The origin of RNA interference: Adaptive or neutral evolution?

Torri, Alessandro; Jaeger, Johannes; Pradeu, Thomas; Saleh, María-Carla

doi:10.1371/journal.pbio.3001715

Cited by 25 publications

(18 citation statements)

References 169 publications

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“…However, they may illustrate the two facets of RNA interference, i.e . defense vs regulation (Torri et al, 2022). We may speculate that in D. simulans , the defense facet appears prominent while the regulation prevails in D. melanogaster .…”

Section: Discussionmentioning

confidence: 99%

A quantitative, genome-wide analysis inDrosophilareveals transposable elements’ influence on gene expression is species-specific

Fablet

Salces-Ortiz

Jacquet

et al. 2022

Preprint

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Transposable elements (TEs) are parasite DNA sequences that are able to move and multiply along the chromosomes of all genomes. They are controlled by the host through the targeting of silencing epigenetic marks, which may affect the chromatin structure of neighboring sequences, including genes. In this study, we used transcriptomic and epigenomic high-throughput data produced from ovarian samples of Drosophila melanogaster and Drosophila simulans wild-type strains, in order to finely quantify the influence of TE insertions on gene RNA levels and histone marks (H3K4me3 and H3K9me3) enrichments. We find general, negative impacts of TE insertions on gene RNA levels and H3K4me3 enrichments, which intensity varies according to the localization of the TE insertion. We also uncover that TE insertions within exons are associated with a reduction in H3K9me3 enrichments, which we propose is associated with TE splicing out. Overall, we find that gene RNA and histone mark levels show contrasted dependencies on TE insertions regarding the species. The fold-decrease in TE-carrying gene proportions between extreme expression classes is 2.6 in D. melanogaster and 1.8 in D. simulans, while it is strongly contrasted between extreme classes of H3K4me3 enrichments: 4.4 in D. melanogaster and 19.2 in D. simulans. This provide a new light on the considerable natural variability provided by TEs, which may be associated with contrasted adaptive and evolutionary potentials.

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Section: Discussionmentioning

confidence: 99%

A quantitative, genome-wide analysis inDrosophilareveals transposable elements’ influence on gene expression is species-specific

Fablet

Salces-Ortiz

Jacquet

et al. 2022

Preprint

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“…The RNAi pathway has diversified extensively since its emergence around the time of the last eukaryotic common ancestor (Torri et al 2022). Functions range from gene regulation to genome defense, but in some specific instances the machinery has been lost to provide a growth advantage (Billmyre et al 2013).…”

Section: Resultsmentioning

confidence: 99%

“…RNA interference (RNAi) is a conserved molecular mechanism that was likely intact in the last common ancestor of modern eukaryotes (Shabalina and Koonin 2008;Torri et al 2022). RNAi uses small RNA (sRNA) molecules to suppress gene expression either transcriptionally by heterochromatin recruitment or post-transcriptionally through sequence-specific messenger RNA (mRNA) degradation or translational interference (Moazed 2009;Dang et al 2011;Torres-Martinez and Ruiz-Vazquez 2017).…”

Section: Introductionmentioning

confidence: 99%

Disruption of theAspergillus fumigatusRNA interference machinery alters the conidial transcriptome

Kelani

Bruch

Rivieccio

et al. 2023

RNA

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The RNA interference (RNAi) pathway has evolved numerous functionalities in eukaryotes, with many on display in Kingdom Fungi. RNAi can regulate gene expression, facilitate drug resistance, or even be altogether lost to improve growth potential in some fungal pathogens. In the WHO fungal priority pathogen,Aspergillus fumigatus, the RNAi system is known to be intact and functional. To extend our limited understanding ofA. fumigatus RNAi, we first investigated the genetic variation in RNAi-associated genes in a collection of 217 environmental and 83 clinical genomes, where we found that RNAi components are conserved even in clinical strains. Using endogenously expressed inverted-repeat transgenes complementary to a conditionally essential gene (pabA) or a nonessential gene (pksP), we determined that a subset of the RNAi componentry is active in inverted-repeat transgene silencing in conidia and mycelium. Analysis of mRNA-seq data from RNAi double-knockout strains linked theA. fumigatusdicer-like enzymes (DclA/B) and RNA-dependent RNA polymerases (RrpA/B) to regulation of conidial ribosome biogenesis genes; however, surprisingly few endogenous small RNAs were identified in conidia that could explain this broad change. Although RNAi was not clearly linked to growth or stress response defects in the RNAi knockouts, serial passaging of RNAi knockout strains for six generations resulted in lineages with diminished spore production over time, indicating that loss of RNAi can exert a fitness cost on the fungus. Cumulatively,A. fumigatus RNAiappears to play an active role in defense against double-stranded RNA species alongside a previously unappreciated housekeeping function in regulation of conidial ribosomal biogenesis genes.

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“…Additionally, metazoan PIWI-interacting RNA (piRNA) guides are generated from longer single-stranded RNA by Zucchini, to suppress transposable elements (TEs) 9 . Both the arms race against TEs and global gene silencing are critical drivers of eukaryotic genome evolution [10][11][12][13][14][15] . As such, the origin and differentiation of AGO and PIWI have broad implications for the emergence and expansion of the eukaryotic tree of life.…”

Section: Mainmentioning

confidence: 99%

RNA-guided RNA silencing by an Asgard archaeal Argonaute

Bastiaanssen,

Ugarte,

Kim

et al. 2023

Preprint

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Eukaryotic Argonaute proteins achieve gene repression and defense against viruses and transposons by RNA-guided RNA silencing. By contrast, known prokaryotic Argonautes adopt single-stranded DNA as guides and/or targets, leaving the evolutionary origin of RNA-guided RNA silencing elusive. Here, we show an evolutionary expansion of Asgard archaeal Argonautes (asAgos), including the discovery of HrAgo1 from the Lokiarchaeon ‘CandidatusHarpocratesius repetitus’ that shares a common origin with eukaryotic PIWI proteins. HrAgo1 exhibits RNA-guided RNA cleavagein vitroand RNA silencing in human cells. The cryo-EM structure of HrAgo1 combined with quantitative single-molecule experiments reveals that HrAgo1 possesses hybrid structural features and target binding modes bridging those of the eukaryotic AGO and PIWI clades. Finally, genomic evidence suggests that eukaryotic Dicer-like processing of double-stranded RNA likely emerged as a mechanism of generating guide RNA for asAgos prior to eukaryogenesis. Our study provides new insights into the evolutionary origin and plasticity of Argonaute-based RNA silencing.

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The origin of RNA interference: Adaptive or neutral evolution?

Cited by 25 publications

References 169 publications

A quantitative, genome-wide analysis inDrosophilareveals transposable elements’ influence on gene expression is species-specific

A quantitative, genome-wide analysis inDrosophilareveals transposable elements’ influence on gene expression is species-specific

Disruption of theAspergillus fumigatusRNA interference machinery alters the conidial transcriptome

RNA-guided RNA silencing by an Asgard archaeal Argonaute

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