RADA is a main branch migration factor in plant mitochondrial recombination and its defect leads to mtDNA instability and cell cycle arrest

Abstract

The mitochondria of flowering plants have large and complex genomes whose structure and segregation are modulated by recombination activities. The late steps of mitochondrial recombination are still poorly characterized: while the loss of mitochondrial recombination is not viable, a deficiency in RECG1-dependent branch migration has little impact on plant development, implying the existence of alternative pathways. Here we present RADA, an ortholog of bacterial RadA/Sms, which is required for the processing of organellar recombination intermediates. While bacterial RadA is dispensable, RADA-deficient plants are severely impacted in their development and fertility, correlating with increased mtDNA ectopic recombination and replication of recombination-generated subgenomes. The radA mutation is epistatic to recG1, indicating that RADA drives the main branch migration pathway of plant mitochondria. In contrast, the double mutation radA recA3 is lethal, underlining the importance of an alternative RECA3-dependent pathway. Although RADA is dually targeted to mitochondria and chloroplasts, we found little to no effects of radA on the stability of the plastidial genome. The stunted growth of radA mutants could not be correlated with obvious defects in mitochondrial gene expression. Rather, it seems that is partially caused by a retrograde signal that activates nuclear genes repressing cell cycle progression.