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DNA damage inArabidopsis thalianaseedlings results in upregulation of hundreds of genes. One of the earliest and highest levels of induction is displayed by a previously uncharacterized gene that we have termedX-ray induced 1(XRI1). Analysis of plants carrying a nullxri1allele revealed two distinct requirements for this gene in plant fertility. XRI1 was important for the post-meiotic stages of pollen development, leading to inviability ofxri−pollen and abnormal segregation of the mutant allele in heterozygousxri1+/−plants. In addition, XRI1 was essential for male and female meiosis, as indicated by the complete sterility of homozygousxri1mutants due to extensive chromosome fragmentation visible in meiocytes. Abolition of programmed DNA double-strand breaks in aspo11-1mutant background failed to rescue the DNA fragmentation ofxri1mutants, suggesting that XRI1 functions at an earlier stage than SPO11-1 does. Yeast two-hybrid studies identified an interaction between XRI1 and a novel component of the Arabidopsis MND1/AHP2 complex, indicating possible requirements for XRI1 in meiotic DNA repair.