The structure of mitochondrial genomes is associated with geography in Arabidopsis thaliana

Chloroplasts and mitochondria are the primary sites for photosynthesis and respiration, each harboring its own unique genome. Although the organellar genomes are considerably smaller compared to the nuclear genome, they are nonetheless essential for survival of the organism. A common feature of many chloroplast and mitochondrial genomes is the presence of large repeated sequences longer than 1 kb. These can be either in inverted or direct orientation, and recombination between them leads to structural heteroplasmy. To understand the intraspecific evolution of organellar genomes, we assembled chloroplast and mitochondrial genomes of 143 A. thaliana accessions from PacBio HiFi sequencing data. We find large repeats to be associated with heteroplasmy and structural variation. Our extensive genome annotation identifies novel open reading frames (ORFs) in those accessions that lost large repeats, potentially introduced via horizontal gene transfer, illuminating additional paths for diversification of plant organelles. The loss of large repeats correlates with geography and phenotypes, pointing to their adaptive importance. The assembled and annotated organellar genomes constitute a rich source for future functional studies of the interaction between the three genomes of a plant.