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Translational regulation of mRNAs for ribosomal proteins during early Drosophila development
Abstract:
In Drosophila, the vast majority of mRNAs that are polysome associated during oogenesis are also polysome associated during early embryogenesis. We have previously identified an exceptional mRNA that appears to be depleted from early-embryo polysomes [Fruscoloni, P., Al-Atia, G. R., & Jacobs-Lorena, M. (1983) Proc. Natl. Acad. Sci. U.S.A. 80, 3359-3363]. This mRNA has been subsequently identified as coding for a ribosomal protein (r-protein) [Kay, M., & Jacobs-Lorena, M. (1985) Mol. Cell. Biol. (in press)]. Changes in association with polysomes of two r-protein mRNAs during early Drosophila development were investigated for this report. Hybridization of cloned DNA probes to blots of RNA obtained from sucrose gradient fractions reveals that r-protein mRNAs are substantially associated with polysomes during oogenesis, depleted from polysomes during early embryogenesis, and again polysome associated during late embryogenesis. Thus, translation of r-protein mRNAs parallels transcription of ribosomal RNA (rRNA) during this time of development. By contrast, no such differences were observed when actin and histone probes were used as controls and hybridized to the same blots. The abundance of mRNAs for r-proteins as a function of development was also measured. Abundance was relatively high and constant during oogenesis and embryogenesis (when translational regulation is apparent), somewhat decreased in larval and pupal stages, and low in adult nonovarian tissues. Coordination between r-protein and rRNA synthesis appears to be achieved by regulating translation of r-protein mRNAs in early embryos and by decreasing their abundance in adult tissues.
Insights
Ribosomal protein (r-protein) mRNAs in Drosophila are translated during oogenesis and late embryogenesis but not early embryogenesis. This translational regulation, alongside abundance changes, coordinates r-protein synthesis with ribosomal RNA (rRNA) production.
Area of Science:
- Developmental Biology
- Molecular Biology
- Genetics
Background:
- Most mRNAs associated with polysomes during Drosophila oogenesis remain associated during early embryogenesis.
- A specific mRNA, later identified as coding for a ribosomal protein (r-protein), was found to be an exception, depleted from early-embryo polysomes.
Purpose of the Study:
- To investigate the changes in polysome association of two r-protein mRNAs during early Drosophila development.
- To measure the abundance of r-protein mRNAs throughout different developmental stages.
Main Methods:
- Hybridization of cloned DNA probes to RNA from sucrose gradient fractions.
- Analysis of polysome association of r-protein mRNAs during oogenesis, early embryogenesis, and late embryogenesis.
- Measurement of r-protein mRNA abundance across various developmental stages (oogenesis, embryogenesis, larval, pupal, adult).
Main Results:
- r-protein mRNAs are polysome-associated during oogenesis and late embryogenesis but depleted during early embryogenesis.
- Translational regulation of r-protein mRNAs parallels ribosomal RNA (rRNA) transcription.
- Actin and histone mRNAs did not show similar polysome association changes.
- r-protein mRNA abundance is high and constant during oogenesis and embryogenesis, decreases in larval/pupal stages, and is low in adult non-ovarian tissues.
Conclusions:
- Drosophila coordinates ribosomal protein synthesis with rRNA production through translational regulation of r-protein mRNAs in early embryos.
- Decreased abundance of r-protein mRNAs in adult tissues further contributes to the regulation of ribosomal protein synthesis.
- This study highlights a sophisticated mechanism for balancing protein synthesis with developmental needs.