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Given the fundamental role of the MRE11 in many aspects of DNA metabolism and signaling in eukaryotes, we analyzed the impact of several MRE11 mutations on DNA damage response (DDR) and DNA repair in Arabidopsis thaliana. Three different atmre11 and an atatm-2 mutant lines, along with the wild-type (WT), were compared by a new -Arabidopsis genotoxic assay for in situ evaluation of the genome integrity and DNA damage repair efficiency after double strand break (DSB) induction. The results showed that, despite the phenotypic differences and the different lengths of the putative truncated AtMRE11 proteins, all three atmre11 and the atatm-2 mutant lines, exhibited common hypersensitivity to the bleomycin-treatment, upon which they reduced mitotic activities only slightly, indicating a G2/M checkpoint abrogation. In contrast to the WT which reduced the frequency of chromosomal aberrations through the recovery period after treatment, all three atmre11 and atatm-2 mutants did not recover. Moreover, atmre11-3 mutants, similarly to atatm-2 mutants, failed to transcriptionally induce several DDR genes and had altered expression of the CYCB1 ; 1::GUS protein. Nevertheless, numerous chromosomal fusions in the atmre11 mutants, observed after DNA damage induction, suggest intensive DNA repair activities. These results indicate that the functional and full-length AtMRE11 is essential for the activation of the cell cycle arrest, transcriptional regulation and the DNA repair upon the induction of DSBs.