Functional characterization of a 'plant-like' HYL1 homolog in the cnidarian Nematostella vectensis indicates a conserved involvement in microRNA biogenesis

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.

Data availability

RNA sequencing data are available at NCBI-SRA under BioProject ID PRJNA630340.

The following data sets were generated

Article and author information

Author details

  1. Abhinandan M Tripathi

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Yael Admoni

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Arie Fridrich

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Magda Lewandowska

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Joachim M Surm

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Reuven Aharoni

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Yehu Moran

    Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel
    For correspondence
    yehu.moran@mail.huji.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9928-9294

Funding

H2020 European Research Council (637456)

  • Yehu Moran

H2020 European Research Council (863809)

  • Yehu Moran

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. René Ketting, IMB Mainz, Germany

Publication history

  1. Preprint posted: May 31, 2020 (view preprint)
  2. Received: April 15, 2021
  3. Accepted: March 14, 2022
  4. Accepted Manuscript published: March 15, 2022 (version 1)
  5. Version of Record published: May 12, 2022 (version 2)

Copyright

© 2022, Tripathi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Abhinandan M Tripathi
  2. Yael Admoni
  3. Arie Fridrich
  4. Magda Lewandowska
  5. Joachim M Surm
  6. Reuven Aharoni
  7. Yehu Moran
(2022)
Functional characterization of a 'plant-like' HYL1 homolog in the cnidarian Nematostella vectensis indicates a conserved involvement in microRNA biogenesis
eLife 11:e69464.
https://doi.org/10.7554/eLife.69464

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