Mitochondria of flowering plants have large genomes whose structure and segregation are modulated by recombination activities. The post-synaptic late steps of mitochondrial DNA (mtDNA) recombination are still poorly characterized. Here we show that RADA, a plant ortholog of bacterial RadA/Sms, is an organellar protein that drives the major branch-migration pathway of plant mitochondria. While RadA/Sms is dispensable in bacteria, RADA-deficient Arabidopsis plants are severely impacted in their development and fertility, correlating with increased mtDNA recombination across intermediate-size repeats and accumulation of recombination-generated mitochondrial subgenomes. The radA mutation is epistatic to recG1 that affects the additional branch migration activity. In contrast, the double mutation radA recA3 is lethal, underlining the importance of an alternative RECA3-dependent pathway. The physical interaction of RADA with RECA2 but not with RECA3 further indicated that RADA is required for the processing of recombination intermediates in the RECA2-depedent recombination pathway of plant mitochondria. Although RADA is dually targeted to mitochondria and chloroplasts we found little to no effects of the radA mutation on the stability of the plastidial genome. Finally, we found that the deficient maintenance of the mtDNA in radA apparently triggers a retrograde signal that activates nuclear genes repressing cell cycle progression.
The involvement of the different Lactuca species in the domestication and diversification of cultivated lettuce is not totally understood. Lactuca serriola is considered as the direct ancestor and the closest relative to Lactuca sativa, while the other wild species that can be crossed with L. sativa, Lactuca virosa, and Lactuca saligna, would have just contributed to the latter diversification of cultivated typologies. To contribute to the study of Lactuca evolution, we assembled the mtDNA genomes of nine Lactuca spp. accessions, among them three from L. virosa, whose mtDNA had not been studied so far. Our results unveiled little to no intraspecies variation among Lactuca species, with the exception of L. serriola where the accessions we sequenced diverge significantly from the mtDNA of a L. serriola accession already reported. Furthermore, we found a remarkable phylogenetic closeness between the mtDNA of L. sativa and the mtDNA of L. virosa, contrasting to the L. serriola origin of the nuclear and plastidial genomes. These results suggest that a cross between L. virosa and the ancestor of cultivated lettuce is at the origin of the actual mitochondrial genome of L. sativa.
Arabidopsis RADA is a main branch migration activity in plant mitochondria, whose 40 deficiency leads to mtDNA instability by recombination, and suppression of plant growth by 41 the activation of repressors of cell cycle progression. 42 43 44 ABSTRACT 45 46 The mitochondria of flowering plants have large and complex genomes whose structure and 47 segregation are modulated by recombination activities. Among unresolved questions is what 48 are the pathways responsible for the late steps of homologous recombination: while the loss 49 of mitochondrial recombination is not viable, a deficiency in RECG1-dependent branch 50 migration has little impact on plant development. Here we present an additional pathway 51 required for the processing of organellar recombination intermediates, the one depending on 52RADA. RADA is similar in structure and activity to bacterial RadA/Sms, and in vitro it binds to 53 ssDNA and accelerates strand-exchange reactions initiated by RecA. RADA-deficient plants 54 are severely impacted in their development and fertility, correlating with increased mtDNA 55 ectopic recombination and replication of recombination-generated subgenomes. The radA 56 mutation is epistatic to recG1, indicating that RADA drives the main branch migration 57 pathway of plant mitochondria. In contrast, the double mutation radA recA3 is lethal, 58 revealing the importance of an alternative RECA3-dependent pathway.
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