DNA damage is a rare event in somatic cells and its repair often leads to deletions, insertions or translocations. In contrast, meiotic cells undergo 150-200 programmed-DNA double-strand breaks (DSBs) with no evidence of genome instability. These DSBs are formed in the chromatin loops tethered to a chromosome axis and form an important substrate for recombination to take place between chromosomes to create novel genetic variation to be transmitted to offspring. However, it remains incompletely understood how these DSBs are processed during meiosis. Moreover, several DNA repair proteins that are expressed in somatic cells are also expressed in meiosis. Why? Can their functions differ between the two cell types? Our work focuses on the kinase ATR, a central factor in somatic DNA repair in Arabidopsis. Our study shows that the function of ATR is integral to the meiotic regulatory programme playing a suppressing role on Class I and Class II crossover formation. Notably, this is reminiscent of its somatic function in inter-sister recombination following DNA damage. Furthermore, we reveal that in conditions where the integrity of the meiotic chromosome axis is perturbed, ATR function switches to a pro-crossover role. Additionally, we show that ATR regulates the localisation of the recombination proteins RPA1a and DMC1 and phosphorylates the axis protein ASY1. Overall, our study reveals that the DSB processing function of ATR is influenced by the cellular context. The extent to which the functions of DNA repair proteins are influenced by the meiotic cellular context to control crossover formation will be discussed.