A record-setting mitogenome in the holoparasitic plant Balanophorayakushimensis accompanied by exceptional loss of organellar DNA repair and recombination genes

Background: Despite only limited sampling, the holoparasitic plant family Balanophoraceae harbors extreme mito-genome diversity and also has exceptionally divergent plastomes. We therefore sequenced the mitochondrial, plastid, and nuclear genomes of Balanophora yakushimensis and its transcriptome. Results: At 1.1 Mb, the B. yakushimensis mitogenome is one of the largest known mitogenomes. Driving this expansion and generating the most repeat-rich mitogenome in land plants are many large (up to 200 kb) duplications and a massive proliferation of short, AT-rich repeated sequences. The repeat proliferation, in conjunction with a highly elevated and unusually AT-biased mutation rate, has produced what is by far the most AT-rich land-plant mito-genome. These invasive repeats also created giant introns, unprecedented in size for organelles, and greatly expanded all rDNA exons. We discovered a record-low, for all genomes, transition/transversion ratio (0.12) in B. yakushimensis mtDNA and documented a 26-fold range in this ratio across angiosperm mitogenomes. The B. yakushimensis nuclear genome has lost exceptionally many genes that function in organellar DNA recombination, repair, and replication (RRR). We discuss ways in which these losses—and other genetic alterations as well as non-genetic ones—may or may not be related to the unusual features of both its mitochondrial and plastid genomes. Conclusions: The mitogenome of B. yakushimensis possesses many exceptional, indeed record-setting properties. The unprecedented loss of nuclear genes for organellar DNA RRR may explain some of these unusual features. These findings expand the boundaries of mitogenome deviancy and raise outstanding questions about the forces driving such extravagantly diversifying evolution.