Dynamics of organelle DNA segregation in Arabidopsis development and reproduction revealed with tissue-specific heteroplasmy profiling and stochastic modelling

Organelle DNA (oDNA) in mitochondria and plastids is vital for plant (and eukaryotic) life. Selection against damaged oDNA is mediated in part by segregation - the sorting of different oDNA types into different cells in the germline. Plants segregate oDNA very rapidly, with oDNA recombination protein MutS Homolog 1 (MSH1), a key driver of this segregation, but in contrast to mammals, we have very limited knowledge of the dynamics of this segregation within plants and between generations. Here, we combine stochastic modelling with tissue-specific heteroplasmy measurements to reveal the trajectories of oDNA segregation in Arabidopsis thaliana development and reproduction. We obtain and use new experimental observations of oDNA through development to confirm and refine the predictions of the theory inferred from existing measurements. Ongoing segregation proceeds gradually but continually during plant development, with a more rapid increase between inflorescence formation and the establishment of the next generation. When MSH1 is compromised, we show that the majority of observed segregation could be achieved through partitioning at cell divisions. When MSH1 is functional, mtDNA segregation is far more rapid than can be achieved through cell divisions; we show that increased oDNA gene conversion is a plausible mechanism quantitatively explaining this acceleration. We also discuss the support for different models of the plant germline provided by these observations.