The Massive Mitochondrial Genome of the Angiosperm Silene noctiflora Is Evolving By Gain or Loss of Entire Chromosomes

Mitochondria, exhibit extreme diversity in mitochondrial genome architecture across eukaryotes, reflecting a remarkable history of highly divergent evolutionary trajectories. In particular, flowering plants have highly derived and diverse mitochondrial genome structures, including the largest and most complex mitochondrial genomes ever identified. For example, the mitochondrial genome of Silene noctiflora (Caryophyllaceae) is 7 Mb in size, larger than most bacterial genomes and even some nuclear genomes, and has been fragmented into dozens of circular mapping chromosomes. However, the ongoing evolution of these multichromosomal structures at an intraspecific level is still unexplored. We have sequenced two mitochondrial genomes from different populations (BRP and OSR) of Silene noctiflora. Overall, these genomes exhibit a high degree of similarity in sequence and structure, but they differ in the presence or absence of entire chromosomes, resulting in a difference of 410 kb in length and chromosome number (6.7 vs 7.1 Mb and 59 vs 63 chromsomes). Eight of the 59 chromosomes in OSR and 11 of the 63 in BRP are unique to their respective genomes.Therefore, in the time that these genomes have accumulated only 9 SNPs in >30 kb of protein-coding gene sequence, they have gained or lost 19 entire chromosomes, most of which contain no identifiable genes. As a result, the two genomes contain the same functional gene content. Our results have important implications for the massive expansion in plant mitochondrial genomes, the repeated evolution of multichromosomal organelle genomes across eukaryotes, and the proliferation and maintenance of non-coding DNA.