Developmental Cell
Volume 46, Issue 3, 6 August 2018, Pages 316-326.e5
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Article
The hpRNA/RNAi Pathway Is Essential to Resolve Intragenomic Conflict in the Drosophila Male Germline

https://doi.org/10.1016/j.devcel.2018.07.004Get rights and content
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Highlights

  • Selfish sex ratio (SR) distorters impede son transmission and must be silenced

  • Multiple SR suppressors in Drosophila simulans correspond to hairpin RNA-siRNA loci

  • Knockout of RNAi pathway derepresses SR drivers and disrupts spermatogenesis

  • Rapidly evolving intragenomic conflicts and suppression by RNAi may underlie speciation

Summary

Intragenomic conflicts are fueled by rapidly evolving selfish genetic elements, which induce selective pressures to innovate opposing repressive mechanisms. This is patently manifest in sex-ratio (SR) meiotic drive systems, in which distorter and suppressor factors bias and restore equal transmission of X and Y sperm. Here, we reveal that multiple SR suppressors in Drosophila simulans (Nmy and Tmy) encode related hairpin RNAs (hpRNAs), which generate endo-siRNAs that repress the paralogous distorters Dox and MDox. All components in this drive network are recently evolved and largely testis restricted. To connect SR hpRNA function to the RNAi pathway, we generated D. simulans null mutants of Dcr-2 and AGO2. Strikingly, these core RNAi knockouts massively derepress Dox and MDox and are in fact completely male sterile and exhibit highly defective spermatogenesis. Altogether, our data reveal how the adaptive capacity of hpRNAs is critically deployed to restrict selfish gonadal genetic systems that can exterminate a species.

Keywords

RNAi
hpRNA
siRNA
Drosophila simulans
sex ratio
intragenomic conflict
spermatogenesis

Cited by (0)

4

These authors contributed equally

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Present address: Division of Biochemistry and Biomedical Sciences, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia

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Lead Contact