High-frequency biparental inheritance of plant mitochondria upon chilling stress and loss of a genome-degrading nuclease

Mitochondria are inherited maternally in the vast majority of eukaryotes. Occasional transmission of paternal mitochondria (paternal leakage) can lead to heterochondriomy and recombination between maternal and paternal mitochondrial genomes. Despite its potential physiological and evolutionary consequences, the extent of paternal leakage and the cellular processes governing mitochondrial inheritance remain largely unknown. Here we have established a robust genetic screen to detect paternal mitochondrial inheritance in tobacco (Nicotiana tabacum). Our data reveal an unexpectedly high paternal transmission frequency of 0.18%, which increased markedly to 7.34% when the organellar exonuclease DPD1 was disrupted and pollen development occurred at low temperature. Notably, paternally transmitted mitochondria restored growth, development and male fertility in progeny that inherited dysfunctional mitochondria from the maternal parent. Together, our findings uncover molecular mechanisms underlying maternal mitochondrial inheritance, and highlight the potential of biparental transmission to rescue mitochondrial function and generate novel mitochondrial genotypes through recombination.