Abstract
In this study we show that the onset of embryonic transcription in the marine snail Patella vulgata coincides with the start of the sixth cleavage, when the cell-cycle elongates and divisions become asynchronous. Changes in mRNA content before and after onset of transcription were initially demonstrated by in vitro translation of isolated mRNA from different stages. Before the sixth cleavage, three major mRNAs encoding proteins of 36, 50 and 52 kDa were present. These proteins probably correspond to cyclin A and B and ribonucleotide reductase. After this stage, three major proteins with molecular weights of 36.5, 52.5 and 53 kDa were found after in vitro translation. Via hybrid selected translation and differential screening cDNAs corresponding to the 52.5 and 53 kDa proteins were cloned. The encoded proteins resemble tubulins from other animals to a high extent (between 96.5 and 93.1% identity for α-tubulin and 97.9 and 75.9% for β-tubulin). The 36.5 kDa protein is the previously described actin. Both tubulins were expressed at or shortly after the first asynchronous division after the fifth cleavage.
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References
Anderson KV Lengyel JA (1980) Changing rates of historic mRNA synthesis and turnover in Drosophila embryos. Cell 21:717–727
Biggelaar JAM van den (1977) Development of dorsoventral polarity and mesentoblast determination in Patella vulgata. J Morphol 154:157–186
Birnstiel ML, Busslinger M, Strub K (1985) Transcriptional termination and 3′ processing: the end is in site. Cell 41:349–359
Brandhorst BP (1980) Simultaneous synthesis, translation, and storage of mRNA including historic mRNA in sea urchin eggs. Dev Biol 79:139–148
Colot HV, Rosbash M (1982) Behavior of individual maternal pA+ RNAs during embryogenesis of Xenopus laevis. Dev Biol 94:79–86
Damen P, Dictus WJAG (1994a) Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca) Dev Biol 162:364–383
Damen P, Dictus WJAG (1994b) Cell lineage analysis of the prototroch of the Gastropod mollusc Patella vulgata shows conditional specification of some trochoblasts. Roux's Arch Dev Biol 203:187–198
Dawid IB, Rebbert ML, Rosa F, Jamrich M, Sargent TD (1988) Gene expression in amphibian embryogenesis. Cell Diff Dev 25 [Suppl]: 67–74
Dworkin MB, Dawid IB (1980) Use of a cloned library for the study of abundant poly(A)+ RNA during Xenopus laevis development. Dev Biol 76:449–464
Dworkin MB, Hersley JWB (1981) Cellular titers and subcellular distribution of abundant polyadenylate-containing ribonucleic acid species during early development of the frog Xenopus laevis. Mol Cell Biol 1:983–993
Dworkin MB, Shrukowski A, Baumgarten M, Dworkin-Rastl E (1984) The accumulation of prominent tadpole mRNAs occurs at the beginning of neurulation in Xenopus laevis embryos. Dev Biol 106:289–295
Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44:871–877
Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33:389–396
Foe VE (1989) Mitotic domain reveal early commitment of cells in Drosophila embryos. Development 107:1–22
Kimelman D, Kirschner M, Scherson T (1987) The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48:399–407
Krieg PA, Melton DA (1985) Developmental regulation of a gastrula-specific gene injected into fertilized Xenopus eggs. EMBO J 4:3463–3471
Krieg PA, Varnum SM, Wormington WM, Melton DA (1989) The mRNA encoding elongation factor 1-α (EF-1α) is a major transcript at the mid blastula transition in Xenopus. Dev Biol 133:93–100
Laufer JS, Bazzicalupo P, Wood WB (1980) Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 19:569–577
Loon AE van, Goedemans HJ, Daemen AJJM, Kamp AJ van de, Biggelaar JAM van den (1993) Actin genes expressed during early development of Patella vulgata. Roux's Arch Dev Biol 202:77–84
Loon AE van, Colas P, Godemans HJ, Neant I, Dalbon P, Guerrier P (1991) The role of cyclins in the maturation of Patella vulgata oocytes. EMBO J 10:3343–3349
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Mason PJ, Wiliams JG (1986) Hybridisation in the analysis of recombinant DNA. In: Glover DM (ed) DNA cloning: a practical approach. IRL Press, Oxford, pp 113–127
Melton DA (1987) Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature 328:80–82
Newport J, Kirschner M (1982a) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30:687–696
Newport J, Kirschner M (1982b) A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686
Nishida H (1992) Determination of developmental fates of blastomeres in ascidian embryos. Dev Growth Differ 34:253–262
Nusslein-Volhard C (1991) Determination of the embryonic axes of Drosophila. Development [Suppl] 1:1–10
O'Farrell PH, Edgar BA, Lakich D, Lehner CF (1989) Directing cell division during development. Science 246:635–640
Pelman S, Rosbash M (1978) Analysis of Xenopus laevis ovary and somatic cell polyadenylated RNA by molecular hybridisation. Dev Biol 63:197–212
Poccia D, Wolff R, Kragh S, Williamson P (1985) RNA synthesis in male pronuclei of the sea urchin. Biochem Biophys Acta 824:349–356
Rosenthal ET, Tansey TR, Ruderman JV (1983) Sequence-specific adenylation and deadenylation accompany changes in the translation of messenger RNA after fertilization of Spisula oocytes. J Mol Biol 166:309–327
Sargent TD, Dawid IB (1983) Differential gene expression in the gastrula of Xenopus laevis. Science 222:135–139
Sargent TD, Dawid IB, Jamrich M, Jonas E, Miyatani S, Winkles JA (1986) Regulated activation of the zygotic genome in developing Xenopus laevis embryos. In: Gall JG (ed) Gametogenesis and the early embryo. Liss, New York, pp 333–345
Schauer IE, Wood WB (1990) Early C. elegans embryos are transcriptionally active. Development 110:1303–1317
Standart NM, Bray SJ, George EL, Hunt T, Ruderman JV (1985) The small subunit of ribonucleotide reductase is encoded by one of the most abundant translationally regulated maternal RNAs in clam and sea urchin eggs. J Cell Biol 100:1968–1976
Verdonk NH, van den Biggelaar JAM (1983) Early development and the formation of the germ layers. In: Verdonk NH, Biggelaar JAM van den, Tompa AS (eds) The Mollusca, vol 3. Academic Press, New York, pp 91–122
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van Loon, A.E., Goedemans, H.J., Weijtens, M.E.M. et al. Onset of transcription in Patella vulgata coincides with cell cycle elongation and expression of tubulin genes. Roux's Arch Dev Biol 204, 193–197 (1995). https://doi.org/10.1007/BF00241272
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DOI: https://doi.org/10.1007/BF00241272