Upon DNA damage, cyclin‐dependent kinases (CDKs) are typically inhibited to block cell division. In many organisms, however, it has been found that CDK activity is required for DNA repair, especially for homology‐dependent repair (HR), resulting in the conundrum how mitotic arrest and repair can be reconciled. Here, we show that Arabidopsis thaliana solves this dilemma by a division of labor strategy. We identify the plant‐specific B1‐type CDKs (CDKB1s) and the class of B1‐type cyclins (CYCB1s) as major regulators of HR in plants. We find that RADIATION SENSITIVE 51 (RAD51), a core mediator of HR, is a substrate of CDKB1‐CYCB1 complexes. Conversely, mutants in CDKB1 and CYCB1 fail to recruit RAD51 to damaged DNA. CYCB1;1 is specifically activated after DNA damage and we show that this activation is directly controlled by SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), a transcription factor that acts similarly to p53 in animals. Thus, while the major mitotic cell‐cycle activity is blocked after DNA damage, CDKB1‐CYCB1 complexes are specifically activated to mediate HR.

The retinoblastoma protein (Rb), which typically functions as a transcriptional repressor of E2F‐regulated genes, represents a major control hub of the cell cycle. Here, we show that loss of the Arabidopsis Rb homolog RETINOBLASTOMA‐RELATED 1 (RBR1) leads to cell death, especially upon exposure to genotoxic drugs such as the environmental toxin aluminum. While cell death can be suppressed by reduced cell‐proliferation rates, rbr1 mutant cells exhibit elevated levels of DNA lesions, indicating a direct role of RBR1 in the DNA‐damage response (DDR). Consistent with its role as a transcriptional repressor, we find that RBR1 directly binds to and represses key DDR genes such as RADIATION SENSITIVE 51 (RAD51), leaving it unclear why rbr1 mutants are hypersensitive to DNA damage. However, we find that RBR1 is also required for RAD51 localization to DNA lesions. We further show that RBR1 is itself targeted to DNA break sites in a CDKB1 activity‐dependent manner and partially co‐localizes with RAD51 at damage sites. Taken together, these results implicate RBR1 in the assembly of DNA‐bound repair complexes, in addition to its canonical function as a transcriptional regulator.

Summary The integrity of the genome is a fundamental prerequisite for the well‐being of all living organisms. Critical for the genomic integrity are effective DNA damage detection mechanisms that enable the cell to rapidly activate the necessary repair machinery. Here, we describe Arabidopsis thaliana ATCSA‐1, which is an ortholog of the mammalian Cockayne Syndrome type‐A protein involved in transcription‐coupled DNA repair processes. ATCSA‐1 is a critical component for initiating the repair of UV‐B‐induced DNA lesions, and, together with the damage‐specific DNA binding protein 2 (DDB2), is necessary for light‐independent repair processes in Arabidopsis. The transcriptional profile of both genes revealed that ATCSA‐1 is strongly expressed in most tissues, whereas DDB2 is only weakly expressed, predominantly in the root tips and anthers of flowers. In contrast to ATCSA‐1, DDB2 expression is rapidly inducible by UV treatment. Like DDB2, ATCSA‐1 is localized to the nucleus, and assembles with DDB1 and CUL4 proteins into a complex. ATCSA‐1 is an unstable protein that is degraded in a 26S proteasome‐dependent manner. Overall, the results presented here form a functional description of a plant Cockayne syndrome factor A (CSA) ortholog, and demonstrate the importance of ATCSA‐1 for UV‐B tolerance.

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