Characterization of the piRNA pathway during development of the sea anemone <i>Nematostella vectensis</i>

Praher, Daniela; Zimmermann, Bob; Genikhovich, Grigory; Columbus-Shenkar, Yaara Y; Modepalli, Vengamanaidu; Aharoni, Reuven; Moran, Yehu; Technau, Ulrich

doi:10.1080/15476286.2017.1349048

Cited by 56 publications

(92 citation statements)

References 157 publications

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“…In Nematostella, unlike most bilaterians, such libraries are predominated by another class of sRNAs: the piRNAs 5,9 . Unlike most bilaterians, Nematostella piRNAs are not restricted to the germline, but are rather expressed broadly in somatic tissues 26 . Hence NveAGO IP enabled us for the first time to overcome this limitation and reliably identify a significantly larger set of lower expressed novel miRNAs.…”

Section: (See the Updated List Of Mirnas Inmentioning

confidence: 99%

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Unravelling the developmental and functional significance of an ancient Argonaute duplication

Fridrich

Modepalli

Lewandowska

et al. 2020

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microRNAs (miRNAs), base-pair to messenger RNA targets and guide Argonaute proteins to mediate their silencing. This target regulation is considered crucial for animal physiology and development.However, this notion is based exclusively on studies in bilaterians, which comprise almost all lab model animals. To fill this glaring phylogenetic gap, we characterized the functions of two Argonaute paralogs in the sea anemone Nematostella vectensis of the phylum Cnidaria, which is separated from bilaterians by ~600 million years. Using genetic manipulation, Argonaute-immunoprecipitations and high-throughput sequencing we provide experimental evidence for the developmental importance of miRNAs in a nonbilaterian animal. Additionally, we uncover unexpected differential distribution of distinct miRNAs between the two Argonautes and the ability of one of them to load additional types of small RNAs. This enables us to postulate a novel model for evolution of miRNA precursors in sea anemones and their relatives, revealing alternative trajectories for metazoan miRNA evolution.

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Section: (See the Updated List Of Mirnas Inmentioning

confidence: 99%

“…In this case, the specificity is enabled via tissue specific co-expression of these particular miRNAs with Alg5 in the germline. In Nematostella, the two AGOs are expressed in all tissues and developmental stages 26 ( Supplementary Fig. 1a, Supplementary table 4).…”

Section: (See the Updated List Of Mirnas Inmentioning

confidence: 99%

Unravelling the developmental and functional significance of an ancient Argonaute duplication

Fridrich

Modepalli

Lewandowska

et al. 2020

Preprint

Self Cite

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“…Second, and in contrast to plants and fungi, animals also possess a Piwi-dependent (piRNA) pathway that provides a defence against TEs in germline (Drosophila and mammals) and/or somatic cells (e.g. [15][16][17]. This pathway is usually characterised by a broad peak of 26-30nt small RNAs bound by Piwi-family Argonaute proteins, and comprises both 5'U primary piRNAs cleaved by homologs of Drosophila Zucchini from long 'piRNA cluster' transcripts (see 18), and secondary piRNAs generated by 'Ping-Pong' amplification.…”

Section: Introductionmentioning

confidence: 99%

Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes

Waldron¹,

Stone²,

Obbard³

2017

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RNA interference (RNAi)-related pathways target viruses and transposable element (TE) transcripts in plants, fungi, and ecdysozoans (nematodes and arthropods), giving protection against infection and transmission. In each case, this produces abundant TE and virus-derived 20-30nt small RNAs, which provide a characteristic signature of RNAi-mediated defence. The broad phylogenetic distribution of the Argonaute and Dicer-family genes that mediate these pathways suggests that defensive RNAi is ancient and probably shared by most metazoan (animal) phyla. Indeed, while vertebrates had been thought an exception, it has recently been suggested that mammals may also possess a functional antiviral RNAi pathway, albeit involving few small RNAs that are challenging to detect. Here we use a metagenomic approach to test for the presence of antiviral RNAi in five divergent metazoan phyla (Porifera, Cnidaria, Echinodermata, Mollusca, and Annelida), and in a brown alga. We use metagenomic RNA sequencing to identify around 80 virus-like contigs in these lineages, and small RNA sequencing to identify small RNAs derived from those viruses. Contrary to our expectations, we were unable to identify canonical (i.e. Drosophila-like) viral small RNAs in any of these organisms, despite the presence of abundant micro-RNAs and putative piwi-interacting piRNAs. Instead, we identified an apparently novel class of virus-derived small RNAs in the mollusc, which have a piRNAlike length distribution but lack key signatures of piRNA biogenesis, and a novel class of 21U virusderived small RNAs in the brown alga. We also identified primary piRNAs derived from putatively endogenous copies of DNA viruses in the cnidarian and the echinoderm, and an endogenous RNA virus in the mollusc. This suggests either that the majority of metazoan phyla lack antiviral RNAi completely, such that antiviral RNAi has evolved independently in ecdysozoans, vertebrates, and molluscs, or that the antiviral RNAi response in most extant phyla-and the ancestral state of Metazoa-more closely resembles that of mammals than arthropods or nematodes.

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“…Incontrast, piRNAs appear to be a metazoan innovation [2]. A functional PIWI-piRNA pathway is present in Hydra and Nematos-tella [28,29]. This system appears to differ between basal metazoans, with it being absent in placozoans and expressed at relatively high levels in cnidarians [2].…”

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confidence: 99%

Diverse RNA interference strategies in early-branching metazoans

Calcino

Taft

Degnan

2018

Preprint

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Background: Micro RNAs (miRNAs) and piwi interacting RNAs (piRNAs), along with the more ancient eukaryotic endogenous small interfering RNAs (endo-siRNAs) constitute the principal components of the RNA interference (RNAi) repertoire of most animals. RNAi in non-bilaterians -sponges, ctenophores, placozoans and cnidarians -appears to be more diverse than that of bilaterians, and includes structurally variable miR-NAs in sponges, an enormous number of piRNAs in cnidarians and the absence of miRNAs in ctenophores and placozoans. Results:Here we identify thousands of endo-siRNAs and piRNAs from the sponge Amphimedon queenslandica, the ctenophore Mnemiopsis leidyi and the cnidarian Nematostella vectensis using a computational approach that clusters mapped small RNA sequences and annotates each cluster based on the read length and relative abundance of the constituent reads. This approach was validated on 11 small RNA libraries in Drosophila melanogaster, demonstrating the successful annotation of RNAi associated loci with properties consistent with previous reports. In the non-bilaterians we uncover seven new miRNAs from Amphimedon and four from Nematostella as well as sub-populations of candidate cis-natural antisense transcript (cis-NAT) endo-siRNAs. In the ctenophore, the absence of miRNAs is confirmed and an abundance of endo-siRNAs is revealed. Analysis of putative piRNA structure suggests that conserved localised secondary structures in primary transcripts may be important for the production of mature piRNAs in Amphimedon and Nematostella, as is also the case for endo-siRNAs. Conclusion:Together, these findings suggest that the last common ancestor of animals did not have the entrained RNAi system that typifies bilaterians. Instead it appears that bilaterians, cnidarians, ctenophores and sponges express unique repertoires and combinations of miRNAs, piRNAs and endo-siRNAs. ABSTRACT 2 BACKGROUND RNA interference (RNAi) evolved prior to the divergence of extant eukaryotic lineages, possibly in response to threats from parasitic double-stranded RNA species such as retroviruses and transposons [1]. In contemporary animals, three independent RNAi systems comprise the bulk of the small RNA (sRNA) repertoire: micro RNAs (miRNAs); Piwi interacting RNAs (piRNAs); and endogenous small interfering RNAs (endo-siRNAs). Amongst non-bilaterian animals -sponges, cnidarians ctenophores and placozoans -miRNAs appear to be lost in latter two lineages, with placozoans and ctenophores also lacking key miRNA biogenic enzymes [2][3][4]. The absence of miRNAs in the sister lineages to the animal kingdom, choanoflagellates, and fungi [2,5,6], suggests the miRNA system has been lost or evolved independently multiple times [7]. Nonetheless, animal miRNAs play fundamental roles in cell type differentiation and maintenance, and their emergence and proliferation is linked to the evolution of complex multicellularity [8]. The prevalence of miRNAs in plants and algae [9] lends further support to the hypothesis that miRNAs may be important regu...

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Characterization of the piRNA pathway during development of the sea anemone Nematostella vectensis

Cited by 56 publications

References 157 publications

Unravelling the developmental and functional significance of an ancient Argonaute duplication

Unravelling the developmental and functional significance of an ancient Argonaute duplication

Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes

Diverse RNA interference strategies in early-branching metazoans

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