Google Scholar]
  21. Blythe SA, Cha SW, Tadjuidje E, Heasman J, Klein PS. 2010. β-Catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Dev. Cell 19:2220–31 [Google Scholar]
  22. Bogdanović O, Fernandez-Minan A, Tena JJ, de la Calle-Mustienes E, Hidalgo C. et al. 2012. Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis. Genome Res 22:102043–53 [Google Scholar]
  23. Bogdanović O, Long SW, van Heeringen SJ, Brinkman AB, Gómez-Skarmeta. et al. 2011. Temporal uncoupling of the DNA methylome and transcriptional repression during embryogenesis. Genome Res. 21:81313–27 [Google Scholar]
  24. Bouniol C, Nguyen E, Debey P. 1995. Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp. Cell Res. 218:157–62 [Google Scholar]
  25. Bouvet P, Omilli F, Arlot-Bonnemains Y, Legagneux V, Roghi C. et al. 1994. The deadenylation conferred by the 3′ untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol. Cell. Biol. 14:31893–900 [Google Scholar]
  26. Braude P, Bolton V, Moore S. 1988. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332:6163459–61 [Google Scholar]
  27. Brown DD, Littna E. 1964. RNA synthesis during the development of Xenopus laevis, the South African clawed toad. J. Mol. Biol. 8:5669–87 [Google Scholar]
  28. Brown JL, Sonoda S, Ueda H, Scott MP, Wu C. 1991. Repression of the Drosophila fushi tarazu (ftz) segmentation gene. EMBO J. 10:3665–74 [Google Scholar]
  29. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ. et al. 2010. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17:6679–87 [Google Scholar]
  30. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T. 2006. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 20:131744–54 [Google Scholar]
  31. Burgess S, Reim G, Chen W, Hopkins N, Brand M. 2002. The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development 129:4905–16 [Google Scholar]
  32. 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. 18:7501–6 [Google Scholar]
  33. Card DAG, Hebbar PB, Li L, Trotter KW, Komatsu Y. et al. 2008. Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol. Cell. Biol. 28:206426–38 [Google Scholar]
  34. Chang C-C, Ma Y, Jacobs S, Tian XC, Yang X, Rasmussen TP. 2005. A maternal store of macroH2A is removed from pronuclei prior to onset of somatic macroH2A expression in preimplantation embryos. Dev. Biol. 278:2367–80 [Google Scholar]
  35. 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 [Google Scholar]
  36. Chen L, Dumelie JG, Li X, Cheng MHK, Yang Z. et al. 2014. Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein. Genome Biol. 15:1R4 [Google Scholar]
  37. Chen PY, Manninga H, Slanchev K, Chien M, Russo JJ. et al. 2005. The developmental miRNA profiles of zebrafish as determined by small RNA cloning. Genes Dev. 19:111288–93 [Google Scholar]
  38. Cho T, Sakai S, Nagata M, Aoki F. 2002. Involvement of chromatin structure in the regulation of mouse zygotic gene activation. Anim. Sci. J. 73:2113–22 [Google Scholar]
  39. Christians E, Campion E, Thompson EM, Renard JP. 1995. Expression of the HSP 70.1 gene, a landmark of early zygotic activity in the mouse embryo, is restricted to the first burst of transcription. Development 121:1113–22 [Google Scholar]
  40. Colgan DF, Murthy KGK, Prives C, Manley JL. 1996. Cell-cycle related regulation of poly(A) polymerase by phosphorylation. Nature 384:6606282–85 [Google Scholar]
  41. 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 341:6148893–96 [Google Scholar]
  42. Collart C, Owens NDL, Bhaw-Rosun L, Cooper B, De Domenico E. et al. 2014. High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141:91927–39 [Google Scholar]
  43. Craig SP. 1970. Synthesis of RNA in non-nucleate fragments of sea urchin eggs. J. Mol. Biol. 47:3615–18 [Google Scholar]
  44. Dantonel J-C, Quintin S, Lakatos L, Labouesse M, Tora L. 2000. TBP-like factor is required for embryonic RNA polymerase II transcription in C. elegans. Mol. Cell 6:3715–22 [Google Scholar]
  45. Davis WJ, De Sousa PA, Schultz RM. 1996. Transient expression of translation initiation factor eIF-4C during the 2-cell stage of the preimplantation mouse embryo: identification by mRNA differential display and the role of DNA replication in zygotic gene activation. Dev. Biol. 174:2190–201 [Google Scholar]
  46. 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. 5:5e117 [Google Scholar]
  47. Dekens MPS, Pelegri FJ, Maischein HM, Nüsslein-Volhard C. 2003. The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebrafish zygote. Development 130:173907–16 [Google Scholar]
  48. 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. 23:2127–32 [Google Scholar]
  49. Dimitrov S, Almouzni G, Dasso M, Wolffe AP. 1993. Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev. Biol. 160:1214–27 [Google Scholar]
  50. Dobson AT, Raja R, Abeyta MJ, Taylor T, Shen S. et al. 2004. The unique transcriptome through day 3 of human preimplantation development. Hum. Mol. Genet. 13:141461–70 [Google Scholar]
  51. Dunican DS, Ruzov A, Hackett JA, Meehan RR. 2008. xDnmt1 regulates transcriptional silencing in pre-MBT Xenopus embryos independently of its catalytic function. Development 135:71295–302 [Google Scholar]
  52. Duval C, Bouvet P, Omilli F, Roghi C, Dorel C. et al. 1990. Stability of maternal mRNA in Xenopus embryos: role of transcription and translation. Mol. Cell. Biol. 10:84123–29 [Google Scholar]
  53. Edgar BA, Datar SA. 1996. Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev. 10:151966–77 [Google Scholar]
  54. Edgar BA, Kiehle CP, Schubiger G. 1986. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44:2365–72 [Google Scholar]
  55. Edgar BA, Schubiger G. 1986. Parameters controlling transcriptional activation during early Drosophila development. Cell 44:6871–77 [Google Scholar]
  56. Edgar LG, Wolf N, Wood WB. 1994. Early transcription in Caenorhabditis elegans embryos. Development 120:2443–51 [Google Scholar]
  57. Faast R, Thonglairoam V, Schulz TC, Beall J, Wells JRE. et al. 2001. Histone variant H2A.Z is required for early mammalian development. Curr. Biol. 11:151183–87 [Google Scholar]
  58. Farrell JA, O'Farrell PH. 2013. Mechanism and regulation of Cdc25/Twine protein destruction in embryonic cell-cycle remodeling. Curr. Biol. 23:2118–26 [Google Scholar]
  59. Ferg M, Sanges R, Gehrig J, Kiss J, Bauer M. et al. 2007. The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish. EMBO J. 26:173945–56 [Google Scholar]
  60. 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. 61:131–70 [Google Scholar]
  61. Fu G, Ghadam P, Sirotkin A, Khochbin S, Skoultchi AI, Clarke HJ. 2003. Mouse oocytes and early embryos express multiple histone H1 subtypes. Biol. Reprod. 68:51569–76 [Google Scholar]
  62. Fu S, Nien C-Y, Liang H-L, Rushlow C. 2014. Co-activation of microRNAs by Zelda is essential for early Drosophila development. Development 141:102108–18 [Google Scholar]
  63. Gerhart JC. 1980. Mechanisms regulating pattern formation in the amphibian egg and early embryo. Biological Regulation and Development R Goldberger 133–316 Boston, MA: Springer [Google Scholar]
  64. Giraldez AJ. 2010. microRNAs, the cell's Nepenthe: clearing the past during the maternal-to-zygotic transition and cellular reprogramming. Curr. Opin. Genet. Dev. 20:4369–75 [Google Scholar]
  65. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S. et al. 2006. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312:577075–79 [Google Scholar]
  66. Goddard MJ, Pratt HPM. 1983. Control of events during early cleavage of the mouse embryo: an analysis of the “2-cell block.” J. Embryol. Exp. Morphol. 73:1111–33 [Google Scholar]
  67. Golbus MS, Calarco PG, Epstein CJ. 1973. The effects of inhibitors of RNA synthesis (α-amanitin and actinomycin D) on preimplantation mouse embryogenesis. J. Exp. Zool. 186:2207–16 [Google Scholar]
  68. Guilgur LG, Prudêncio P, Sobral D, Liszekova D, Rosa A, Martinho RG. 2014. Requirement for highly efficient pre-mRNA splicing during Drosophila early embryonic development. eLife 3:e02181 [Google Scholar]
  69. Guttman M, Rinn JL. 2012. Modular regulatory principles of large non-coding RNAs. Nature 482:7385339–46 [Google Scholar]
  70. 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 135:1149–60 [Google Scholar]
  71. Haberle V, Li N, Hadzhiev Y, Plessy C, Previti C. et al. 2014. Two independent transcription initiation codes overlap on vertebrate core promoters. Nature 507:381–85 [Google Scholar]
  72. Hamatani T, Carter MG, Sharov AA, Ko MSH. 2004. Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6:1117–31 [Google Scholar]
  73. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:7254473–78 [Google Scholar]
  74. Harrison MM, Botchan MR, Cline TW. 2010. Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes. Dev. Biol. 345:2248–55 [Google Scholar]
  75. 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. 7:10e1002266 [Google Scholar]
  76. Harvey SA, Sealy I, Kettleborough R, Fenyes F, White R. et al. 2013. Identification of the zebrafish maternal and paternal transcriptomes. Development 140:132703–10 [Google Scholar]
  77. Heyn P, Kircher M, Dahl A, Kelso J, Tomancak P. et al. 2014. The earliest transcribed zygotic genes are short, newly evolved, and different across species. Cell Rep. 6:2285–92 [Google Scholar]
  78. Howe JA, Howell M, Hunt T, Newport JW. 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]
  79. Huntzinger E, Izaurralde E. 2011. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12:299–110 [Google Scholar]
  80. Jallow Z, Jacobi UG, Weeks DL, Dawid IB, Veenstra GJ. 2004. Specialized and redundant roles of TBP and a vertebrate-specific TBP paralog in embryonic gene regulation in Xenopus. Proc. Natl. Acad. Sci. USA 101:3713525–30 [Google Scholar]
  81. Jayaramaiah Raja S, Renkawitz-Pohl R. 2005. Replacement by Drosophila melanogaster protamines and Mst77f of histones during chromatin condensation in late spermatids and role of sesame in the removal of these proteins from the male pronucleus. Mol. Cell. Biol. 25:146165–77 [Google Scholar]
  82. Jiang L, Zhang J, Wang JJ, Wang L, Zhang L. et al. 2013. Sperm, but not oocyte, DNA methylome is inherited by zebrafish early embryos. Cell 153:4773–84 [Google Scholar]
  83. Kaltenbach L, Horner MA, Rothman JH, Mango SE. 2000. The TBP-like factor CeTLF is required to activate RNA polymerase II transcription during C. elegans embryogenesis. Mol. Cell 6:3705–13 [Google Scholar]
  84. Kane DA, Hammerschmidt M, Mullins MC, Maischein HM, Brand M. et al. 1996. The zebrafish epiboly mutants. Development 123:47–55 [Google Scholar]
  85. Kane DA, Kimmel CB. 1993. The zebrafish midblastula transition. Development 119:2447–56 [Google Scholar]
  86. Karr TL, Ali Z, Drees B, Kornberg T. 1985. The engrailed locus of D. melanogaster provides an essential zygotic function in precellular embryos. Cell 43:3 Pt.2591–601 [Google Scholar]
  87. Kimelman D, Kirschner M, Scherson T. 1987. The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48:3399–407 [Google Scholar]
  88. Knowland J, Graham C. 1972. RNA synthesis at the two-cell stage of mouse development. J. Embryol. Exp. Morphol. 27:1167–76 [Google Scholar]
  89. Laubichler MD, Davidson EH. 2008. Boveri's long experiment: sea urchin merogones and the establishment of the role of nuclear chromosomes in development. Dev. Biol. 314:11–11 [Google Scholar]
  90. Lecuit T, Samanta R, Wieschaus E. 2002. slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo. Dev. Cell 2:4425–36 [Google Scholar]
  91. Lécuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T. et al. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131:1174–87 [Google Scholar]
  92. Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR. et al. 2013. Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503:7476360–64 [Google Scholar]
  93. Leichsenring M, Maes J, Mössner R, Driever W, Onichtchouk D. 2013. Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341:61491005–9 [Google Scholar]
  94. Lepikhov K, Walter J. 2004. Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev. Biol. 4:12 [Google Scholar]
  95. 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 456:7220400–3 [Google Scholar]
  96. Lin C-J, Conti M, Ramalho-Santos M. 2013. Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140:173624–34 [Google Scholar]
  97. Lindeman LC, Andersen IS, Reiner AH, Li N, Aanes H. et al. 2011. Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev. Cell 21:6993–1004 [Google Scholar]
  98. 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 9:2e1000590 [Google Scholar]
  99. 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 136:122101–10 [Google Scholar]
  100. Lund E, Liu M, Hartley RS, Sheets MD, Dahlberg JE. 2009. Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA 15:122351–63 [Google Scholar]
  101. Majumder S, DePamphilis ML. 1995. A unique role for enhancers is revealed during early mouse development. BioEssays 17:10879–89 [Google Scholar]
  102. Martianov I, Viville S, Davidson I. 2002. RNA polymerase II transcription in murine cells lacking the TATA binding protein. Science 298:55951036–39 [Google Scholar]
  103. Martínez-Salas E, Linney E, Hassell J, DePamphilis ML. 1989. The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus. Genes Dev. 3:101493–506 [Google Scholar]
  104. Mathavan S, Lee SGP, Mak A, Miller LD, Murthy KRK. et al. 2005. Transcriptome analysis of zebrafish embryogenesis using microarrays. PLOS Genet. 1:2260–76 [Google Scholar]
  105. Merrill PT, Sweeton D, Wieschaus E. 1988. Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development 104:3495–509 [Google Scholar]
  106. Mhanni AA, McGowan RA. 2004. Global changes in genomic methylation levels during early development of the zebrafish embryo. Dev. Genes Evol. 214:8412–17 [Google Scholar]
  107. Müller F, Lakatos T, Dantonel J, Strähle U, Tora L. 2001. TBP is not universally required for zygotic RNA polymerase II transcription in zebrafish. Curr. Biol. 11:4282–87 [Google Scholar]
  108. Nemer M. 1963. Old and new RNA in the embryogenesis of the purple sea urchin. Proc. Natl. Acad. Sci. USA 50:2230 [Google Scholar]
  109. Nepal C, Hadzhiev Y, Previti C, Haberle V, Li N. et al. 2013. Dynamic regulation of the transcription initiation landscape at single nucleotide resolution during vertebrate embryogenesis. Genome Res 23:111938–50 [Google Scholar]
  110. Newport J, Kirschner M. 1982a. 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]
  111. Newport J, Kirschner M. 1982b. A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:3687–96 [Google Scholar]
  112. Nien C-Y, Liang H-L, Butcher S, Sun Y, Fu S. et al. 2011. Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLOS Genet 7:10e1002339 [Google Scholar]
  113. Nonchev S, Tsanev R. 1990. Protamine-histone replacement and DNA replication in the male mouse pronucleus. Mol. Reprod. Dev. 25:172–76 [Google Scholar]
  114. Okuda Y, Ogura E, Kondoh H, Kamachi Y. 2010. B1 SOX coordinate cell specification with patterning and morphogenesis in the early zebrafish embryo. PLOS Genet. 6:5e1000936 [Google Scholar]
  115. Onichtchouk D, Geier F, Polok B, Messerschmidt DM, Mössner R. et al. 2010. Zebrafish Pou5f1-dependent transcriptional networks in temporal control of early development. Mol. Syst. Biol. 6:354 [Google Scholar]
  116. Orkin SH, Hochedlinger K. 2011. Chromatin connections to pluripotency and cellular reprogramming. Cell 145:6835–50 [Google Scholar]
  117. Oron E, Ivanova N. 2012. Cell fate regulation in early mammalian development. Phys. Biol. 9:4045002 [Google Scholar]
  118. Oswald J, Engemann S, Lane N, Mayer W, Olek A. et al. 2000. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10:8475–78 [Google Scholar]
  119. Paillard L, Omilli F, Legagneux V, Bassez T, Maniey D, Osborne HB. 1998. EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J. 17:1278–87 [Google Scholar]
  120. Paranjpe SS, Jacobi UG, van Heeringen SJ, Veenstra GJC. 2013. A genome-wide survey of maternal and embryonic transcripts during Xenopus tropicalis development. BMC Genomics 14:762 [Google Scholar]
  121. Park S-J, Komata M, Inoue F, Yamada K, Nakai K. et al. 2013. Inferring the choreography of parental genomes during fertilization from ultralarge-scale whole-transcriptome analysis. Genes Dev. 27:242736–48 [Google Scholar]
  122. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL. et al. 2012. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22:3577–91 [Google Scholar]
  123. Pérez-Montero S, Carbonell A, Morán T, Vaquero A, Azorín F. 2013. The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev. Cell 26:6578–90 [Google Scholar]
  124. Pikó L, Clegg KB. 1982. Quantitative changes in total RNA, total poly(A), and ribosomes in early mouse embryos. Dev. Biol. 89:2362–78 [Google Scholar]
  125. Poccia D, Wolff R, Kragh S, Williamson P. 1985. RNA synthesis in male pronuclei of the sea urchin. Biochim. Biophys. Acta 824:4349–56 [Google Scholar]
  126. Posfai E, Kunzmann R, Brochard V, Salvaing J, Cabuy E. et al. 2012. Polycomb function during oogenesis is required for mouse embryonic development. Genes Dev. 26:9920–32 [Google Scholar]
  127. Potok ME, Nix DA, Parnell TJ, Cairns BR. 2013. Reprogramming the maternal zebrafish genome after fertilization to match the paternal methylation pattern. Cell 153:4759–72 [Google Scholar]
  128. Prioleau MN, Huet J, Sentenac A, Méchali M. 1994. Competition between chromatin and transcription complex assembly regulates gene expression during early development. Cell 77:3439–49 [Google Scholar]
  129. Pritchard DK, Schubiger G. 1996. Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev. 10:91131–42 [Google Scholar]
  130. Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K. et al. 2008. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40:4411–20 [Google Scholar]
  131. Qin X, Ahn S, Speed TP, Rubin GM. 2007. Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol. 8:4R63 [Google Scholar]
  132. Ram PT, Schultz RM. 1993. Reporter gene expression in G2 of the 1-cell mouse embryo. Dev. Biol. 156:2552–56 [Google Scholar]
  133. Richter JD, Lasko P. 2011. Translational control in oocyte development. Cold Spring Harb. Perspect. Biol. 3:9a002758 [Google Scholar]
  134. Rothe M, Pehl M, Taubert H, Jäckle H. 1992. Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature 359:6391156–59 [Google Scholar]
  135. Rothstein JL, Johnson D, DeLoia JA, Skowronski J, Solter D, Knowles B. 1992. Gene expression during preimplantation mouse development. Genes Dev. 6:71190–201 [Google Scholar]
  136. Ruzov A, Dunican DS, Prokhorchouk A, Pennings S, Stancheva I. et al. 2004. Kaiso is a genome-wide repressor of transcription that is essential for amphibian development. Development 131:246185–94 [Google Scholar]
  137. Santos F, Hendrich B, Reik W, Dean W. 2002. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241:1172–82 [Google Scholar]
  138. Santos F, Peters AH, Otte AP, Reik W, Dean W. 2005. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280:1225–36 [Google Scholar]
  139. Satija R, Bradley RK. 2012. The TAGteam motif facilitates binding of 21 sequence-specific transcription factors in the Drosophila embryo. Genome Res. 22:4656–65 [Google Scholar]
  140. Sawicki JA, Magnuson T, Epstein CJ. 1981. Evidence for expression of the paternal genome in the two-cell mouse embryo. Nature 294:5840450–51 [Google Scholar]
  141. Schuettengruber B, Ganapathi M, Leblanc B, Portoso M, Janschek R. et al. 2009. Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLOS Biol. 7:1e13 [Google Scholar]
  142. Schuff M, Siegel D, Philipp M, Bundschu K, Heymann N. et al. 2012. Characterization of Danio rerio Nanog and functional comparison to Xenopus Vents. Stem Cells Dev. 21:81225–38 [Google Scholar]
  143. Selvig SE, Gross PR, Hunter AL. 1970. Cytoplasmic synthesis of RNA in the sea urchin embryo. Dev. Biol. 22:2343–65 [Google Scholar]
  144. 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. 15:4284–94 [Google Scholar]
  145. Shechter D, Nicklay JJ, Chitta RK, Shabanowitz J, Hunt DF, Allis CD. 2009. Analysis of histones in Xenopus laevis. I. A distinct index of enriched variants and modifications exists in each cell type and is remodeled during developmental transitions. J. Biol. Chem. 284:21064–74 [Google Scholar]
  146. Shermoen AW, O'Farrell PH. 1991. Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell 67:2303–10 [Google Scholar]
  147. Shin C, Manley JL. 2002. The SR protein SRp38 represses splicing in M phase cells. Cell 111:3407–17 [Google Scholar]
  148. Simon JA, Kingston RE. 2009. Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10:10697–708 [Google Scholar]
  149. Sirard MA, Dufort I, Vallée M, Massicotte L, Gravel C. et al. 2005. Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development: preliminary analysis using a bovine embryonic array. Reprod. Fertil. Dev. 17:1–247–57 [Google Scholar]
  150. Sive HL, St John T. 1988. A simple subtractive hybridization technique employing photoactivatable biotin and phenol extraction. Nucleic Acids Res. 16:2210937 [Google Scholar]
  151. Skirkanich J, Luxardi G, Yang J, Kodjabachian L, Klein P. 2011. An essential role for transcription before the MBT in Xenopus laevis. Dev. Biol. 357:2478–91 [Google Scholar]
  152. Smith RC, Dworkin-Rastl E, Dworkin MB. 1988. Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev. 2:101284–95 [Google Scholar]
  153. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A. et al. 2012. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484:7394339–44 [Google Scholar]
  154. Sørensen CS, Syljuåsen RG. 2012. Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res. 40:2477–86 [Google Scholar]
  155. Stancheva I, El-Maarri O, Walter J, Niveleau A, Meehan RR. 2002. DNA methylation at promoter regions regulates the timing of gene activation in Xenopus laevis embryos. Dev. Biol. 243:1155–65 [Google Scholar]
  156. Stancheva I, Meehan RR. 2000. Transient depletion of xDnmt1 leads to premature gene activation in Xenopus embryos. Genes Dev. 14:3313–27 [Google Scholar]
  157. Staudt N, Fellert S, Chung HR, Jäckle H, Vorbrüggen G. 2006. Mutations of the Drosophila zinc finger-encoding gene vielfältig impair mitotic cell divisions and cause improper chromosome segregation. Mol. Biol. Cell 17:52356–65 [Google Scholar]
  158. Stitzel ML, Pellettieri J, Seydoux G. 2006. The C. elegans DYRK kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr. Biol. 16:156–62 [Google Scholar]
  159. Storfer-Glazer FA, Wood WB. 1994. Effects of chromosomal deficiencies on early cleavage patterning and terminal phenotype in Caenorhabditis elegans embryos. Genetics 137:2499–508 [Google Scholar]
  160. Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100:164–119 [Google Scholar]
  161. Sun F, Tang F, Yan AY, Fang HY, Sheng HZ. 2007. Expression of SRG3, a chromatin-remodelling factor, in the mouse oocyte and early preimplantation embryos. Zygote 15:2129–38 [Google Scholar]
  162. Sung H-W, Spangenberg S, Vogt N, Großhans J. 2013. Number of nuclear divisions in the Drosophila blastoderm controlled by onset of zygotic transcription. Curr. Biol. 23:2133–38 [Google Scholar]
  163. Surdej P, Jacobs-Lorena M. 1998. Developmental regulation of bicoid mRNA stability is mediated by the first 43 nucleotides of the 3′ untranslated region. Mol. Cell. Biol. 18:52892–900 [Google Scholar]
  164. Svoboda P, Flemr M. 2010. The role of miRNAs and endogenous siRNAs in maternal-to-zygotic reprogramming and the establishment of pluripotency. EMBO Rep 11:8590–97 [Google Scholar]
  165. Swinburne IA, Silver PA. 2008. Intron delays and transcriptional timing during development. Dev. Cell 14:3324–30 [Google Scholar]
  166. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L. 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]
  167. Tadros W, Lipshitz HD. 2009. The maternal-to-zygotic transition: a play in two acts. Development 136:183033–42 [Google Scholar]
  168. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:4663–76 [Google Scholar]
  169. Tan MH, Au KF, Yablonovitch AL, Wills AE, Chuang J. et al. 2013. RNA sequencing reveals a diverse and dynamic repertoire of the Xenopus tropicalis transcriptome over development. Genome Res. 23:1201–16 [Google Scholar]
  170. Tanaka M, Hennebold JD, Macfarlane J, Adashi EY. 2001. A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128:5655–64 [Google Scholar]
  171. Tang F, Kaneda M, O'Carroll D, Hajkova P, Barton SC. et al. 2007. Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21:6644–48 [Google Scholar]
  172. Tani S, Kusakabe R, Naruse K, Sakamoto H, Inoue K. 2010. Genomic organization and embryonic expression of miR-430 in medaka (Oryzias latipes): insights into the post-transcriptional gene regulation in early development. Gene 449:1–241–49 [Google Scholar]
  173. ten Bosch JR, Benavides JA, Cline TW. 2006. The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription. Development 133:101967–77 [Google Scholar]
  174. Thomas S, Li XY, Sabo PJ, Sandstrom R, Thurman RE. et al. 2011. Dynamic reprogramming of chromatin accessibility during Drosophila embryo development. Genome Biol. 12:5R43 [Google Scholar]
  175. Torres-Padilla M-E, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M. 2006. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 50:5455–61 [Google Scholar]
  176. Tsurumi A, Xia F, Li J, Larson K, LaFrance R, Li WX. 2011. STAT is an essential activator of the zygotic genome in the early Drosophila embryo. PLOS Genet. 7:5e1002086 [Google Scholar]
  177. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. 2011. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147:71537–50 [Google Scholar]
  178. Ulitsky I, Shkumatava A, Jan CH, Subtelny AO, Koppstein D. et al. 2012. Extensive alternative polyadenylation during zebrafish development. Genome Res 22:102054–66 [Google Scholar]
  179. van der Heijden GW, Derijck AAHA, Ramos L, Giele M, van der Vlag J, de Boer P. 2006. Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev. Biol. 298:2458–69 [Google Scholar]
  180. Vassena R, Boué S, González-Roca E, Aran B, Auer H. et al. 2011. Waves of early transcriptional activation and pluripotency program initiation during human preimplantation development. Development 138:173699–709 [Google Scholar]
  181. Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A. et al. 2010. Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464:7290922–26 [Google Scholar]
  182. Veenstra GJ, Destrée OH, Wolffe AP. 1999. Translation of maternal TATA-binding protein mRNA potentiates basal but not activated transcription in Xenopus embryos at the midblastula transition. Mol. Cell. Biol. 19:127972–82 [Google Scholar]
  183. Veenstra GJC, Weeks DL, Wolffe AP. 2000. Distinct roles for TBP and TBP-like factor in early embryonic gene transcription in Xenopus. Science 290:55002312–15 [Google Scholar]
  184. Vesterlund L, Jiao H, Unneberg P, Hovatta O, Kere J. 2011. The zebrafish transcriptome during early development. BMC Dev. Biol. 11:30 [Google Scholar]
  185. Voeltz GK, Steitz JA. 1998. AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol. Cell. Biol. 18:127537–45 [Google Scholar]
  186. Walser CB, Lipshitz HD. 2011. Transcript clearance during the maternal-to-zygotic transition. Curr. Opin. Genet. Dev. 21:4431–43 [Google Scholar]
  187. Wang J, Garrey J, Davis RE. 2014. Transcription in pronuclei and one- to four-cell embryos drives early development in a nematode. Curr. Biol. 24:2124–33 [Google Scholar]
  188. Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP. et al. 2004. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6:1133–44 [Google Scholar]
  189. Warner CM, Versteegh LR. 1974. In vivo and in vitro effect of α-amanitin on preimplantation mouse embryo RNA polymerase. Nature 248:450678–80 [Google Scholar]
  190. Watanabe T, Takeda A, Mise K, Okuno T, Suzuki T. et al. 2005. Stage-specific expression of microRNAs during Xenopus development. FEBS Lett 579:2318–24 [Google Scholar]
  191. Wei Z, Angerer RC, Angerer LM. 2006. A database of mRNA expression patterns for the sea urchin embryo. Dev. Biol. 300:1476–84 [Google Scholar]
  192. Whittle CM, McClinic KN, Ercan S, Zhang X, Green RD. et al. 2008. The genomic distribution and function of histone variant HTZ-1 during C. elegans embryogenesis. PLOS Genet. 4:9e1000187 [Google Scholar]
  193. Wiekowski M, Miranda M, DePamphilis ML. 1991. Regulation of gene expression in preimplantation mouse embryos: effects of the zygotic clock and the first mitosis on promoter and enhancer activities. Dev. Biol. 147:2403–14 [Google Scholar]
  194. Wiekowski M, Miranda M, DePamphilis ML. 1993. Requirements for promoter activity in mouse oocytes and embryos distinguish paternal pronuclei from maternal and zygotic nuclei. Dev. Biol. 159:1366–78 [Google Scholar]
  195. Wu S-F, Zhang H, Cairns BR. 2011. Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm. Genome Res. 21:4578–89 [Google Scholar]
  196. Xie D, Chen CC, Ptaszek LM, Xiao S, Cao X. et al. 2010. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res. 20:6804–15 [Google Scholar]
  197. Xin H-P, Zhao J, Sun M-X. 2012. The maternal-to-zygotic transition in higher plants. J. Integr. Plant Biol. 54:9610–15 [Google Scholar]
  198. Xu C, Fan ZP, Müller P, Fogley R, DiBiase A. et al. 2012. Nanog-like regulates endoderm formation through the Mxtx2-Nodal pathway. Dev. Cell 22:3625–38 [Google Scholar]
  199. Xue Z, Huang K, Cai C, Cai L, Jiang CY. et al. 2013. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500:7464593–97 [Google Scholar]
  200. Yanai I, Peshkin L, Jorgensen P, Kirschner MW. 2011. Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. Dev. Cell 20:4483–96 [Google Scholar]
  201. Yang J, Tan C, Darken RS, Wilson PA, Klein PS. 2002. β-Catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129:245743–52 [Google Scholar]
  202. Yasuda GK, Baker J, Schubiger G. 1991. Temporal regulation of gene expression in the blastoderm Drosophila embryo. Genes Dev. 5:101800–12 [Google Scholar]
  203. Yasuda GK, Schubiger G. 1992. Temporal regulation in the early embryo: Is MBT too good to be true?. Trends Genet. 8:4124–27 [Google Scholar]
  204. Young RA. 2011. Control of the embryonic stem cell state. Cell 144:6940–54 [Google Scholar]
  205. Zalokar M. 1976. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev. Biol. 49:2425–37 [Google Scholar]
  206. Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:212227–41 [Google Scholar]
  207. Zeng F, Schultz RM. 2003. Gene expression in mouse oocytes and preimplantation embryos: use of suppression subtractive hybridization to identify oocyte- and embryo-specific genes. Biol. Reprod. 68:131–39 [Google Scholar]
  208. Zhang P, Zucchelli M, Bruce S, Hambiliki F, Savreus-Evers A. et al. 2009. Transcriptome profiling of human pre-implantation development. PLOS ONE 4:11e7844 [Google Scholar]
  209. Zhang Y, Vastenhouw NL, Feng J, Fu K, Wang C. et al. 2014. Canonical nucleosome organization at promoters forms during genome activation. Genome Res. 24:2260–66 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100913-013027
Loading
/content/journals/10.1146/annurev-cellbio-100913-013027
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error