Functional lability of RNA-dependent RNA polymerases in animals

RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require...

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Published inPLoS genetics Vol. 15; no. 2; p. e1007915
Main Authors Pinzón, Natalia, Bertrand, Stéphanie, Subirana, Lucie, Busseau, Isabelle, Escrivá, Hector, Seitz, Hervé
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 19.02.2019
Public Library of Science (PLoS)
Subjects
Animal genetics
Animals
Biology and life sciences
Branchiostoma
Developmental stages
EDTA
Eukaryotes
Functional plasticity
Fungi
Genes
Genetic research
Genetics
Genomes
Insects
Lability
Life Sciences
MicroRNAs
Nematodes
Nucleotide sequence
Physiological aspects
Proteins
RNA
RNA interference
RNA polymerase
RNA polymerases
RNA-mediated interference
Roundworms
siRNA
France
United States > US
Online AccessGet full text
ISSN1553-7404
1553-7390
1553-7404
DOI10.1371/journal.pgen.1007915

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Abstract RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways.
AbstractList RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum ), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways. RNA interference (RNAi) is a conserved gene regulation system in eukaryotes. In non-animal eukaryotes, it necessitates RNA-dependent RNA polymerases (“RdRPs”). Among animals, only nematodes appear to require RdRPs for RNAi. Yet additional animal clades have RdRPs and it is assumed that they participate in RNAi. Here, we find that RdRPs are much more common in animals than previously thought, but their genes were independently lost in many lineages. Focusing on a species with RdRP genes (a cephalochordate), we found that it does not use them for RNAi. While RNAi is the only known function for eukaryotic RdRPs, our results suggest additional roles. Eukaryotic RdRPs thus have a complex evolutionary history in animals, with frequent independent losses and apparent functional diversification.
RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways.
RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways.RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways.
Audience Academic
Author Seitz, Hervé
Subirana, Lucie
Escrivá, Hector
Bertrand, Stéphanie
Busseau, Isabelle
Pinzón, Natalia
AuthorAffiliation Stanford University School of Medicine, UNITED STATES
1 Institut de Génétique Humaine, UMR 9002 CNRS and université de Montpellier, 141, rue de la Cardonille, 34396 Montpellier CEDEX 5, France
2 Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, F-66650 Banyuls-sur-Mer, France
AuthorAffiliation_xml – name: Stanford University School of Medicine, UNITED STATES
– name: 2 Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, F-66650 Banyuls-sur-Mer, France
– name: 1 Institut de Génétique Humaine, UMR 9002 CNRS and université de Montpellier, 141, rue de la Cardonille, 34396 Montpellier CEDEX 5, France
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  surname: Bertrand
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  surname: Seitz
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30779744$$D View this record in MEDLINE/PubMed
https://hal.sorbonne-universite.fr/hal-02081479$$DView record in HAL
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Copyright COPYRIGHT 2019 Public Library of Science
2019 Pinzón et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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– notice: 2019 Pinzón et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Current address: INSERM U981, Gustave Roussy Cancer Campus, Paris-Saclay University, Villejuif, France
The authors have declared that no competing interests exist.
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Snippet RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for...
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SubjectTerms Animal genetics
Animals
Biology and life sciences
Branchiostoma
Developmental stages
EDTA
Eukaryotes
Functional plasticity
Fungi
Genes
Genetic research
Genetics
Genomes
Insects
Lability
Life Sciences
MicroRNAs
Nematodes
Nucleotide sequence
Physiological aspects
Proteins
RNA
RNA interference
RNA polymerase
RNA polymerases
RNA-mediated interference
Roundworms
siRNA
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Title Functional lability of RNA-dependent RNA polymerases in animals
URI https://www.ncbi.nlm.nih.gov/pubmed/30779744
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http://dx.doi.org/10.1371/journal.pgen.1007915
Volume 15
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