Regulation of Maternal Transcript Destabilization During Egg Activation in Drosophila

Abstract

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.

Greatwall-Endos-PP2A/B55 Twins network regulates translation and stability of maternal transcripts in the Drosophila oocyte-to-embryo transition

“…In both the above cases, however, a proportion of embryos derived from png 1058 /png 3318 females with compromised PP2A activity developed through considerably more mitotic cycles to have hundreds of nuclei ( figure 2 a ). Thus, our findings extend previous work indicating that the png mitotic phenotype can be rescued by mutation of the catalytic subunit of PP2A [ 7 , 9 ]. Thus, reducing PP2A/B55 Twins protein phosphatase activity appears sufficient to overcome the block to mitotic progression imposed by this png mutant background ( figure 2 and electronic supplementary material, table S1).…”

“…Elevated expression of Endos or to some extent mutation in tws , encoding the B55 regulatory subunit of PP2A, also suppress png mutants. We interpret this suppression of the png mitotic phenotype as a consequence of increased activation of the Cdk1/Cyclin B mitotic kinase or its substrates and promotion of mitosis by elevated Endos and decreased PP2A/B55 Twins activity echoing a previous finding of partial rescue of png by mts mutants [7,9]. Indeed, this was previously interpreted as the promotion of the mitotic state through the global loss of PP2A function.…”

“…(b) The Gwl and Pan Gu pathways intersect through PP2A/B55 Twins As Gwl is required for the correct regulation of the mitotic cycle and Png for the activation of the mitotic cycles in the syncytial embryo, we considered that the pathways may share at least one common regulatory element. Of several possible mitotic regulators, it has been reported that the png mitotic phenotype can be rescued by mutation of the catalytic subunit of PP2A [7,9], encoded by microtubule star in Drosophila. PP2A is a trimeric complex that, in addition to its catalytic subunit (C), has a structural subunit (A) and one of several possible regulatory subunits (B).…”

“…In plant or animal embryos, transcripts and proteins deposited by the mother in the oocyte support the development of the newly created zygote before the onset of zygotic transcription [1][2][3][4][5]. In Drosophila, the Pan Gu kinase is activated at the oocyte-to-embryo transition and triggers a dramatic reorganization of the maternal translatome, on which depends the onset of the mitotic cycles [6][7][8][9][10][11][12][13].…”

Temporal Transcriptome Analysis Reveals Dynamic Expression Profiles of Gametes and Embryonic Development in Japanese Flounder (Paralichthys olivaceus)

“…In Drosophila, maternal gene products were degraded immediately after egg activation. The minor wave ZGA occurred in the 8-cell division of early embryos, and large-scale transcription occurred at 14-cell division [9,10]. Fast-developing embryos in vertebrate, such as amphibians and fish, often exhibit late ZGA stage [2].…”