The mitochondrial genome of Malus domestica and the import-driven hypothesis of mitochondrial genome expansion in seed plants

Mitochondrial genomes of spermatophytes are the largest among all organellar genomes. Their large size has been attributed to various factors; however the relative contribution of these factors to mtDNA expansion remains undetermined. We estimated their relative contribution in Malus domestica (apple). The mitochondrial genome of apple has a size of 396,947 bp and a one to nine ratio of coding to non-coding DNA, close to the corresponding average values for angiosperms. We determined that 71.5% of the apple mtDNA sequence was highly similar to sequences of its nuclear DNA. Using nuclear gene exons, nuclear transposable elements and chloroplast DNA as markers of promiscuous DNA content in mtDNA, we estimated that, approximately, 20% of the apple mtDNA consisted of DNA sequence imported from other cell compartments, mostly from the nucleus. Similar marker-based estimates of promiscous DNA content in the mitochondrial genomes of other species ranged between 21.2-25.3% of the total mtDNA length for grape, between 23.1-38.6% for rice, and between 47.1-78.4% for maize. All these estimates are conservative, because they underestimate the import of non-functional DNA. We propose that the import of promiscuous DNA is a core mechanism for mtDNA size expansion in seed plants. In apple, maize and grape this mechanism contributed far more to genome expansion than did homologous recombination. In rice the estimated contribution of both mechanisms was found to be similar.