Centrophilic retrotransposon integration via CENH3 chromatin in Arabidopsis

• 成果类型: Article
• 署名作者: Tsukahara, Sayuri; Bousios, Alexandros; Perez-Roman, Estela; Yamaguchi, Sota; Leduque, Basile; Nakano, Aimi; Naish, Matthew; Osakabe, Akihisa; Toyoda, Atsushi; Ito, Hidetaka; Edera, Alejandro; Tominaga, Sayaka; Juliarni, Kae; Kato, Kae; Oda, Shoko; Inagaki, Soichi; Lorkovic, Zdravko; Nagaki, Kiyotaka; Berger, Frederic; Kawabe, Akira; Quadrana, Leandro; Henderson, Ian; Kakutani, Tetsuji
• 署名单位: University of Tokyo; University of Sussex; Universite Paris Saclay; INRAE; Universite Paris Cite; University of Cambridge; Research Organization of Information & Systems (ROIS); National Institute of Genetics (NIG) - Japan; Hokkaido University; Research Organization of Information & Systems (ROIS); National Institute of Genetics (NIG) - Japan; Vienna Biocenter (VBC); Austrian Academy of Sciences; Okayama University; Kyoto Sangyo University
• 刊物名称: Nature
• ISSN/ISSBN: 0028-2487
• DOI: 10.1038/s41586-024-08319-7
• 发表日期: 2025-01-16
• 关键词: dna methylation; transposable elements; epigenetic control; site selection; sequence; maintenance; heterochromatin; Visualization; retroviruses; divergence

摘要

In organisms ranging from vertebrates to plants, major components of centromeres are rapidly evolving repeat sequences, such as tandem repeats (TRs) and transposable elements (TEs), which harbour centromere-specific histone H3 (CENH3)1,2. Complete centromere structures recently determined in human and Arabidopsis suggest frequent integration and purging of retrotransposons within the TR regions of centromeres3, 4-5. Despite the high impact of 'centrophilic' retrotransposons on the paradox of rapid centromere evolution, the mechanisms involved in centromere targeting remain poorly understood in any organism. Here we show that both Ty3 and Ty1 long terminal repeat retrotransposons rapidly turnover within the centromeric TRs of Arabidopsis species. We demonstrate that the Ty1/Copia element Tal1 (Transposon of Arabidopsis lyrata 1) integrates de novo into regions occupied by CENH3 in Arabidopsisthaliana, and that ectopic expansion of the CENH3 region results in spread of Tal1 integration regions. The integration spectra of chimeric TEs reveal the key structural variations responsible for contrasting chromatin-targeting specificities to centromeres versus gene-rich regions, which have recurrently converted during the evolution of these TEs. Our findings show the impact of centromeric chromatin on TE-mediated rapid centromere evolution, with relevance across eukaryotic genomes.