Abstract

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 phylogenetic gap, we characterize 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 manipulations, Argonaute-immunoprecipitations and high-throughput sequencing, we provide experimental evidence for the developmental importance of miRNAs in a non-bilaterian 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.

Highlights

  • MicroRNAs base-pair to messenger RNA targets and guide Argonaute proteins to mediate their silencing

  • These morphological phenotypes are grossly similar to the phenotypes that we previously obtained when we inhibited other components involved in the miRNA pathway[8]

  • Using IP, KDs, and high-throughput sequencing we revealed the developmental importance and functional differences of two hexacorallian AGOs that duplicated at least 500 million years ago (MYA) at the split of sea anemones and reef-building corals

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Summary

Introduction

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. This notion is based exclusively on studies in bilaterians, which comprise almost all lab model animals To fill this phylogenetic gap, we characterize 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. MicroRNAs (miRNAs) are pivotal players in posttranscriptional gene regulation in animals and plants As such, they carry important roles in many developmental and physiological processes in both kingdoms[1,2,3,4]. Our previous studies revealed that the miRNAs of Cnidaria (sea anemones, corals, jellyfish, and hydroids), the sister group of Bilateria, exhibit remarkable similarities to plant miRNA biogenesis and mode of action[8,9,10].

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