Atsushi Shimada, Jonathan Cahn, Evan Ernst, Jason Lynn, Daniel Grimanelli, Ian Henderson, Tetsuji Kakutani, Robert A. Martienssen
{"title":"Retrotransposon addiction promotes centromere function via epigenetically activated small RNAs","authors":"Atsushi Shimada, Jonathan Cahn, Evan Ernst, Jason Lynn, Daniel Grimanelli, Ian Henderson, Tetsuji Kakutani, Robert A. Martienssen","doi":"10.1038/s41477-024-01773-1","DOIUrl":null,"url":null,"abstract":"Retrotransposons have invaded eukaryotic centromeres in cycles of repeat expansion and purging, but the function of centromeric retrotransposons has remained unclear. In Arabidopsis, centromeric ATHILA retrotransposons give rise to epigenetically activated short interfering RNAs in mutants in DECREASE IN DNA METHYLATION1 (DDM1). Here we show that mutants that lose both DDM1 and RNA-dependent RNA polymerase have pleiotropic developmental defects and mis-segregate chromosome 5 during mitosis. Fertility and segregation defects are epigenetically inherited with centromere 5, and can be rescued by directing artificial small RNAs to ATHILA5 retrotransposons that interrupt tandem satellite repeats. Epigenetically activated short interfering RNAs promote pericentromeric condensation, chromosome cohesion and chromosome segregation in mitosis. We propose that insertion of ATHILA silences centromeric transcription, while simultaneously making centromere function dependent on retrotransposon small RNAs in the absence of DDM1. Parallels are made with the fission yeast Schizosaccharomyces pombe, where chromosome cohesion depends on RNA interference, and with humans, where chromosome segregation depends on both RNA interference and HELLSDDM1. Centromeric satellite repeats on Arabidopsis chromosome 5 are interrupted by ATHILA5 retrotransposons, and cohesion is compromised in ddm1 chromatin remodelling mutants that have also lost RNAi. Mis-segregation is epigenetically inherited but can be rescued by ATHILA5 small RNA.","PeriodicalId":18904,"journal":{"name":"Nature Plants","volume":null,"pages":null},"PeriodicalIF":15.8000,"publicationDate":"2024-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41477-024-01773-1.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Nature Plants","FirstCategoryId":"99","ListUrlMain":"https://www.nature.com/articles/s41477-024-01773-1","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Retrotransposons have invaded eukaryotic centromeres in cycles of repeat expansion and purging, but the function of centromeric retrotransposons has remained unclear. In Arabidopsis, centromeric ATHILA retrotransposons give rise to epigenetically activated short interfering RNAs in mutants in DECREASE IN DNA METHYLATION1 (DDM1). Here we show that mutants that lose both DDM1 and RNA-dependent RNA polymerase have pleiotropic developmental defects and mis-segregate chromosome 5 during mitosis. Fertility and segregation defects are epigenetically inherited with centromere 5, and can be rescued by directing artificial small RNAs to ATHILA5 retrotransposons that interrupt tandem satellite repeats. Epigenetically activated short interfering RNAs promote pericentromeric condensation, chromosome cohesion and chromosome segregation in mitosis. We propose that insertion of ATHILA silences centromeric transcription, while simultaneously making centromere function dependent on retrotransposon small RNAs in the absence of DDM1. Parallels are made with the fission yeast Schizosaccharomyces pombe, where chromosome cohesion depends on RNA interference, and with humans, where chromosome segregation depends on both RNA interference and HELLSDDM1. Centromeric satellite repeats on Arabidopsis chromosome 5 are interrupted by ATHILA5 retrotransposons, and cohesion is compromised in ddm1 chromatin remodelling mutants that have also lost RNAi. Mis-segregation is epigenetically inherited but can be rescued by ATHILA5 small RNA.
期刊介绍:
Nature Plants is an online-only, monthly journal publishing the best research on plants — from their evolution, development, metabolism and environmental interactions to their societal significance.