The genetic and epigenetic landscape of the Arabidopsis centromeres

Matthew Naish; Michael Alonge; Piotr Wlodzimierz; Andrew J. Tock; Bradley W. Abramson; Anna Schmücker; Terezie Mandáková; Bhagyshree Jamge; Christophe Lambing; Pallas Kuo; Natasha Yelina; Nolan Hartwick; Kelly Colt; Lisa M. Smith; Jurriaan Ton; Tetsuji Kakutani; Robert A. Martienssen; Korbinian Schneeberger; Martin A. Lysak; Frédéric Berger; Alexandros Bousios; Todd P. Michael; Michael C. Schatz; Ian R. Henderson

doi:10.1126/science.abi7489

The genetic and epigenetic landscape of the Arabidopsis centromeres

Matthew Naish, Michael Alonge, Piotr Wlodzimierz, Andrew J. Tock, Bradley W. Abramson, Anna Schmücker, Terezie Mandáková, Bhagyshree Jamge, Christophe Lambing, Pallas Kuo, Natasha Yelina, Nolan Hartwick, Kelly Colt, Lisa M. Smith, Jurriaan Ton, Tetsuji Kakutani, Robert A. Martienssen, Korbinian Schneeberger, Martin A. Lysak, Frédéric BergerAlexandros Bousios, Todd P. Michael, Michael C. Schatz, Ian R. Henderson

Research output: Contribution to journal › Article › peer-review

Abstract

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.

Original language	English (US)
Article number	eabi7489
Journal	Science
Volume	374
Issue number	6569
DOIs	https://doi.org/10.1126/science.abi7489
State	Published - Nov 12 2021
Externally published	Yes

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Naish, M., Alonge, M., Wlodzimierz, P., Tock, A. J., Abramson, B. W., Schmücker, A., Mandáková, T., Jamge, B., Lambing, C., Kuo, P., Yelina, N., Hartwick, N., Colt, K., Smith, L. M., Ton, J., Kakutani, T., Martienssen, R. A., Schneeberger, K., Lysak, M. A., ... Henderson, I. R. (2021). The genetic and epigenetic landscape of the Arabidopsis centromeres. Science, 374(6569), Article eabi7489. https://doi.org/10.1126/science.abi7489

Naish, M, Alonge, M, Wlodzimierz, P, Tock, AJ, Abramson, BW, Schmücker, A, Mandáková, T, Jamge, B, Lambing, C, Kuo, P, Yelina, N, Hartwick, N, Colt, K, Smith, LM, Ton, J, Kakutani, T, Martienssen, RA, Schneeberger, K, Lysak, MA, Berger, F, Bousios, A, Michael, TP, Schatz, MC & Henderson, IR 2021, 'The genetic and epigenetic landscape of the Arabidopsis centromeres', Science, vol. 374, no. 6569, eabi7489. https://doi.org/10.1126/science.abi7489

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title = "The genetic and epigenetic landscape of the Arabidopsis centromeres",

abstract = "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.",

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AU - Wlodzimierz, Piotr

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AU - Abramson, Bradley W.

AU - Schmücker, Anna

AU - Mandáková, Terezie

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AU - Colt, Kelly

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AU - Ton, Jurriaan

AU - Kakutani, Tetsuji

AU - Martienssen, Robert A.

AU - Schneeberger, Korbinian

AU - Lysak, Martin A.

AU - Berger, Frédéric

AU - Bousios, Alexandros

AU - Michael, Todd P.

AU - Schatz, Michael C.

AU - Henderson, Ian R.

PY - 2021/11/12

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N2 - 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.

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The genetic and epigenetic landscape of the Arabidopsis centromeres

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