Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans

Meiotic drive loci distort the normally equal segregation of alleles, which benefits their own transmission even in the face of severe fitness costs to their host organism. However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms...

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Veröffentlicht in:PLoS biology 2023-06, Vol.21 (6), p.e3002136
Hauptverfasser: Vedanayagam, Jeffrey, Herbette, Marion, Mudgett, Holly, Lin, Ching-Jung, Lai, Chun-Ming, McDonough-Goldstein, Caitlin, Dorus, Stephen, Loppin, Benjamin, Meiklejohn, Colin, Dubruille, Raphaëlle, Lai, Eric C
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container_title PLoS biology
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creator Vedanayagam, Jeffrey
Herbette, Marion
Mudgett, Holly
Lin, Ching-Jung
Lai, Chun-Ming
McDonough-Goldstein, Caitlin
Dorus, Stephen
Loppin, Benjamin
Meiklejohn, Colin
Dubruille, Raphaëlle
Lai, Eric C
description Meiotic drive loci distort the normally equal segregation of alleles, which benefits their own transmission even in the face of severe fitness costs to their host organism. However, relatively little is known about the molecular identity of meiotic drivers, their strategies of action, and mechanisms that can suppress their activity. Here, we present data from the fruitfly Drosophila simulans that address these questions. We show that a family of de novo, protamine-derived X-linked selfish genes (the Dox gene family) is silenced by a pair of newly emerged hairpin RNA (hpRNA) small interfering RNA (siRNA)-class loci, Nmy and Tmy. In the w[XD1] genetic background, knockout of nmy derepresses Dox and MDox in testes and depletes male progeny, whereas knockout of tmy causes misexpression of PDox genes and renders males sterile. Importantly, genetic interactions between nmy and tmy mutant alleles reveal that Tmy also specifically maintains male progeny for normal sex ratio. We show the Dox loci are functionally polymorphic within D. simulans, such that both nmy-associated sex ratio bias and tmy-associated sterility can be rescued by wild-type X chromosomes bearing natural deletions in different Dox family genes. Finally, using tagged transgenes of Dox and PDox2, we provide the first experimental evidence Dox family genes encode proteins that are strongly derepressed in cognate hpRNA mutants. Altogether, these studies support a model in which protamine-derived drivers and hpRNA suppressors drive repeated cycles of sex chromosome conflict and resolution that shape genome evolution and the genetic control of male gametogenesis.
doi_str_mv 10.1371/journal.pbio.3002136
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subjects Alleles
Animals
Biology and Life Sciences
Cell division
Chromosomes
Drosophila
Drosophila - genetics
Drosophila simulans
Drosophila simulans - genetics
Equilibrium
Fertility
Fruit flies
Gametogenesis
Gene silencing
Genes
Genetic aspects
Genetic control
Genetic engineering
Genetic research
Genomes
Genotype & phenotype
Insects
Life Sciences
Male
Males
Meiosis
Meiosis - genetics
Meiotic drive
Mutants
Progeny
Protamine
Research and Analysis Methods
Ribonucleic acid
RNA
RNA, Small Interfering - genetics
Sex
Sex chromosomes
Sex Chromosomes - genetics
Sex Ratio
siRNA
Sterility
Suppressors
Transgenes
X Chromosome
title Essential and recurrent roles for hairpin RNAs in silencing de novo sex chromosome conflict in Drosophila simulans
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