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In Situ Detection of Ribonucleoprotein Complex Assembly in the C. elegans Germline using Proximity Ligation Assay
Published on: May 5, 2020
DPL-1 (DP) acts in the germ line to coordinate ovulation and fertilization in C. elegans
1Department of Genetics, Yale University School of Medicine, New Haven, CT 06510, USA.
Abstract:
Proper coordination of oogenesis, ovulation, and fertilization is essential for successful reproduction. In Caenorhabditis elegans, a strong loss-of-function mutation in dpl-1, which encodes a subunit of the E2F heterodimeric transcription factor EFL-1/DPL-1, causes severe defects during ovulation and fertilization. Here we demonstrate that the somatic gonad structure and sheath cell contraction rate appear normal in dpl-1 mutants, but that dilation of the spermatheca valve does not occur properly, causing oocytes to become trapped in the proximal gonad arm and enter endomitosis. This ovulation defect can be partially suppressed by increasing the activity of ITR-1, an inositol triphosphate receptor in the spermatheca that promotes dilation in response to IP(3) signaling. Tissue-specific rescue experiments demonstrate that expression of DPL-1 in germ cells but not the spermatheca can restore both ovulation and fertilization in dpl-1 mutants, indicating that the absence of DPL-1 likely disrupts a pro-ovulation signal originating in the oocyte that in turn stimulates the spermatheca. Moreover, we found that expression of a single EFL-1/DPL-1-responsive gene, rme-2, in the germ line of dpl-1 mutants significantly rescues ovulation, but not fertilization. Instead, other EFL-1/DPL-1-responsive genes function to promote successful fertilization. We propose that DPL-1 acts with EFL-1 in developing oocytes to directly regulate a transcriptional program that couples the critical events of ovulation and fertilization.
Insights
Successful reproduction requires coordinated oogenesis, ovulation, and fertilization. In C. elegans, mutations in dpl-1 disrupt ovulation by impairing oocyte signaling, trapping eggs and preventing fertilization.
Area of Science:
- Reproductive Biology
- Developmental Biology
- Genetics
Background:
- Successful reproduction depends on the precise coordination of oogenesis, ovulation, and fertilization.
- The E2F transcription factor heterodimer EFL-1/DPL-1 plays a critical role in these processes.
Purpose of the Study:
- To investigate the role of DPL-1 in ovulation and fertilization in Caenorhabditis elegans.
- To elucidate the molecular mechanisms by which DPL-1 regulates these reproductive events.
Main Methods:
- Analysis of dpl-1 loss-of-function mutants in C. elegans.
- Spermatheca valve dilation assays and sheath cell contraction rate measurements.
- Tissue-specific rescue experiments and gene expression analysis of EFL-1/DPL-1-responsive genes.
Main Results:
- dpl-1 mutants exhibit ovulation defects due to impaired spermatheca valve dilation, leading to oocyte entrapment and endomitosis.
- Increasing inositol triphosphate receptor (ITR-1) activity partially rescues ovulation.
- DPL-1 expression in germ cells, but not the spermatheca, rescues ovulation and fertilization, suggesting an oocyte-derived signal.
- Germline expression of the EFL-1/DPL-1-responsive gene rme-2 rescues ovulation, while other responsive genes are crucial for fertilization.
Conclusions:
- DPL-1 in developing oocytes regulates a transcriptional program essential for ovulation and fertilization.
- DPL-1 acts by signaling to the spermatheca to promote ovulation and by regulating other genes to ensure successful fertilization.
- This study reveals a novel mechanism by which oocyte-derived signals, regulated by DPL-1, coordinate key reproductive events.
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