Comprehensive re-analysis of hairpin small RNAs in fungi reveals loci with conserved links

  1. Nathan R Johnson
  2. Luis F Larrondo
  3. José M Álvarez  Is a corresponding author
  4. Elena A Vidal  Is a corresponding author
  1. Universidad Mayor, Chile
  2. Pontificia Universidad Católica de Chile, Chile
  3. Universidad Andrés Bello, Chile

Abstract

RNA interference is an ancient mechanism with many regulatory roles in eukaryotic genomes, with small RNAs acting as their functional element. While there is a wide array of classes of small-RNA-producing loci, those resulting from stem-loop structures (hairpins) have received profuse attention. Such is the case of microRNAs (miRNAs), which have distinct roles in plants and animals. Fungi also produce small RNAs, and several publications have identified miRNAs and miRNA-like (mi/milRNA) hairpin RNAs in diverse fungal species using deep sequencing technologies. Despite this relevant source of information, relatively little is known about mi/milRNA-like features in fungi, mostly due to a lack of established criteria for their annotation. To systematically assess mi/miRNA-like characteristics and annotation confidence, we searched for publications describing mi/milRNA loci and re-assessed the annotations for 41 fungal species. We extracted and normalized the annotation data for 1,727 reported mi/milRNA-like loci and determined their abundance profiles, concluding that less than half of the reported loci passed basic standards used for hairpin RNA discovery. We found that fungal mi/milRNA are generally more similar in size to animal miRNAs and were frequently associated with protein-coding genes. The compiled genomic analyses identified 25 mi/milRNA loci conserved in multiple species. Our pipeline allowed us to build a general hierarchy of locus quality, identifying more than 150 loci with high-quality annotations. We provide a centralized annotation of identified mi/milRNA hairpin RNAs in fungi which will serve as a resource for future research and advance in understanding the characteristics and functions of mi/milRNAs in fungal organisms.

Data availability

Sequencing data used in this work is available in public repositories, with publication details provided in Table S1 and all data accessions provided in Table S3. Results of abundance profiling are found in File S1 and summarized in Table S4.

The following previously published data sets were used

Article and author information

Author details

  1. Nathan R Johnson

    Facultad de Ciencias, Universidad Mayor, Santiago, Chile
    Competing interests
    No competing interests declared.
  2. Luis F Larrondo

    Molecular Genetics and Microbiology department, Pontificia Universidad Católica de Chile, Santiago, Chile
    Competing interests
    Luis F Larrondo, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8832-7109
  3. José M Álvarez

    Facultad de Ciencias, Universidad Andrés Bello, Santiago, Chile
    For correspondence
    jose.alvarez.h@unab.cl
    Competing interests
    No competing interests declared.
  4. Elena A Vidal

    Facultad de Ciencias, Universidad Mayor, Santiago, Chile
    For correspondence
    elena.vidal@umayor.cl
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8208-7327

Funding

Fondo Nacional de Desarrollo Científico y Tecnológico (11220727)

  • Nathan R Johnson

Instituto Milenio de Biologia Integrativa (ICN17_022)

  • Nathan R Johnson
  • Luis F Larrondo
  • Elena A Vidal

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

Copyright

© 2022, Johnson 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.

Metrics

  • 1,125
    views
  • 138
    downloads
  • 5
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Nathan R Johnson
  2. Luis F Larrondo
  3. José M Álvarez
  4. Elena A Vidal
(2022)
Comprehensive re-analysis of hairpin small RNAs in fungi reveals loci with conserved links
eLife 11:e83691.
https://doi.org/10.7554/eLife.83691

Share this article

https://doi.org/10.7554/eLife.83691

Further reading

    1. Cell Biology
    2. Genetics and Genomics
    Priyanka Das, Alejandro Aballay, Jogender Singh
    Research Article

    Calcineurin is a highly conserved calcium/calmodulin-dependent serine/threonine protein phosphatase with diverse functions. Inhibition of calcineurin is known to enhance the lifespan of Caenorhabditis elegans through multiple signaling pathways. Aiming to study the role of calcineurin in regulating innate immunity, we discover that calcineurin is required for the rhythmic defecation motor program (DMP) in C. elegans. Calcineurin inhibition leads to defects in the DMP, resulting in intestinal bloating, rapid colonization of the gut by bacteria, and increased susceptibility to bacterial infection. We demonstrate that intestinal bloating caused by calcineurin inhibition mimics the effects of calorie restriction, resulting in enhanced lifespan. The TFEB ortholog, HLH-30, is required for lifespan extension mediated by calcineurin inhibition. Finally, we show that the nuclear hormone receptor, NHR-8, is upregulated by calcineurin inhibition and is necessary for the increased lifespan. Our studies uncover a role for calcineurin in the C. elegans DMP and provide a new mechanism for calcineurin inhibition-mediated longevity extension.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Philipp H Schiffer, Paschalis Natsidis ... Maximilian J Telford
    Research Article Updated

    The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can provide important comparative data and help understand the evolution and biology of enigmatic species better. Here, we assemble and analyze the genome of the simple, marine xenacoelomorph Xenoturbella bocki, a key species for our understanding of early bilaterian evolution. Our highly contiguous genome assembly of X. bocki has a size of ~111 Mbp in 18 chromosome-like scaffolds, with repeat content and intron, exon, and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signaling pathways are also largely complete and most bilaterian miRNAs are present. Overall, we conclude that X. bocki has a complex genome typical of bilaterians, which does not reflect the apparent simplicity of its body plan that has been so important to proposals that the Xenacoelomorpha are the simple sister group of the rest of the Bilateria.