Rare maternal and biparental transmission of the cucumber mitochondrial DNA reveals sorting of polymorphisms among progenies.

key messageWe used a mitochondrial (mt) mutant of cucumber to document rare maternal transmission of mt polymorphisms and demonstrate that polymorphisms can become more prevalent and sort to progenies to increase mt DNA diversity. The mitochondrial (mt) DNAs of most angiosperms show maternal inheritance, although relatively rare biparental or paternal transmission has been documented. The mt DNAs of plants in the genus Cucumis (family Cucurbitaceae) are paternally transmitted in intra- and interspecific crosses. MSC16 is an inbred line of cucumber (Cucumis sativus) with a mitochondrially associated mosaic (MSC) phenotype. MSC16 was crossed as the male parent to wild-type cultivar Calypso, and hybrid progenies were evaluated for the wild-type phenotype in order to screen for rare maternal or biparental transmission of the mt DNA. We then used standard and droplet digital (dd) PCR to study the transmission of polymorphic mt markers across three generations. We observed evidence for occasional maternal and biparental transmission of the mt DNA in cucumber. The transmission of specific regions of the maternal mt DNA could be as high as 17.8%, although the amounts of these maternal regions were often much lower relative to paternally transmitted regions. Different combinations of maternal and paternal mt polymorphisms were detected in progenies across generations, indicating that relatively rare maternal regions can be transmitted to progenies and become predominant to increase mt DNA diversity over generations.