Diversity of RNA interference pathways in regulation of endogenous and exogenous sequences expression in ciliates Tetrahymena and Paramecium

Nekrasova, Irina; Потехин, А. А.

doi:10.17816/ecogen172113-125

Cited by 5 publications

(7 citation statements)

References 35 publications

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“…Interestingly, the emergence of this mechanism appears to be a by-product of preexisting biological features that are already likely to be under strong selective pressure. For instance, the essential RNAi system of the host, which in some ciliates can function in exogenous RNA processing, transposon elimination, nuclear rearrangement and transcriptional regulation ( 43 – 46 , 48 , 53 , 68 – 71 ). Or, furthermore, the conserved gene repertoire and sequence composition of the host and endosymbiont transcriptomes from which some “RNAi collisions” have here been identified [including many transcripts which are conditionally essential in other systems ( 61 )].…”

Section: Discussionmentioning

confidence: 99%

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Jenkins

Maguire

Leonard

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryote–eukaryote endosymbiosis was responsible for the spread of chloroplast (plastid) organelles. Stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms that act to stabilize emergent endosymbioses—between two fundamentally selfish biological organisms—are unclear. Theory suggests that enforcement mechanisms, which punish misbehavior, may act to stabilize such interactions by resolving conflict. However, how such mechanisms can emerge in a facultative endosymbiosis has yet to be explored. Here, we propose that endosymbiont–host RNA–RNA interactions, arising from digestion of the endosymbiont population, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model facultative endosymbiosis between Paramecium bursaria and Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) system. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived messenger RNA (mRNA) released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We predict multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate through delivery of synthetic endosymbiont sRNA that exposure to these regions can knock down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knockdown in response to endosymbiont-derived RNA processing by host RNAi factors, which we term “RNAi collisions,” represents a mechanism that can promote stability in a facultative eukaryote–eukaryote endosymbiosis. Specifically, by imposing a cost for breakdown of the endosymbiosis, endosymbiont–host RNA–RNA interactions may drive maintenance of the symbiosis across fluctuating ecological conditions.

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Section: Discussionmentioning

confidence: 99%

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Jenkins

Maguire

Leonard

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…In ciliates, multiple whole genome duplication (WGD) events have led to the rapid expansion of gene families encoding RNAi components [38][39][40], resulting in a subsequent diversification of protein function. Example functions include transposon elimination, nuclear rearrangement and transcriptional regulation [32,35,[41][42][43][44][45]. Elegant investigation of the non-photo-endosymbiotic model system, Paramecium tetraurelia, has identified three distinct classes of RNAi pathway in Paramecium.…”

Section: Introductionmentioning

confidence: 99%

“…28-nt) pathways are endogenous, and function primarily to eliminate the bulk of non-coding DNA present in the germline micronuclear genome during development of the somatic macronucleus [35,[41][42][43]46,47]. Paramecium also encodes a short-interfering (si)RNA (23-nt) pathway capable of processing both exogenously [48][49][50][51] and endogenously [32,44] derived RNA precursors. Although siRNA is believed to have evolved to protect against foreign genetic elements (such as viruses, transposons and transgenes) [52], some siRNA-based RNAi factors have also been implicated in the regulation of endogenous transcriptome expression in the non-photo-endosymbiotic model system, P. tetraurelia [32].…”

Section: Introductionmentioning

confidence: 99%

Characterization of the RNA-interference pathway as a tool for reverse genetic analysis in the nascent phototrophic endosymbiosis, Paramecium bursaria

et al. 2021

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Endosymbiosis was fundamental for the evolution of eukaryotic complexity. Endosymbiotic interactions can be dissected through forward- and reverse-genetic experiments, such as RNA-interference (RNAi). However, distinguishing small (s)RNA pathways in a eukaryote–eukaryote endosymbiotic interaction is challenging. Here, we investigate the repertoire of RNAi pathway protein-encoding genes in the model nascent endosymbiotic system, Paramecium bursaria–Chlorella spp. Using comparative genomics and transcriptomics supported by phylogenetics, we identify essential proteome components of the small interfering (si)RNA, scan (scn)RNA and internal eliminated sequence (ies)RNA pathways. Our analyses reveal that copies of these components have been retained throughout successive whole genome duplication (WGD) events in the Paramecium clade. We validate feeding-induced siRNA-based RNAi in P. bursaria via knock-down of the splicing factor, u2af1 , which we show to be crucial to host growth. Finally, using simultaneous knock-down ‘paradox’ controls to rescue the effect of u2af1 knock-down, we demonstrate that feeding-induced RNAi in P. bursaria is dependent upon a core pathway of host-encoded Dcr1 , Piwi and Pds1 components. Our experiments confirm the presence of a functional, host-derived RNAi pathway in P. bursaria that generates 23-nt siRNA, validating the use of the P. bursaria – Chlorella spp. system to investigate the genetic basis of a nascent endosymbiosis.

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“…The ciliate-specific scan (scn)RNA (25-nt) and internal eliminated sequence (ies)RNA (~28-nt) pathways are endogenous, and function primarily to eliminate the bulk of noncoding DNA present in the germline micronuclear genome during development of the somatic macronucleus 35,[41][42][43]46,47 . Paramecium also encodes a shortinterfering (si)RNA (23-nt) pathway capable of processing both exogenously [48][49][50][51] and endogenously 32,44 derived RNA precursors. Although siRNA is believed to have evolved to protect against foreign genetic elements (such as viruses, transposons and transgenes) 52 , some siRNA-based RNAi factors have also been implicated in the regulation of endogenous transcriptome expression in the non-photo-endosymbiotic model system, P. tetraurelia 32 .…”

Section: Introductionmentioning

confidence: 99%

“…Paramecium also encodes a short-interfering (si)RNA (23-nt) pathway capable of processing both exogenously [48][49][50][51] and endogenously 32,44 derived RNA precursors. Although siRNA is believed to have evolved to protect against foreign genetic elements (such as viruses, transposons and transgenes) 52 , some siRNA-based RNAi factors have also been implicated in the regulation of endogenous transcriptome expression in the non-photo-endosymbiotic model system, P. tetraurelia 32 .…”

Section: Introductionmentioning

confidence: 99%

Characterisation of the RNA-interference pathway as a Tool for Genetics in the Nascent Phototrophic Endosymbiosis,Paramecium bursaria

Jenkins

Maguire

Leonard

et al. 2020

Preprint

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Endosymbiosis was fundamental for the evolution of eukaryotic complexity. Endosymbiotic interactions can be dissected through forward and reverse-genetic experiments, such as RNA-interference (RNAi). However, distinguishing small (s)RNA pathways in a eukaryote-eukaryote endosymbiotic interaction is challenging. Here, we investigate the repertoire of RNAi pathway protein-encoding genes in the model nascent endosymbiotic system, Paramecium bursaria–Chlorella spp. Using comparative genomics and transcriptomics supported by phylogentics, we identify essential proteome components of the small interfering (si)RNA, scan (scn)RNA, and internal eliminated sequence (ies)RNA pathways. Our analyses reveal that copies of these components have been retained throughout successive whole genome duplication (WGD) events in the Paramecium clade. We then validate feeding-induced siRNA-based RNAi in P. bursaria via knock-down of the splicing factor, u2af1, which we show to be crucial to host growth. Finally, using simultaneous knock-down paradox controls to rescue the effect u2af1 knock-down, we demonstrate that feeding-induced RNAi in P. bursaria is dependent upon a core pathway of host-encoded Dcr1, Piwi and Pds1 components. Our experiments confirm the presence of a functional, host-derived RNAi pathway in P. bursaria that generates 23-nt siRNA, validating use of the P. bursaria-Chlorella spp. system to investigate the genetic basis of a nascent endosymbiosis.

show abstract

Diversity of RNA interference pathways in regulation of endogenous and exogenous sequences expression in ciliates Tetrahymena and Paramecium

Cited by 5 publications

References 35 publications

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Characterization of the RNA-interference pathway as a tool for reverse genetic analysis in the nascent phototrophic endosymbiosis, Paramecium bursaria

Characterisation of the RNA-interference pathway as a Tool for Genetics in the Nascent Phototrophic Endosymbiosis,Paramecium bursaria

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