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First published online February 20, 2009
doi: 10.1242/10.1242/dev.031815

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An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition

¹ Program in Molecular Medicine and the Program in Cell Dynamics, University of Massachusetts Medical School, 377 Plantation Street, Worcester, MA 01605, USA.
² Institut Jacques Monod, UMR7592, 2 place Jussieu, 75251 Paris, Cedex 05, France.
³ Department of Molecular Genetics, University of Toronto, 1 King's College Circle, Toronto, Ontario M5S 1A8, Canada.
⁴ Program in Developmental and Stem Cell Biology, Research Institute, Hospital for Sick Children, TMDT Building, 101 College Street, Toronto, Ontario M5G 1L7, Canada.
⁵ Department of Cell and Systems Biology and Canadian Drosophila Microarray Centre, University of Toronto, Mississauga, Ontario L5L 1C6, Canada.
⁶ Department of Biochemistry, University of Toronto, 1 King's College Circle, Toronto, Ontario M5S 1A8, Canada.

^* Author for correspondence (e-mail: william.theurkauf{at}umassmed.edu)

Accepted 17 December 2008

Genetic control of embryogenesis switches from the maternal to the zygotic genome during the maternal-to-zygotic transition (MZT), when maternal mRNAs are destroyed, high-level zygotic transcription is initiated, the replication checkpoint is activated and the cell cycle slows. The midblastula transition (MBT) is the first morphological event that requires zygotic gene expression. The Drosophila MBT is marked by blastoderm cellularization and follows 13 cleavage-stage divisions. The RNA-binding protein Smaug is required for cleavage-independent maternal transcript destruction during the Drosophila MZT. Here, we show that smaug mutants also disrupt syncytial blastoderm stage cell-cycle delays, DNA replication checkpoint activation, cellularization, and high-level zygotic expression of protein coding and micro RNA genes. We also show that Smaug protein levels increase through the cleavage divisions and peak when the checkpoint is activated and zygotic transcription initiates, and that transgenic expression of Smaug in an anterior-to-posterior gradient produces a concomitant gradient in the timing of maternal transcript destruction, cleavage cell cycle delays, zygotic gene transcription, cellularization and gastrulation. Smaug accumulation thus coordinates progression through the MZT.

Key words: Cell cycle, Midblastula transition, Transcription, Drosophila

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