An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition.
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.
Benoit
Beatrice
B
Program in Molecular Medicine, University of Massachusetts Medical School, 377 Plantation Street, Worcester, MA 01605, USA.
He
Chun Hua
CH
Zhang
Fan
F
Votruba
Sarah M
SM
Tadros
Wael
W
Westwood
J Timothy
JT
Smibert
Craig A
CA
Lipshitz
Howard D
HD
Theurkauf
William E
WE
D000818:Animals; D004261:DNA Replication; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000196:embryology / Q000235:genetics / Q000378:metabolism*; D005260:Female; D018507:Gene Expression Regulation, Developmental; D049750:Genome, Insect / Q000235:genetics; D035683:MicroRNAs / Q000235:genetics; D009035:Mothers; D005810:Multigene Family / Q000235:genetics; D020411:Oligonucleotide Array Sequence Analysis; D016601:RNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D012097:Repressor Proteins / Q000235:genetics / Q000378:metabolism*; D015053:Zygote / Q000378:metabolism*
D029721:Drosophila Proteins; D035683:MicroRNAs; D016601:RNA-Binding Proteins; D012097:Repressor Proteins; C402587:smg protein, Drosophila