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miRNA-target complementarity in cnidarians resembles its counterpart in plants

Yael Admoni,A. Fridrich,Paris K Weavers,R. Aharoni,Talya Razin,Miguel Salinas-Saavedra,Michal Rabani,Uri Frank,Yehu Moran

Published 2025 in EMBO Reports

ABSTRACT

microRNAs (miRNAs) are important post-transcriptional regulators that activate silencing mechanisms by annealing to mRNA transcripts. While plant miRNAs match their targets with nearly-full complementarity leading to mRNA cleavage, miRNAs in most animals require only a short sequence called ‘seed’ to inhibit target translation. Recent findings showed that miRNAs in cnidarians, early-branching metazoans, act similarly to plant miRNAs, by exhibiting full complementarity and target cleavage; however, it remained unknown if seed-based regulation was possible in cnidarians. Here, we investigate the miRNA-target complementarity requirements for miRNA activity in the cnidarian Nematostella vectensis. We show that bilaterian-like complementarity of seed-only or seed and supplementary 3’ matches are insufficient for miRNA-mediated knockdown. Furthermore, miRNA-target mismatches in the cleavage site decrease knockdown efficiency. Finally, miRNA silencing of a target with three seed binding sites in the 3’ untranslated region that mimics typical miRNA targeting was repressed in zebrafish but not in Nematostella and another cnidarian, Hydractinia symbiolongicarpus. Altogether, these results unravel striking similarities between plant and cnidarian miRNAs supporting a possible common evolutionary origin of miRNAs in plants and animals. miRNAs in plants and cnidarian animals operate similarly by binding their targets with nearly-full complementarity, in contrast to miRNAs in bilaterian animals that bind via a short seed-match. This is important for the understanding of the evolution of the miRNA system and its mechanistic features in cnidarians. miRNAs in Nematostella and Hydractinia require nearly-full complementarity to their targets in order to silence gene expression. A bilaterian-like seed-match is inefficient in mediating silencing in cnidarians. Binding of positions 10–11 of the miRNA, which represent the cleavage site, are crucial for miRNA activity in Nematostella. miRNAs in Nematostella and Hydractinia require nearly-full complementarity to their targets in order to silence gene expression. A bilaterian-like seed-match is inefficient in mediating silencing in cnidarians. Binding of positions 10–11 of the miRNA, which represent the cleavage site, are crucial for miRNA activity in Nematostella. miRNAs in plants and cnidarian animals operate similarly by binding their targets with nearly-full complementarity, in contrast to miRNAs in bilaterian animals that bind via a short seed-match. This is important for the understanding of the evolution of the miRNA system and its mechanistic features in cnidarians.

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