piRNAs initiate transcriptional silencing of spermatogenic genes during C. elegans germline development

Cornes, Eric; Bourdon, Loan; Singh, Meetali; Mueller, Florian; Quarato, Piergiuseppe; Wernersson, Erik; Bienko, Magda; Li, Blaise; Cecere, Germano

doi:10.1016/j.devcel.2021.11.025

Cited by 31 publications

(32 citation statements)

References 75 publications

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“…This result is consistent with the model that piRNA targeting induces the production of 22G-RNAs which are then loaded into WAGO-1 and HRDE-1 (Lee et al, 2012;Cornes et al, 2022). Our complete analysis reveals that PPW-1 and PPW-2 also work within the context of PRG-1 targeting.…”

Section: Hierarchy and Interconnected Regulation Of Multiple Srna Pat...supporting

confidence: 90%

A Comprehensive Survey of C. elegans Argonaute Proteins Reveals Organism-wide Gene Regulatory Networks and Functions

Seroussi

Lugowski

Wadi

et al. 2022

Preprint

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Argonaute (AGO) proteins associate with small RNAs to direct their effector function on complementary transcripts. The nematode C. elegans contains an expanded family of 19 functional AGO proteins, many of which have not been fully characterized. In this work we systematically analyzed every C. elegans AGO, using CRISPR-Cas9 genome editing to introduce GFP::3xFLAG tags. We have characterized the expression patterns of each AGO throughout development, identified small RNA binding complements, and determined the effects of ago loss on small RNA populations and developmental phenotypes. Our analysis indicates stratification of subsets of AGOs into distinct regulatory modules, and integration of our data led us to uncover novel stress-induced fertility and pathogen response phenotypes due to ago loss.

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Section: Hierarchy and Interconnected Regulation Of Multiple Srna Pat...supporting

confidence: 90%

A Comprehensive Survey of C. elegans Argonaute Proteins Reveals Organism-wide Gene Regulatory Networks and Functions

Seroussi

Lugowski

Wadi

et al. 2022

Preprint

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“…3 E).This subpackage further permits us to perform localization of RNAs with subpixel accuracy by using a Gaussian fitting ( Mueller et al 2013 ). Lastly, we provide the possibility to perform a colocalization analysis between spot detection performed in multiple channels ( Cornes et al 2021 ).…”

Section: Resultsmentioning

confidence: 99%

FISH-quant v2: a scalable and modular tool for smFISH image analysis

Imbert

Ouyang

Safieddine

et al. 2022

RNA

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Regulation of RNA abundance and localization is a key step in gene expression control. Single-molecule RNA fluorescence in-situ hybridization (smFISH) is a widely used single-cell-single-molecule imaging technique enabling quantitative studies of gene expression and its regulatory mechanisms. Today, these methods are applicable at a large scale, which in turn come with a need for adequate tools for data analysis and exploration. Here, we present FISH-quant v2, a highly modular tool accessible for both experts and non-experts. Our user-friendly package allows the user to segment nuclei and cells, detect isolated RNAs, decompose dense RNA clusters, quantify RNA localization patterns and visualize these results both at the single-cell level and variations within the cell population. This tool was validated and applied on large-scale smFISH image datasets, revealing diverse subcellular RNA localization patterns and a surprisingly high degree of cell-to-cell heterogeneity.

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“…Our analyses indicate that CSR-1 binding at various locations in a transcript can result in the protection of the entire transcript from piRNA recognition (Figure 6). Indeed, a recent report has shown that tethering of CSR-1 to a single locus at the 3’ UTR of an endogenous mRNA can protect that mRNA from piRNA silencing (34). In addition, our analyses reveal that CSR-1 targeted regions are locally protected against WAGO 22G-RNA production (Figure 6).…”

Section: Discussionmentioning

confidence: 99%

Transcriptome-wide analysis suggests piRNAs preferentially recognize the coding region of mRNAs in C. elegans

Brown

Shiue

et al. 2022

Preprint

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Background: PIWI-interacting RNAs (piRNAs) protect genome integrity by silencing transposon mRNAs and some endogenous mRNAs in various animals. However, C. elegans piRNAs fail to trigger gene silencing at many sequence-based predicted targeting sites. Results: To gain insights into the mechanisms that control piRNA silencing capability, we compared the transcriptome-wide predicted piRNA targeting sites to the in vivo piRNA binding sites. Surprisingly, while predicted piRNA targeting sites are enriched in 3' UTRs, we found that C. elegans piRNAs preferentially bind to coding regions (CDS) of target mRNAs, leading to preferential production of secondary silencing small RNAs in the CDS. Furthermore, our analyses suggest that Argonaute protein CSR-1 protects mRNAs from piRNA silencing through two distinct mechanisms - by inhibiting piRNA binding across the entire CSR-1 targeted transcript, and by inhibiting secondary silencing small RNA production locally at CSR-1 bound sites. However, CSR-1 is not responsible for the piRNA binding preference for the CDS. Conclusions: Our work identifies the CDS as the critical region that is uniquely competent for piRNA silencing in C. elegans. We speculate that the preference for CDS recognition by piRNAs may represent a mechanism to counteract the evolution of foreign protein-coding RNAs that evade piRNA surveillance.

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piRNAs initiate transcriptional silencing of spermatogenic genes during C. elegans germline development

Cited by 31 publications

References 75 publications

A Comprehensive Survey of C. elegans Argonaute Proteins Reveals Organism-wide Gene Regulatory Networks and Functions

A Comprehensive Survey of C. elegans Argonaute Proteins Reveals Organism-wide Gene Regulatory Networks and Functions

FISH-quant v2: a scalable and modular tool for smFISH image analysis

Transcriptome-wide analysis suggests piRNAs preferentially recognize the coding region of mRNAs in C. elegans

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