Novel roles for RNA binding proteins squid, hephaesteus, and Hrb27C in Drosophila oogenesis

Finger, Danielle S.; Williams, Anna E.; Holt, Vivian V.; Ables, Elizabeth T.

doi:10.1002/dvdy.550

Cited by 4 publications

(1 citation statement)

References 84 publications

(188 reference statements)

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“…In addition, SQD-1 has also been reported to physically interact with GLD-1 (Akay and others 2013), an RBP critical to regulate RNA patterning and translational repression in the germline (Scheckel and others 2012). Drosophila squid is known to direct embryo patterning via RNA localization (Clouse and others 2008; Goodrich and others 2004; Kelley 1993; Lall and others 1999; Norvell and others 1999) and has recently been shown to be required for germline stem cell maintenance (Finger and others 2023). Here, we report the first examination of the effects of depleting sqd-1 on germline morphology and gene expression.…”

Section: Introductionmentioning

confidence: 99%

ADR-2 regulates fertility and oocyte fate inC. elegans

Erdmann,

Forbes,

Becker

et al. 2023

Preprint

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RNA binding proteins play essential roles in coordinating germline gene expression and development in all organisms. Characterization of gross fertility defects, such as sterility, has identified RNA binding proteins that are critical regulators of germline gene expression; however, broader screens for RNA binding proteins involved in specific reproductive processes are lacking. Here, a reverse genetic screen was performed to identify RNA binding proteins that impact yolk and embryo production inCaenorhabditis eleganshermaphrodites. This screen makes use of animals expressing a vitellogenin (yolk protein) fusion with green fluorescent protein, in a genetic background that corrects for a previously identified fertility defect in this strain. From this screen, we identified 23 RNA binding proteins that regulate embryo production inCaenorhabditis elegans. This screen lays groundwork for future interrogations into the molecular roles of these proteins in yolk production and embryogenesis. Additionally, the screen uncovered a genetic interaction between ADR-2, a member of the Adenosine DeAminase Acting on RNA (ADAR) family, and SQD-1, a member of the heterogenous nuclear ribonucleoprotein (hnRNP) family. Transcriptome-wide assessment in animals depleted ofsqd-1revealed over 8000 misregulated transcripts, suggesting SQD-1 is a major regulator of gene expression. Consistent with this, microscopy and reproductive assays reveal thatsqd-1is essential for oogenesis. In the absence ofadr-2, the effects of loss ofsqd-1on gene expression are attenuated, as well as the defects in oogenesis. Together, these data indicate that both ADR-2 and SQD-1 are important regulators of germline gene expression and oogenesis.Article SummaryThe molecular information that controls early development is RNA. Interactions between RNA and RNA binding proteins are critical for successful reproduction across species. In this study, over 250 RNA binding proteins were assessed for effects on yolk and embryo production inCaenorhabditis elegans. Twenty-three regulators of these important reproductive steps were identified, including 7 novel regulators. This screen also revealed a genetic interaction between two RNA binding proteins, SQD-1 and ADR-2, which impacts germline gene expression, oogenesis, and fertility.

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Section: Introductionmentioning

confidence: 99%

ADR-2 regulates fertility and oocyte fate inC. elegans

Erdmann,

Forbes,

Becker

et al. 2023

Preprint

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Single-cell profiling of Anopheles gambiae spermatogenesis defines the onset of meiotic silencing and premeiotic overexpression of the X chromosome

et al. 2023

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Understanding development and genetic regulation in the Anopheles gambiae germline is essential to engineer effective genetic control strategies targeting this malaria mosquito vector. These include targeting the germline to induce sterility or using regulatory sequences to drive transgene expression for applications such as gene drive. However, only very few germline-specific regulatory elements have been characterised with the majority showing leaky expression. This has been shown to considerably reduce the efficiency of current genetic control strategies, which rely on regulatory elements with more tightly restricted spatial and/or temporal expression. Meiotic silencing of the sex chromosomes limits the flexibility of transgene expression to develop effective sex-linked genetic control strategies. Here, we build on our previous study, dissecting gametogenesis into four distinct cell populations, using single-cell RNA sequencing to define eight distinct cell clusters and associated germline cell–types using available marker genes. We reveal overexpression of X-linked genes in a distinct cluster of pre-meiotic cells and document the onset of meiotic silencing of the X chromosome in a subcluster of cells in the latter stages of spermatogenesis. This study provides a comprehensive dataset, characterising the expression of distinct cell types through spermatogenesis and widening the toolkit for genetic control of malaria mosquitoes.

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ADR-2 regulates fertility and oocyte fate in Caenorhabditis elegans

Erdmann,

Forbes,

Becker

et al. 2024

Genetics

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RNA binding proteins play essential roles in coordinating germline gene expression and development in all organisms. Here, we report that loss of ADR-2, a member of the Adenosine DeAminase acting on RNA (ADAR) family of RNA binding proteins and the sole adenosine-to-inosine RNA editing enzyme in C. elegans, can improve fertility in multiple genetic backgrounds. First, we show that loss of RNA editing by ADR-2 restores normal embryo production to subfertile animals that transgenically express a vitellogenin (yolk protein) fusion to green fluorescent protein. Using this phenotype, a high-throughput screen was designed to identify RNA binding proteins that when depleted yield synthetic phenotypes with loss of adr-2. The screen uncovered a genetic interaction between ADR-2 and SQD-1, a member of the heterogenous nuclear ribonucleoprotein (hnRNP) family of RNA binding proteins. Microscopy, reproductive assays, and high-throughput sequencing reveal that sqd-1 is essential for the onset of oogenesis and oogenic gene expression in young adult animals, and that loss of adr-2 can counteract the effects of loss of sqd-1 on gene expression and rescue the switch from spermatogenesis to oogenesis. Together, these data demonstrate that ADR-2 can contribute to the suppression of fertility and suggest novel roles for both RNA editing-dependent and independent mechanisms in regulating embryogenesis.

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Novel roles for RNA binding proteins squid, hephaesteus, and Hrb27C in Drosophila oogenesis

Cited by 4 publications

References 84 publications

ADR-2 regulates fertility and oocyte fate inC. elegans

ADR-2 regulates fertility and oocyte fate inC. elegans

Single-cell profiling of Anopheles gambiae spermatogenesis defines the onset of meiotic silencing and premeiotic overexpression of the X chromosome

ADR-2 regulates fertility and oocyte fate in Caenorhabditis elegans

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