Abstract
PIWI-interacting RNAs (piRNAs) and associated proteins comprise a conserved pathway for silencing transposons in metazoan germlines. piRNA pathway components are also expressed in multipotent somatic stem cells in various organisms. piRNA functions have been extensively explored in bilaterian model systems, however, comprehensive studies in non-bilaterian phyla remain limited. Here we investigate the piRNA pathway during the development of Nematostella vectensis, a well-established model system belonging to Cnidaria, the sister group to Bilateria. To date, no population of somatic stem cells has been identified in this organism, despite its long life-span and regenerative capacities that require a constant cell-renewal. We show that Nematostella piRNA pathway components are broadly expressed in early developmental stages, while piRNAs themselves show differential expression, suggesting specific developmental roles of distinct piRNA families. In adults, piRNA associated proteins are enriched in the germline but also expressed in somatic cells, indicating putative stem cell properties. Furthermore, we provide experimental evidence that Nematostella piRNAs cleave transposable elements as well as protein-coding genes. Our results demonstrate that somatic expression of piRNA associated proteins as well as the roles of piRNAs in transposon repression and gene regulation are likely ancestral features that evolved before the split between Cnidaria and Bilateria.
| Original language | American English |
|---|---|
| Pages (from-to) | 1727-1741 |
| Number of pages | 15 |
| Journal | RNA Biology |
| Volume | 14 |
| Issue number | 12 |
| DOIs | |
| State | Published - 2 Dec 2017 |
Bibliographical note
Funding Information:The protocol for in situ hybridization of adult sea anemones was established by Patrick Steinmetz. We thank Stefan Jahnel for sharing his expertise in the procedures of dissecting and sectioning adult animal parts. We thank Sabrina Kaul-Strehlow for her support in figure assembly. Small RNAs of different stages of Nematostella vectensis were sequenced by Herv? Seitz. We thank the Core Facility for Cell Imaging and Ultrastructure Research of the University of Vienna for the access to the confocal microscope. This work was supported by grants of the Austrian Science Fund FWF (P22618, P24858) to U.T., European Research Council Starting Grant (CNIDARIAMICRORNA, 637456) to Y.M. and a PhD completion fellowship of the University of Vienna to D.P.
Funding Information:
This work was supported by grants of the Austrian Science Fund FWF (P22618, P24858) to U.T., European Research Council Starting Grant (CNIDARIAMICRORNA, 637456) to Y.M. and a PhD completion fellowship of the University of Vienna to D.P.
Publisher Copyright:
© 2017 The Author(s). Published with license by Taylor & Francis Group, LLC © 2017, © Daniela Praher, Bob Zimmermann, Grigory Genikhovich, Yaara Columbus-Shenkar, Vengamanaidu Modepalli, Reuven Aharoni, Yehu Moran, and Ulrich Technau.
Keywords
- Cnidaria
- Nematostella vectensis
- Piwi
- Vasa
- evolution
- piRNA