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.

Central European Institute of Technology Masaryk University Brno Czech Republic

Departamento de Genética Molecular de Plantas Centro Nacional de Biotecnología Consejo Superior de Investigaciones Científicas Madrid Spain

Department of Chromosome Biology Max Planck Institute for Plant Breeding Research Cologne Germany

Department of Molecular Biology Max Planck Institute for Biology Tübingen Tübingen Germany

Department of Plant Sciences University of Cambridge Cambridge UK

Gregor Mendel Institute Vienna Austrian Academy of Sciences Vienna BioCenter Vienna Austria

LIPME INRAE CNRS Université de Toulouse Castanet Tolosan France

School of Life Sciences University of Sussex Brighton UK

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