Intraspecific Polymorphism for the Presence and Absence of Entire Mitochondrial Chromosomes

Abstract

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. We also included the closely related species S. turkestanica and S. undulata, with the latter exhibiting a surprising phylogenetic placement nested within the diversity of S. noctiflora mitochondrial haplotypes. 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. Despite the fragmented structures of these mitochondrial genomes and the evidence for occasional biparental inheritance in other Silene species, we did not find any indication of recombination between distinct mitochondrial haplotypes either within or among mitochondrial chromosomes, which may reflect the extreme paucity of nucleotide sequence polymorphism and/or the high selfing rate in this species. These results suggest 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.