Centromeres attach chromosomes to spindle microtubules during cell division and, despite this conserved role, show paradoxically rapid evolution and are typified by complex repeats. We used long-read sequencing to generate the Col-CEN Arabidopsis thaliana genome assembly that resolves all five centromeres. The centromeres consist of megabase-scale tandemly repeated satellite arrays, which support CENTROMERE SPECIFIC HISTONE H3 (CENH3) occupancy and are densely DNA methylated, with satellite variants private to each chromosome. CENH3 preferentially occupies satellites that show the least amount of divergence and occur in higher-order repeats. The centromeres are invaded by ATHILA retrotransposons, which disrupt genetic and epigenetic organization. Centromeric crossover recombination is suppressed, yet low levels of meiotic DNA double-strand breaks occur that are regulated by DNA methylation. We propose that Arabidopsis centromeres are evolving through cycles of satellite homogenization and retrotransposon-driven diversification.

Central European Institute of Technology Masaryk University Kamenice 5 Brno 625 00 Czech Republic

Department of Biological Sciences University of Tokyo Tokyo Japan

Department of Chromosome Biology Max Planck Institute for Plant Breeding Research Carl von Linné Weg 10 50829 Cologne Germany

Department of Computer Science Johns Hopkins University Baltimore MD USA

Department of Plant Sciences Downing Street University of Cambridge Cambridge CB2 3EA UK

Faculty of Biology LMU Munich Großhaderner Str 2 82152 Planegg Martinsried Germany

Gregor Mendel Institute Dr Bohr Gasse 3 1030 Vienna Austria

Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor NY USA

School of Biosciences and Institute for Sustainable Food University of Sheffield Sheffield S10 2TN UK

School of Life Sciences University of Sussex Brighton BN1 9RH UK

The Plant Molecular and Cellular Biology Laboratory Salk Institute for Biological Studies La Jolla CA USA

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Trends Genet. 2022 May;38(5):416-418. doi: 10.1016/j.tig.2022.02.001. PubMed

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