The presence of endosymbiotically derived organelles with their own genomes (mitochondria and plastids) is a defining characteristic of eukaryotes, but the mechanisms by which these genomes are maintained and expressed differs wildly across the eukaryotic tree of life. I will present work from our group on how fundamental features of DNA repair and gene expression in plant organelles contrast with other eukaryotic lineages and how these differences have been shaped by horizontal/endosymbiotic gene transfer events. Specifically, I will show how plant MSH1, an enigmatic member of the MutS DNA repair family that was likely acquired from giant viruses, is responsible for the remarkably low mutation rates in land plant organelle genomes. In addition, I will describe how bacterial-like MutS2 genes were acquired via plastid endosymbiosis and, thus, distinguish plants from other eukaryotic lineages. Recent work in our lab suggests that these genes play key roles in maintaining plant organelle gene expression. Therefore, peculiarities of the Central Dogma of Molecular Biology in plant organelles reflect their complex evolutionary history and acquisition of foreign MutS genes.