Unicellular origin of the animal microRNA machinery
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Abstract
The emergence of multicellular animals was associated with an increase in phenotypic complexity and with the acquisition of spatial cell differentiation and embryonic development. Paradoxically, this phenotypic transition was not paralleled by major changes in the underlying developmental toolkit and regulatory networks. In fact, most of these systems are ancient, established already in the unicellular ancestors of animals [1-5]. In contrast, the Microprocessor protein machinery, which is essential for microRNA (miRNA) biogenesis in animals, as well as the miRNA genes themselves produced by this Microprocessor, have not been identified outside of the animal kingdom [6]. Hence, the Microprocessor, with the key proteins Pasha and Drosha, is regarded as an animal innovation [7-9]. Here, we challenge this evolutionary scenario by investigating unicellular sister lineages of animals through genomic and transcriptomic analyses. We identify in Ichthyosporea both Drosha and Pasha (DGCR8 in vertebrates), indicating that the Microprocessor complex evolved long before the last common ancestor of animals, consistent with a pre-metazoan origin of most of the animal developmental gene elements. Through small RNA sequencing, we also discovered expressed bona fide miRNA genes in several species of the ichthyosporeans harboring the Microprocessor. A deep, pre-metazoan origin of the Microprocessor and miRNAs comply with a view that the origin of multicellular animals was not directly linked to the innovation of these key regulatory components.
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Ctenophores depart from other metazoans in terms of their genetic machinery, having lost several gene classes (e.g., microRNA processing enzymes and HOX genes).
“having lost several gene classes (e.g., microRNA processing enzymes [57”
From Cambrian Sessile, Suspension Feeding Stem-Group Ctenophores and Evolution of the Comb Jelly Body Plan (2019) · cites this paper as [57]
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- Authors
- Bråte, J., Neumann, R. S., Fromm, B., Haraldsen, A. A. B., Tarver, J. E., Suga, H., Donoghue, P. C. J., Peterson, K. J., Ruiz-Trillo, I., Grini, P. E., & Shalchian-Tabrizi, K.
- Affiliations
- University of Oslo (NO)
- Oslo University Hospital (NO)
- University of Bristol (GB)
- Prefectural University of Hiroshima (JP)
- Dartmouth College (US)
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2018-10
- Volume
- 28
- Issue
- 20
- Pages
- 3288-3295.e5
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC6206976
- OpenAlex
- W2897291496
- Cited by
- 53
- References
- 87
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 3 · 2023: 9 · 2022: 8 · 2021: 6 · 2020: 6 · 2019: 10 · 2018: 3 · 2016: 1 · 2012: 1
- FWCI
- 2.22
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Explore Bristol Research (submittedVersion, cc-by-nc-nd)
- Bristol Research (University of Bristol) (submittedVersion, cc-by-nc-nd)
- NORA - Norwegian Open Research Archives (submittedVersion, cc-by-nc-nd)
- Funders
- South-Eastern Norway Regional Health Authority (2014041)
- JSPS KAKENHI (16K07468)
- Natural Environment Research Council (NE/P013678/1)
- ERC (ERC-2012-Co-616960)
- Secretary’s Office for Universities and Research of the Generalitat de Catalunya (2014 SGR 619)
- Spanish Ministry for Economy and Competitiveness (BFU2017-90114-P)
- European Regional Development Fund (Nr. 213703, 240284)
- Norwegian Research Council
- Molecular Life Science board at University of Oslo
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Keywords
- microRNA biogenesis, microprocessor complex, Drosha, pashas, DGCR8, Ichthyosporea, origin of multicellularity, small RNA, miRNA genes
- MeSH terms
- Animals, Base Sequence, Phylogeny, Evolution, Molecular, MicroRNAs, Mesomycetozoea
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