Worldwide population genomics reveal long-term stability of the mitochondrial chromosome composition in a keystone marine plant

Mitochondrial genomes (mitogenomes) of flowering plants are comprised of multiple chromosomes. Their copy number and composition can be dynamic within and among individual plants due to uneven replication of the chromosomes and homologous recombination. Nonetheless, despite their functional importance, the level of mitogenome conservation within species remains understudied. Whether the ontogenetic variation translates to evolution of mitogenome composition over generations is currently unknown. Here we show that the mitochondrial chromosome composition of the seagrass Zostera marina is conserved among worldwide populations that diverged ca 350,000 years ago. Using long-read sequencing we characterized the Z. marina mitochondrial genome and inferred the repertoire of recombination-induced configurations of its eight chromosomes. To characterize the chromosome composition worldwide and study its evolution we examined the mitogenome in Z. marina meristematic region sampled in 16 populations from the Pacific and Atlantic oceans. Our results reveal a striking similarity in the chromosome copy number suggesting stable equal proportions among distantly related populations and a high conservation of the mitochondrial genome within the plant germline, despite a notable variability during individual ontogenesis. Our study supplies a link between observations of dynamic mitogenomes at the level of plant individuals and long-term mitochondrial evolution. Significance statementExtensive studies on evolution of plant mitochondria in individual plants revealed great variability of the mitogenome architecture across tissues, however, data on the mitochondrion evolution at the population level is still scarce. We show that the mitochondrial genome architecture in a keystone marine plant, Zostera marina, remained conserved over ca. 350,000 years worldwide. We suggest that the extreme conservation of the Z. marina mitochondria is a manifestation of streamlined mitochondria inheritance over plant generations, e.g., via a plant germline.