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Low input ribosome profiling reveals stage-specific translational regulation during early C. elegans embryogenesis

ABSTRACT: Translation of maternal mRNAs guides early embryonic development. C. elegans embryos exhibit an invariant cell lineage from the first division, offering a unique opportunity to trace the impact of post-transcriptional gene regulation on subsequent embryonic development. Although prior work has explored the translation of a select few transcripts, we lack a transcriptome-wide view of translation control during early embryogenesis. We developed a method for low-input ribosome profiling and combined it with low-input RNA sequencing to measure new protein translation during the first four cell cycles of C. elegans embryogenesis. Strikingly, our results show a poor correlation between RNA abundance and ribosome occupancy in this system compared to other model systems, emphasizing the predominant role of variation in translation efficiency in this system. We found numerous translationally regulated transcripts that had not been previously identified. Housekeeping genes involved in ribosome function and biogenesis were stably translated throughout the studied stages, while genes involved in mRNA processing and mRNA binding are dynamically regulated, consistent with roles in cell fate specification. A gain-of-function mutation in a known translational repressor protein, OMA-1, stalls the developmental program by preventing the translational remodeling that should occur at the 2-cell stage. These insights advance our understanding of the post-transcriptional regulatory mechanisms that shape the embryonic proteome and direct cell differentiation, and provide a valuable resource studies of C. elegans development.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE281412 | GEO | 2025/02/14

REPOSITORIES: GEO

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mRNAs that co-purify with OMA-1 in the C. elegans germline (sequencing)

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2014-09-29 | E-GEOD-54517 | biostudies-arrayexpress

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Project description:The oocytes of most animals arrest at diplotene or diakinesis, but resume meiosis (meiotic maturation) in response to hormones. In C. elegans, maturation of the –1 oocyte requires the presence of sperm, Gas-adenylate cyclase-PKA signaling in the gonadal sheath cells, and germline function of two Tis11-like CCCH zinc-finger proteins, OMA-1 and OMA-2 (OMA proteins). Prior studies indicate that the OMA proteins redundantly repress the translation of specific mRNAs in oocytes (zif-1, mom-2, nos-2, glp-1) and early embryos (mei-1). We purified OMA-1-containing ribonucleoprotein particles (RNPs) and identified mRNAs that associate with OMA-1 in oocytes using microarrays. We examined the relative abundances of mRNAs in OMA-1 RNPs using high-throughput RNA sequencing. Previously identified targets of OMA-dependent translational repression in oocytes were found to be both enriched (>2-fold relative to input RNA) and abundant in purified OMA-1 RNPs. Furthermore, we verified that some of the newly identified mRNAs that share these characteristics are translationally repressed by OMA-1/2 in oocytes through sequences in their 3’UTRs. Although meiotic maturation is stimulated by sperm, we found that the mRNAs copurifying with OMA-1 are not significantly different in the presence and absence of sperm, suggesting that sperm-dependent signaling does not modify the suite of mRNAs stably associated with OMA-1. Further, several tested OMA-1-associated mRNAs were shown to be translationally repressed in both the presence and absence of sperm. RNA co-purifiying with OMA-1 (IP RNA) was isolated and compared to total lysate RNA (input RNA). Immunopurifications were performed, in triplicate, from lysates made from two different sterile strains. Sterile fog-1 adults lack sperm. Sterile spe-9 adults contain fertilization-incompetent sperm that promote meiotic maturation.

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Low input ribosome profiling reveals stage-specific translational regulation during early C. elegans embryogenesis

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