Regulation of maternal transcript destabilization during egg activation in Drosophila.
In animals, the transfer of developmental control from maternal RNAs and proteins to zygotically derived products occurs at the midblastula transition. This is accompanied by the destabilization of a subset of maternal transcripts. In Drosophila, maternal transcript destabilization occurs in the absence of fertilization and requires specific cis-acting instability elements. We show here that egg activation is necessary and sufficient to trigger transcript destabilization. We have identified 13 maternal-effect lethal loci that, when mutated, result in failure of maternal transcript degradation. All mutants identified are defective in one or more additional processes associated with egg activation. These include vitelline membrane reorganization, cortical microtubule depolymerization, translation of maternal mRNA, completion of meiosis, and chromosome condensation (the S-to-M transition) after meiosis. The least pleiotropic class of transcript destabilization mutants consists of three genes: pan gu, plutonium, and giant nuclei. These three genes regulate the S-to-M transition at the end of meiosis and are thought to be required for the maintenance of cyclin-dependent kinase (CDK) activity during this cell cycle transition. Consistent with a possible functional connection between this S-to-M transition and transcript destabilization, we show that in vitro-activated eggs, which exhibit aberrant postmeiotic chromosome condensation, fail to initiate transcript degradation. Several genetic tests exclude the possibility that reduction of CDK/cyclin complex activity per se is responsible for the failure to trigger transcript destabilization in these mutants. We propose that the trigger for transcript destabilization occurs coincidently with the S-to-M transition at the end of meiosis and that pan gu, plutonium, and giant nuclei regulate maternal transcript destabilization independent of their role in cell cycle regulation.
Tadros
Wael
W
Program in Developmental Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.
Houston
Simon A
SA
Bashirullah
Arash
A
Cooperstock
Ramona L
RL
Semotok
Jennifer L
JL
Reed
Bruce H
BH
Lipshitz
Howard D
HD
D000818:Animals; D002453:Cell Cycle / Q000235:genetics / Q000502:physiology*; D018797:Cell Cycle Proteins / Q000378:metabolism; D004268:DNA-Binding Proteins / Q000378:metabolism; D004330:Drosophila; D029721:Drosophila Proteins / Q000378:metabolism; D005260:Female; D018507:Gene Expression Regulation, Developmental; D015151:Immunoblotting; D007150:Immunohistochemistry; D018613:Microscopy, Confocal; D009154:Mutation / Q000235:genetics; D010063:Ovum / Q000502:physiology*; D017346:Protein Serine-Threonine Kinases / Q000378:metabolism; D020871:RNA Stability / Q000235:genetics*; D014157:Transcription Factors / Q000378:metabolism
D018797:Cell Cycle Proteins; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; C085874:PLU protein, Drosophila; D014157:Transcription Factors; C477039:gnu protein, Drosophila; C417221:png protein, Drosophila; D017346:Protein Serine-Threonine Kinases