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Unicellular Origin of the Animal MicroRNA Machinery
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 an...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cell Press
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206976/ https://www.ncbi.nlm.nih.gov/pubmed/30318349 http://dx.doi.org/10.1016/j.cub.2018.08.018 |
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author | Bråte, Jon Neumann, Ralf S. Fromm, Bastian Haraldsen, Arthur A.B. Tarver, James E. Suga, Hiroshi Donoghue, Philip C.J. Peterson, Kevin J. Ruiz-Trillo, Iñaki Grini, Paul E. Shalchian-Tabrizi, Kamran |
author_facet | Bråte, Jon Neumann, Ralf S. Fromm, Bastian Haraldsen, Arthur A.B. Tarver, James E. Suga, Hiroshi Donoghue, Philip C.J. Peterson, Kevin J. Ruiz-Trillo, Iñaki Grini, Paul E. Shalchian-Tabrizi, Kamran |
author_sort | Bråte, Jon |
collection | PubMed |
description | 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, 2, 3, 4, 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, 8, 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. |
format | Online Article Text |
id | pubmed-6206976 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Cell Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-62069762018-11-06 Unicellular Origin of the Animal MicroRNA Machinery Bråte, Jon Neumann, Ralf S. Fromm, Bastian Haraldsen, Arthur A.B. Tarver, James E. Suga, Hiroshi Donoghue, Philip C.J. Peterson, Kevin J. Ruiz-Trillo, Iñaki Grini, Paul E. Shalchian-Tabrizi, Kamran Curr Biol Article 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, 2, 3, 4, 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, 8, 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. Cell Press 2018-10-22 /pmc/articles/PMC6206976/ /pubmed/30318349 http://dx.doi.org/10.1016/j.cub.2018.08.018 Text en © 2018 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Article Bråte, Jon Neumann, Ralf S. Fromm, Bastian Haraldsen, Arthur A.B. Tarver, James E. Suga, Hiroshi Donoghue, Philip C.J. Peterson, Kevin J. Ruiz-Trillo, Iñaki Grini, Paul E. Shalchian-Tabrizi, Kamran Unicellular Origin of the Animal MicroRNA Machinery |
title | Unicellular Origin of the Animal MicroRNA Machinery |
title_full | Unicellular Origin of the Animal MicroRNA Machinery |
title_fullStr | Unicellular Origin of the Animal MicroRNA Machinery |
title_full_unstemmed | Unicellular Origin of the Animal MicroRNA Machinery |
title_short | Unicellular Origin of the Animal MicroRNA Machinery |
title_sort | unicellular origin of the animal microrna machinery |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206976/ https://www.ncbi.nlm.nih.gov/pubmed/30318349 http://dx.doi.org/10.1016/j.cub.2018.08.018 |
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