Eukaryotic organisms have evolved a set of strategies to safeguard genome integrity, but the underlying mechanisms remain poorly understood. Here, we report that ASYMMETRIC LEAVES1/2 ENHANCER7 ( AE7 ), an Arabidopsis thaliana gene encoding a protein in the evolutionarily conserved Domain of Unknown Function 59 family, participates in the cytosolic iron-sulfur ( Fe-S ) cluster assembly ( CIA ) pathway to maintain genome integrity. The severe ae7-2 allele is embryo lethal, whereas plants with the weak ae7 ( ae7-1 ) allele are viable but exhibit highly accumulated DNA damage that activates the DNA damage response to arrest the cell cycle. AE7 is part of a protein complex with CIA1, NAR1, and MET18, which are highly conserved in eukaryotes and are involved in the biogenesis of cytosolic and nuclear Fe-S proteins. ae7-1 plants have lower activities of the cytosolic (4Fe-4S) enzyme aconitase and the nuclear (4Fe-4S) enzyme DNA glycosylase ROS1. Additionally, mutations in the gene encoding the mitochondrial ATP binding cassette transporter ATM3/ABCB25, which is required for the activity of cytosolic Fe-S enzymes in Arabidopsis , also result in defective genome integrity similar to that of ae7-1 . These results indicate that AE7 is a central member of the CIA pathway, linking plant mitochondria to nuclear genome integrity through assembly of Fe-S proteins. Glossary Fe-S iron-sulfur DSB double-strand break CIA cytosolic iron-sulfur cluster assembly MMS methyl methanesulfonate HR homologous recombination qRT-PCR quantitative RT-PCR L er Landsberg erecta Col-0 Columbia-0 GUS β-glucuronidase Co-IP coimmunoprecipitation BiFC bimolecular fluorescence complementation ACO aconitase AO aldehyde oxidase TAP tandem affinity protein YFP yellow fluorescent protein
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