Structural variation and DNA methylation shape the centromere-proximal meiotic crossover landscape in Arabidopsis

Fernandes, J. B.; Naish, M.; Lian, Q.; Burns, R.; Tock, A. J.; Rabanal, F. A.; Wlodzimierz, P.; Habring, A.; Nicholas, R. E.; Weigel, D.; Mercier, R.; Henderson, I. R.

doi:10.1101/2023.06.12.544545

bioRxiv · 10.1101/2023.06.12.544545

Structural variation and DNA methylation shape the centromere-proximal meiotic crossover landscape in Arabidopsis

Fernandes, J. B.·Naish, M.·Lian, Q.·Burns, R.·Tock, A. J.·Rabanal, F. A.·Wlodzimierz, P.·Habring, A.·Nicholas, R. E.·Weigel, D.·Mercier, R.·Henderson, I. R.

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Abstract

BackgroundCentromeres load kinetochore complexes onto chromosomes, which mediate spindle attachment and allow segregation during cell division. Although centromeres perform a conserved cellular function, their underlying DNA sequences are highly divergent within and between species. Despite variability in DNA sequence, centromeres are also universally suppressed for meiotic crossover recombination, across eukaryotes. However, the genetic and epigenetic factors responsible for suppression of centromeric crossovers remain to be completely defined. ResultsTo explore the centromere-proximal recombination landscape, we mapped 14,397 crossovers against fully assembled Arabidopsis thaliana genomes. A. thaliana centromeres comprise megabase-scale satellite repeat arrays that load nucleosomes containing the CENH3 histone variant. Each chromosome possesses a structurally polymorphic 3-4 megabase region where crossovers were absent, that includes the satellite arrays, flanked by 1-2 megabase low-recombination zones. The recombination-suppressed regions are enriched for Gypsy/Ty3 retrotransposons, and additionally contain expressed genes with high genetic diversity that initiate meiotic recombination, yet do not crossover. We mapped crossovers at high-resolution in proximity to CEN3, which resolved punctate centromere-proximal hotspots that overlapped gene islands embedded in heterochromatin. Centromeres are densely DNA methylated and the recombination landscape was remodelled in DNA methylation mutants. We observed that the centromeric low-recombining zones decreased and increased crossovers in CG (met1) and non-CG (cmt3) mutants, respectively, whereas the core non recombining zones remained suppressed. ConclusionOur work relates the genetic and epigenetic organisation of the A. thaliana centromeres and flanking pericentromeric heterochromatin to the zones of crossover suppression that surround the CENH3-occupied satellite repeat arrays.

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Fernandes, J. B., Naish, M., Lian, Q., Burns, R., Tock, A. J., Rabanal, F. A., Wlodzimierz, P., Habring, A., Nicholas, R. E., Weigel, D., Mercier, R., Henderson, I. R.. 2023-06-12. Structural variation and DNA methylation shape the centromere-proximal meiotic crossover landscape in Arabidopsis. https://doi.org/10.1101/2023.06.12.544545

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