Evolution of mitochondria and plastids across populations of a keystone marine plant Zostera marina

The genomes of mitochondria and plastids are testimony to their evolutionary origin as bacterial endosymbionts during the emergence of eukaryotic cells. The two organellar genomes differ markedly from the nuclear genome and between each another. They are smaller in size, can have a more complex genome organization and feature multiple copies per cell. Moreover, distinct modes of replication and inheritance of the organellar genomes define their unique evolutionary dynamics. Cross-species phylogenetic studies demonstrate lower evolutionary rates of the plant organelles in comparison to the nucleus. However, the fundamental principles governing organellar evolution remain understudied and the population genetics theory is lacking suitable models for organellar allele dynamics. Here we examine mitochondrial and plastid genomes across worldwide populations of a widespread marine flowering plant Zostera marina. We show that the composition of mitochondrial chromosomes remains remarkably conserved within Z. marina for over 350,000 years of evolution despite rapid shifts during individual plant development. Further we demonstrate that the mitochondrial and plastid DNA sequences mutate at the same rate, however plastid alleles at neutral sites remain in a heteroplasmic state ca. 20 times longer than mitochondrial. Using a stochastic agent-based simulation, we suggest that the difference in allele segregation time is due to differences in the inheritance mode of the two organelles. Our findings supply a link between observations of organellar evolution at the level of plant individuals and long-term evolution of taxonomic groups. Our research provides a general framework for population genetics of extrachromosomal elements, including e.g., prokaryotic plasmids. The mode of replication and inheritance of extrachromosomal elements have a stark effect on their evolution dynamics, a concept that can be applied also to symbiotic microbes in metaorganisms.