Origin of three characteristic onion (Allium cepa L.) mitochondrial genome rearrangements in Allium species

Abstract

Dynamic mitochondrial genome rearrangements between normal and male-sterile onions (Allium cepa) were reported in previous studies, but the origin and distribution of these rearrangements in other Allium species remain unknown. Distribution of three characteristic mitochondrial DNA (mtDNA) rearrangements was surveyed using 32 Allium species. The trans-splicing group II intron of cox2, first identified in onions, was observed in all tested Allium species, indicating that the transition from cis- to trans-splicing of cox2 might occur in a common ancestor of all tested Allium species. The breakpoints of group II intron of all tested Allium species were, as expected, found in domain IV of self-splicing cox2 introns. Meanwhile, cis-splicing of cox2 gene was observed in five Allium-related species belonging to the same order, family, or subfamily as Allium. A chimeric gene, orf725, present in CMS-S and CMS-T cytotypes causing male-sterility in onion was identified only in A. roylei, suggesting a very recent occurrence of the orf725 gene in a common ancestor of onions and closely related species. In addition, five completely different mtDNA organizations linked to the partial atp9 sequences were identified from analyzed Allium species, showing that the atp9 gene might be a hotspot for mtDNA rearrangement in Allium species. The integration of the partial chloroplast gene ycf2 was detected in 11 Allium species including onion CMS-S cytotype, implying that ycf2 integration might occur in a common ancestor of 11 related Allium species, but that mtDNA organization containing the ycf2 integration might disappear via substoichiometric shifting in the normal onion cytotype.