Diversification of small RNA pathways underlies germline RNA interference incompetence in wild <i>Caenorhabditis elegans</i> strains

Chou, Han Ting; Valencia, Francisco; Alexander, Jacqueline C; Bell, Avery Davis; Deb, Diptodip; Pollard, Daniel A; Paaby, Annalise B

doi:10.1093/genetics/iyad191

Cited by 3 publications

(1 citation statement)

References 76 publications

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“…Secondary siRNAs are produced by an amplification machinery, for which different pools of primary siRNAs compete 15,35 , including endo-siRNAs dependent on Argonautes ERGO-1 and ALG-3/4, the genomically encoded piRNAs, and the siRNAs derived from exogenous double-stranded RNAs 13,16,[36][37][38] . Depending on the genomic and environmental contexts, genetic variation favoring one or the other primary siRNA pathway could have been selected [39][40][41][42] . Research in mammals has shown the importance of dosage of the orthologous MOV10 helicase on retrovirus silencing 43 .…”

Section: Phenotypic Effect Of the Structural Variation At Eri-6/7 On ...mentioning

confidence: 99%

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Zhang,

Félix,

Andersen

2024

Preprint

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Transposable elements (TEs) are parasitic DNA sequences that insert into the host genome and can cause alterations in host gene structure and expression. Host organisms cope with the often detrimental consequences caused by recent transposition and develop mechanisms that repress TE activities. In the nematode Caenorhabditis elegans, a small interfering RNA (siRNA) pathway dependent on the helicase ERI-6/7 primarily silences long terminal repeat retrotransposons and recent genes of likely viral origin. By studying gene expression variation among wild C. elegans strains, we discovered that structural variants and transposon remnants at the eri-6/7 locus alter its expression in cis and underlie a trans-acting expression quantitative trait locus affecting non-conserved genes and pseudogenes. Multiple insertions of the Polinton DNA transposon (also known as Mavericks) reshuffled the eri-6/7 locus in different configurations, separating the eri-6 and eri-7 exons and causing the inversion of eri-6 as seen in the reference N2 genome. In the inverted configuration, gene function was previously shown to be repaired by unusual trans-splicing mediated by direct repeats flanking the inversion. We show that these direct repeats originated from terminal inverted repeats specific to C. elegans Polintons. This trans-splicing event occurs infrequently compared to cis-splicing to novel downstream exons, thus affecting the production of ERI-6/7. Diverse Polinton-induced structural variations display regulatory effects within the locus and on targets of ERI-6/7-dependent siRNA pathways. Our findings highlight the role of host-transposon interactions in driving rapid host genome diversification among natural populations and shed light on evolutionary novelty in genes and splicing mechanisms.

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Section: Phenotypic Effect Of the Structural Variation At Eri-6/7 On ...mentioning

confidence: 99%

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Zhang,

Félix,

Andersen

2024

Preprint

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Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Zhang,

Félix,

Andersen

2024

Sci. Adv.

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Transposable elements (TEs) can alter host gene structure and expression, whereas host organisms develop mechanisms to repress TE activities. In the nematode Caenorhabditis elegans , a small interfering RNA pathway dependent on the helicase ERI-6/7 primarily silences retrotransposons and recent genes of likely viral origin. By studying gene expression variation among wild C. elegans strains, we found that structural variants and transposon remnants likely underlie expression variation in eri-6/7 and the pathway targets. We further found that multiple insertions of the DNA transposons, Polintons, reshuffled the eri-6/7 locus and induced inversion of eri-6 in some wild strains. In the inverted configuration, gene function was previously shown to be repaired by unusual trans-splicing mediated by direct repeats. We identified that these direct repeats originated from terminal inverted repeats of Polintons . Our findings highlight the role of host-transposon interactions in driving rapid host genome diversification among natural populations and shed light on evolutionary novelty in genes and splicing mechanisms.

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Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

Frézal,

Saglio,

Zhang

et al. 2023

EMBO Reports

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The animal germline lineage needs to be maintained along generations. However, some Caenorhabditis elegans wild isolates display a mortal germline phenotype, leading to sterility after several generations at 25°C. Using a genome‐wide association approach, we detect a significant peak on chromosome III around 5 Mb, confirmed by introgressions. Thus, a seemingly deleterious genotype is maintained at intermediate frequency in the species. Environmental rescue is a likely explanation, and indeed associated bacteria and microsporidia suppress the phenotype of wild isolates as well as mutants in small RNA inheritance (nrde‐2) and histone modifications (set‐2). Escherichia coli strains of the K‐12 lineage suppress the phenotype compared to B strains. By shifting a wild strain from E. coli K‐12 to E. coli B, we find that memory of the suppressing condition is maintained over several generations. Thus, the mortal germline phenotype of wild C. elegans is in part revealed by laboratory conditions and may represent variation in epigenetic inheritance and environmental interactions. This study also points to the importance of non‐genetic memory in the face of environmental variation.

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Diversification of small RNA pathways underlies germline RNA interference incompetence in wild Caenorhabditis elegans strains

Cited by 3 publications

References 76 publications

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

Genome‐wide association and environmental suppression of the mortal germline phenotype of wild C. elegans

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