Planarians recruit piRNAs for mRNA turnover in adult stem cells

Iana V. Kim, Elizabeth M. Duncan, Eric J. Ross, Vladyslava Gorbovytska, Stephanie H. Nowotarski, Sarah A. Elliott, Alejandro Sánchez Alvarado, Claus D. Kuhn

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

PIWI proteins utilize small RNAs called piRNAs to silence transposable elements, thereby protecting germline integrity. In planarian flatworms, PIWI proteins are essential for regeneration, which requires adult stem cells termed neoblasts. Here, we characterize planarian piRNAs and examine the roles of PIWI proteins in neoblast biology. We find that the planarian PIWI proteins SMEDWI-2 and SMEDWI-3 cooperate to degrade active transposons via the ping-pong cycle. Unexpectedly, we discover that SMEDWI-3 plays an additional role in planarian mRNA surveillance. While SMEDWI-3 degrades numerous neoblast mRNAs in a homotypic ping-pong cycle, it is also guided to another subset of neoblast mRNAs by antisense piRNAs and binds these without degrading them. Mechanistically, the distinct activities of SMEDWI-3 are primarily dictated by the degree of complementarity between target mRNAs and antisense piRNAs. Thus, PIWI proteins enable planarians to repurpose piRNAs for potentially critical roles in neoblast mRNA turnover.

Original languageEnglish
Pages (from-to)1575-1590
Number of pages16
JournalGenes and Development
Volume33
Issue number21-22
DOIs
StatePublished - Nov 1 2019

Bibliographical note

Publisher Copyright:
© 2019 Kim et al.; Published by Cold Spring Harbor Laboratory Press.

Keywords

  • PIWI proteins
  • RNA-binding proteins
  • S. mediterranea
  • mRNA surveillance
  • mRNA turnover
  • piRNAs
  • planarians
  • posttranscriptional gene silencing
  • regeneration
  • stem cells

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology

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