The mitochondrial orf125 affects male fertility of Solanum tuberosum (+) S. commersonii somatic hybrids and participates in the onset of “Tuberosum”-Type CMS and evolution of common potato

Cytoplasmic male sterility (CMS) is an agronomically significant trait and a powerful tool to study interactions between nuclear and cytoplasmic genomes. In this study, the chondriomes of two isonuclear male-fertile and sterile somatic hybrids (SH9A and SH9B, respectively) between the common potato ( Solanum tuberosum Group Tuberosum , tbr ) and the wild species S. commersonii ( cmm ), were sequenced and compared to those of parental species to identify mitochondrial genes involved in the expression of male sterility. A putative novel gene ( orf125 ) was found only in tbr and in male-sterile hybrids. Two approaches, a physical or functional deletion of orf125 by mtDNA editing in SH9B and its allotopic expression in SH9A, clearly demonstrate that orf125 affects male fertility. To trace the origin of orf125 and hypothesize its role in the evolution of common potato, we searched it in tbr varieties, tuber-bearing potato relatives and other Solanaceae. The organization of the mitochondrial genome region implicated in CMS remained consistent across all common potato accessions in GenBank. An identical tbr copy of orf125 was also detected in all six accessions belonging to the S. berthaultii complex ( ber ) analyzed. Such findings corroborate the hypothesis that ber accessions with T/β cytoplasm crossed as female with Andean potato ( S. tuberosum Group Andigenum , adg ), giving rise to the differentiation of the Chilean potato ( S. tuberosum Group Chilotanum ), and highlights the origin of mitochondrial factors contributing to genic-cytoplasmic male sterility in tbr x adg (or some wild species) hybrids.