Recombination and intraspecific polymorphism for the presence and absence of entire chromosomes in mitochondrial genomes.

Although mitochondrial genomes are typically thought of as single circular molecules, these genomes are fragmented into multiple chromosomes in many eukaryotes, raising intriguing questions about inheritance and (in)stability of mtDNA in such systems. A previous comparison of mitochondrial genomes from two different individuals of the angiosperm species Silene noctiflora found variation in the presence of entire mitochondrial chromosomes. Here, we expand on this work with a geographically diverse sampling of 25 S. noctiflora populations and the closely related species S. turkestanica and S. undulata. Using a combination of deep sequencing and PCR-based screening for the presence of 22 different mitochondrial chromosomes, we found extensive variation in the complement of chromosomes across individuals. Much of this variation could be attributed to recent chromosome loss events, suggesting that the massively expanded and fragmented mitochondrial genomes of S. noctiflora may have entered a phase of genome reduction in which they are losing entire chromosomes at a rapid rate. Sequence analysis of mitochondrial and plastid genomes revealed genealogical differences both between these organelles and within the mitochondrial genome, indicating a history of recombination. Evidence that recombination has generated novel combinations of alleles was more frequent between loci on different mitochondrial chromosomes than it was within chromosomes. Therefore, the fragmentation of mitochondrial genomes and the assortment of chromosomes during mitochondrial inheritance appears to have contributed to a history of sexual-like recombination in the mtDNA of this species.