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Curr Biol. 2018 Oct 22;28(20):3288-3295.e5. doi: 10.1016/j.cub.2018.08.018. Epub 2018 Oct 11.

Unicellular Origin of the Animal MicroRNA Machinery.

Author information

1
Centre for Epigenetics, Development and Evolution (CEDE) and Centre for Integrative Microbial Evolution (CIME), Section for Genetics and Evolutionary Biology (EVOGENE), University of Oslo, Oslo, Norway.
2
Department of Tumor Biology, Institute for Cancer Research, Norwegian Radium Hospital, Oslo University Hospital, Oslo, Norway; Science for Life Laboratory, Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 10691 Stockholm, Sweden.
3
School of Earth Sciences, University of Bristol, Bristol BS8 1TQ, UK.
4
Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Nanatsuka 562, Shobara, Hiroshima 727-0023, Japan.
5
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA.
6
Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), 08003 Barcelona, Spain; ICREA, 08010 Barcelona, Spain.
7
Centre for Epigenetics, Development and Evolution (CEDE) and Centre for Integrative Microbial Evolution (CIME), Section for Genetics and Evolutionary Biology (EVOGENE), University of Oslo, Oslo, Norway. Electronic address: kamran@ibv.uio.no.

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.

KEYWORDS:

DGCR8; Drosha; Holozoa; Ichthyosporea; Pasha; Sphaeroforma; evolution; miRNA; microRNA; microprocessor

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