Abstract
While the biogenesis of microRNAs (miRNAs) in both animals and plants depends on the RNase III Dicer, its partner proteins are considered distinct for each kingdom. Nevertheless, recent discovery of homologs of Hyponastic Leaves1 (HYL1), a 'plant-specific' Dicer partner, in the metazoan phylum Cnidaria, challenges the view that miRNAs evolved convergently in animals and plants. Here, we show that the HYL1 homolog Hyl1-like a (Hyl1La) is crucial for development and miRNA biogenesis in the cnidarian model Nematostella vectensis. Inhibition of Hyl1La by morpholinos resulted in metamorphosis arrest in Nematostella embryos and a significant reduction in levels of most miRNAs. Further, meta-analysis of morphants of miRNA biogenesis components, like Dicer1, shows clustering of their miRNA profiles with Hyl1La morphants. Strikingly, immunoprecipitation of Hyl1La followed by quantitative PCR revealed that in contrast to the plant HYL1, Hyl1La interacts only with precursor miRNAs and not with primary miRNAs. This was complemented by an in vitro binding assay of Hyl1La to synthetic precursor miRNA. Altogether, these results suggest that the last common ancestor of animals and plants carried a HYL1 homolog that took essential part in miRNA biogenesis and indicate early emergence of the miRNA system before plants and animals separated.
Highlights
MicroRNAs are 21-24 nucleotides-long small RNAs that are known to be involved in post-transcriptional gene regulation and play important roles in both plant and animal development (Alvarez-Garcia & Miska, 2005; Bråte et al, 2018; Voinnet, 2009)
The Hyponastic Leaves1 (HYL1) protein is known to play an essential role in the growth and development of the model plant Arabidopsis thaliana by regulating miRNA biogenesis
Unlike its paralog Hyl1Lb that is specific to stinging cells and carries additional protein domains, Hyl1La expression is ubiquitously distributed throughout Nematostella tissues and shares its domain structure with other cnidarian HYL1 homologs (Moran et al, 2013)
Summary
Faculty of Science, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel. Presence of a functional homolog of HYL1 in Nematostella vectensis, a basal animal model, indicates divergent evolution of miRNA biogenesis pathway in plants and animals from an ancestral miRNA system
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