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Mechanistic insights into DNA damage recognition and checkpoint control in plants

Abstract

The plant DNA damage response (DDR) pathway safeguards genomic integrity by rapid recognition and repair of DNA lesions that, if unrepaired, may cause genome instability. Most frequently, DNA repair goes hand in hand with a transient cell cycle arrest, which allows cells to repair the DNA lesions before engaging in a mitotic event, but consequently also affects plant growth and yield. Through the identification of DDR proteins and cell cycle regulators that react to DNA double-strand breaks or replication defects, it has become clear that these proteins and regulators form highly interconnected networks. These networks operate at both the transcriptional and post-transcriptional levels and include liquid–liquid phase separation and epigenetic mechanisms. Strikingly, whereas the upstream DDR sensors and signalling components are well conserved across eukaryotes, some of the more downstream effectors are diverged in plants, probably to suit unique lifestyle features. Additionally, DDR components display functional diversity across ancient plant species, dicots and monocots. The observed resistance of DDR mutants towards aluminium toxicity, phosphate limitation and seed ageing indicates that gaining knowledge about the plant DDR may offer solutions to combat the effects of climate change and the associated risk for food security.

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Fig. 1: Three-step-based activation of the DDR, leading to efficient DNA repair.
Fig. 2: Multistep formation of RAD51 nucleofilaments and the active SMC5/6 complex.
Fig. 3: The molecular mechanisms of the SOG1/WEE1-mediated DNA damage checkpoint.
Fig. 4: The roles of DREAM complexes in the DNA damage checkpoint control.
Fig. 5: The importance of a functional DDR during various environmental extremes.

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Acknowledgements

We thank A. Bleys, M. Dubois and J. Heyman for critical reading and editing of the manuscript. This work was supported by grants from the Research Foundation Flanders (projects G011420N and G0A6J24N).

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L.D.V. led the project. J.H., Q.-Q.L. and L.D.V. wrote the manuscript. J.H. and Q.-Q.L. prepared the figures. All authors read and approved the final manuscript.

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Correspondence to Lieven De Veylder.

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Herbst, J., Li, QQ. & De Veylder, L. Mechanistic insights into DNA damage recognition and checkpoint control in plants. Nat. Plants 10, 539–550 (2024). https://doi.org/10.1038/s41477-024-01652-9

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