Cycles of satellite and transposon evolution in Arabidopsis centromeres

Piotr Wlodzimierz, Fernando A. Rabanal, Robin Burns, Matthew Naish, Elias Primetis, Alison Scott, Terezie Mandáková, Nicola Gorringe, Andrew J. Tock, Daniel Holland, Katrin Fritschi, Anette Habring, Christa Lanz, Christie Patel, Theresa Schlegel, Maximilian Collenberg, Miriam Mielke, Magnus Nordborg, Fabrice Roux, Gautam Shirsekar, Carlos Alonso-Blanco, Martin A. Lysak, Polina Y. Novikova, Alexandros Bousios (), Detlef Weigel () and Ian R. Henderson ()
Additional contact information
Piotr Wlodzimierz: University of Cambridge
Fernando A. Rabanal: Max Planck Institute for Biology Tübingen
Robin Burns: University of Cambridge
Matthew Naish: University of Cambridge
Elias Primetis: University of Sussex
Alison Scott: Max Planck Institute for Plant Breeding Research
Terezie Mandáková: Masaryk University
Nicola Gorringe: University of Cambridge
Andrew J. Tock: University of Cambridge
Daniel Holland: University of Cambridge
Katrin Fritschi: Max Planck Institute for Biology Tübingen
Anette Habring: Max Planck Institute for Biology Tübingen
Christa Lanz: Max Planck Institute for Biology Tübingen
Christie Patel: University of Cambridge
Theresa Schlegel: Max Planck Institute for Biology Tübingen
Maximilian Collenberg: Max Planck Institute for Biology Tübingen
Miriam Mielke: Max Planck Institute for Biology Tübingen
Magnus Nordborg: Gregor Mendel Institute, Vienna, Austrian Academy of Sciences, Vienna BioCenter
Fabrice Roux: Université de Toulouse
Gautam Shirsekar: Max Planck Institute for Biology Tübingen
Carlos Alonso-Blanco: Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas
Martin A. Lysak: Masaryk University
Polina Y. Novikova: Max Planck Institute for Plant Breeding Research
Alexandros Bousios: University of Sussex
Detlef Weigel: Max Planck Institute for Biology Tübingen
Ian R. Henderson: University of Cambridge

Nature, 2023, vol. 618, issue 7965, 557-565

Abstract: Abstract Centromeres are critical for cell division, loading CENH3 or CENPA histone variant nucleosomes, directing kinetochore formation and allowing chromosome segregation1,2. Despite their conserved function, centromere size and structure are diverse across species. To understand this centromere paradox3,4, it is necessary to know how centromeric diversity is generated and whether it reflects ancient trans-species variation or, instead, rapid post-speciation divergence. To address these questions, we assembled 346 centromeres from 66 Arabidopsis thaliana and 2 Arabidopsis lyrata accessions, which exhibited a remarkable degree of intra- and inter-species diversity. A. thaliana centromere repeat arrays are embedded in linkage blocks, despite ongoing internal satellite turnover, consistent with roles for unidirectional gene conversion or unequal crossover between sister chromatids in sequence diversification. Additionally, centrophilic ATHILA transposons have recently invaded the satellite arrays. To counter ATHILA invasion, chromosome-specific bursts of satellite homogenization generate higher-order repeats and purge transposons, in line with cycles of repeat evolution. Centromeric sequence changes are even more extreme in comparison between A. thaliana and A. lyrata. Together, our findings identify rapid cycles of transposon invasion and purging through satellite homogenization, which drive centromere evolution and ultimately contribute to speciation.

Date: 2023
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DOI: 10.1038/s41586-023-06062-z

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