Centrophilic retrotransposon integration via CENH3 chromatin in Arabidopsis

Sayuri Tsukahara (), Alexandros Bousios (), Estela Perez-Roman, Sota Yamaguchi, Basile Leduque, Aimi Nakano, Matthew Naish, Akihisa Osakabe, Atsushi Toyoda, Hidetaka Ito, Alejandro Edera, Sayaka Tominaga, Juliarni, Kae Kato, Shoko Oda, Soichi Inagaki, Zdravko Lorković, Kiyotaka Nagaki, Frédéric Berger, Akira Kawabe, Leandro Quadrana, Ian Henderson and Tetsuji Kakutani ()
Additional contact information
Sayuri Tsukahara: The University of Tokyo
Alexandros Bousios: University of Sussex
Estela Perez-Roman: University of Sussex
Sota Yamaguchi: The University of Tokyo
Basile Leduque: Centre National de la Recherche Scientifique, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Université Evry, Université Paris‐Saclay
Aimi Nakano: The University of Tokyo
Matthew Naish: University of Cambridge
Akihisa Osakabe: The University of Tokyo
Atsushi Toyoda: National Institute of Genetics
Hidetaka Ito: Hokkaido University
Alejandro Edera: Centre National de la Recherche Scientifique, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Université Evry, Université Paris‐Saclay
Sayaka Tominaga: The University of Tokyo
Juliarni: The University of Tokyo
Kae Kato: National Institute of Genetics
Shoko Oda: The University of Tokyo
Soichi Inagaki: The University of Tokyo
Zdravko Lorković: Vienna BioCenter (VBC)
Kiyotaka Nagaki: Okayama University
Frédéric Berger: Vienna BioCenter (VBC)
Akira Kawabe: Kyoto Sangyo University
Leandro Quadrana: Centre National de la Recherche Scientifique, Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement, Université Evry, Université Paris‐Saclay
Ian Henderson: University of Cambridge
Tetsuji Kakutani: The University of Tokyo

Nature, 2025, vol. 637, issue 8046, 744-748

Abstract: Abstract 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 centromeres3–5. 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 Arabidopsis thaliana, 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.

Date: 2025
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DOI: 10.1038/s41586-024-08319-7

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