Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila

Highlights

• We find widespread change in mRNA polyadenylation during Drosophila egg activation.

• Surprisingly, the change affects most maternally-loaded mRNAs (but not all GO classes).

• The GLD2 cytoplasmic poly(A) polymerase “Wispy” causes the poly(A) elongation.

• The candidate regulated-mRNAs that we tested co-IP with Wispy.

• Wispy also regulates polyadenylation of many mRNAs in late-stage oocytes.

Abstract

The GLD-2 class of poly(A) polymerases regulate the timing of translation of stored transcripts by elongating the poly(A) tails of target mRNAs in the cytoplasm. WISPY is a GLD-2 enzyme that acts in the Drosophila female germline and is required for the completion of the egg-to-embryo transition. Though a handful of WISPY target mRNAs have been identified during both oogenesis and early embryogenesis, it was unknown whether WISP simply regulated a small pool of patterning or cell cycle genes, or whether, instead, cytoplasmic polyadenylation was widespread during this developmental transition. To identify the full range of WISPY targets, we carried out microarray analysis to look for maternal mRNAs whose poly(A) tails fail to elongate in the absence of WISP function. We examined the polyadenylated portion of the maternal transcriptome in both stage 14 (mature) oocytes and in early embryos that had completed egg activation. Our analysis shows that the poly(A) tails of thousands of maternal mRNAs fail to elongate in wisp-deficient oocytes and embryos. Furthermore, we have identified specific classes of genes that are highly regulated in this manner at each stage. Our study shows that cytoplasmic polyadenylation is a major regulatory mechanism during oocyte maturation and egg activation.