Sequential Regulation of Maternal mRNAs through a Conserved cis-Acting Element in Their 3′ UTRs

• Published in: Cell reports (Cambridge) Vol. 25; no. 13; pp. 3828 - 3843.e9
• Main Authors: Flora, Pooja, Wong-Deyrup, Siu Wah, Martin, Elliot Todd, Palumbo, Ryan J., Nasrallah, Mohamad, Oligney, Andrew, Blatt, Patrick, Patel, Dhruv, Fuchs, Gabriele, Rangan, Prashanth
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 26.12.2018; Elsevier
• Subjects: 3' Untranslated Regions - genetics; Animals; Base Sequence; Bruno; Cell Differentiation - genetics; Conserved Sequence - genetics; Drosophila melanogaster - embryology; Drosophila melanogaster - genetics; Drosophila Proteins - metabolism; Gene Expression Regulation, Developmental; oogenesis; Oogenesis - genetics; pgc; Protein Binding; Protein Biosynthesis; Pumilio; RNA regulation; RNA, Messenger, Stored - genetics; RNA, Messenger, Stored - metabolism; Bruno; RNA regulation; Pumilio; pgc; oogenesis
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2018.12.007

Maternal mRNAs synthesized during oogenesis initiate the development of future generations. Some maternal mRNAs are either somatic or germline determinants and must be translationally repressed until embryogenesis. However, the translational repressors themselves are temporally regulated. We used polar granule component (pgc), a Drosophila maternal mRNA, to ask how maternal transcripts are repressed while the regulatory landscape is shifting. pgc, a germline determinant, is translationally regulated throughout oogenesis. We find that different conserved RNA-binding proteins bind a 10-nt sequence in the 3′ UTR of pgc mRNA to continuously repress translation at different stages of oogenesis. Pumilio binds to this sequence in undifferentiated and early-differentiating oocytes to block Pgc translation. After differentiation, Bruno levels increase, allowing Bruno to bind the same sequence and take over translational repression of pgc mRNA. We have identified a class of maternal mRNAs that are regulated similarly, including zelda, the activator of the zygotic genome. [Display omitted] •pgc, a germline RNA, is translationally regulated throughout Drosophila oogenesis•A conserved 10-nt sequence in the pgc 3′ UTR is required for its regulation•Pum and Bru, conserved RBPs, sequentially repress pgc translation via this sequence•A class of maternal RNAs are also regulated by Pum and Bru during oogenesis Flora et al. show that pgc, a germline determinant, is translationally regulated throughout oogenesis. Different conserved RBPs bind a 10-nt sequence in the 3′ UTR to continuously repress translation throughout oogenesis. This mode of regulation applies to a class of maternal mRNAs, including zelda, the activator of the zygotic genome.