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. 2024 May 2;16(5):evae098.
doi: 10.1093/gbe/evae098.

The Evolution and Characterization of the RNA Interference Pathways in Lophotrochozoa

Alessandro Formaggioni  1 , Gianmarco Cavalli  1 , Mayuko Hamada  2 , Tatsuya Sakamoto  2 , Federico Plazzi  1 , Marco Passamonti  1
Affiliations

The Evolution and Characterization of the RNA Interference Pathways in Lophotrochozoa

Alessandro Formaggioni et al. Genome Biol Evol. .

Abstract

In animals, three main RNA interference mechanisms have been described so far, which respectively maturate three types of small noncoding RNAs (sncRNAs): miRNAs, piRNAs, and endo-siRNAs. The diversification of these mechanisms is deeply linked with the evolution of the Argonaute gene superfamily since each type of sncRNA is typically loaded by a specific Argonaute homolog. Moreover, other protein families play pivotal roles in the maturation of sncRNAs, like the DICER ribonuclease family, whose DICER1 and DICER2 paralogs maturate respectively miRNAs and endo-siRNAs. Within Metazoa, the distribution of these families has been only studied in major groups, and there are very few data for clades like Lophotrochozoa. Thus, we here inferred the evolutionary history of the animal Argonaute and DICER families including 43 lophotrochozoan species. Phylogenetic analyses along with newly sequenced sncRNA libraries suggested that in all Trochozoa, the proteins related to the endo-siRNA pathway have been lost, a part of them in some phyla (i.e. Nemertea, Bryozoa, Entoprocta), while all of them in all the others. On the contrary, early diverging phyla, Platyhelminthes and Syndermata, showed a complete endo-siRNA pathway. On the other hand, miRNAs were revealed the most conserved and ubiquitous mechanism of the metazoan RNA interference machinery, confirming their pivotal role in animal cell regulation.

Keywords: Argonaute; DICER; Lophotrochozoa; Metazoa; RNAi.

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Figures

Fig. 1.
Fig. 1.
ML tree of the lophotrochozoan Argonaute proteins. For the six marked nodes, the label shows UFBoot/SH-alrt value. Support values of the remaining nodes are shown in supplementary fig. S1, Supplementary Material online. Clades formed by paralogs of the same species were collapsed and represented with a triangle. For reference proteins, the UniProt accession code is reported in brackets. Species are colored according to the phylum. The color legend on the bottom left reconstructs the main phylogenetic relationships according to the latest Lophotrochozoa phylogenetic analyses (Kocot et al. 2017; Bleidorn 2019; Marlétaz et al. 2019).
Fig. 2.
Fig. 2.
ML tree of the lophotrochozoan DICER proteins. For two marked nodes, it is reported respectively the UFBoot and the SH-alrt value. Support values of the remaining nodes are shown in the supplementary fig. S2, Supplementary Material online. Clades formed by paralogs of the same species were collapsed and represented with a triangle. Reference species retrieved from the analysis of Mukherjee and colleagues (2013) are marked with an asterisk. Species are colored according to the phylum. The color legend on the bottom left reconstructs the main phylogenetic relationships according to the latest Lophotrochozoa phylogenetic analyses (Kocot et al. 2017; Bleidorn 2019; Marlétaz et al. 2019).
Fig. 3.
Fig. 3.
Evaluating the siRNA signature in sncRNA libraries. The plot reports the Z-score between the number of pairs of all possible overlaps. A Z-score > 1 means that pairs overlapping of that length are at least a standard deviation more numerous than the mean of all the overlaps. The species are sorted by the presence/absence of DICER2.
Fig. 4.
Fig. 4.
The loss of DICER2 and siAGO along the Metazoa evolution. The lophotrochozoan phylogenetic tree is reconstructed according to the latest Lophotrochozoa phylogenetic analyses (Kocot et al. 2017; Bleidorn 2019; Marlétaz et al. 2019). For each protein, it is reported its presence, with a check, or the absence, with a cross, in each metazoan clade.
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