Stochastic organelle genome segregation through Arabidopsis development and reproduction

Abstract

Organelle DNA (oDNA) in mitochondria and plastids is vital for plant (and eukaryotic) life. Selection against damaged oDNA is mediated in part by segregation – sorting different oDNA types into different cells in the germline. Plants segregate oDNA very rapidly, with oDNA recombination protein MSH1 a key driver of this segregation, but we have limited knowledge of the dynamics of this segregation within plants and between generations. Here, we reveal how oDNA evolves through Arabidopsis thaliana development and reproduction. We combine stochastic modelling, Bayesian inference, and model selection with new and existing tissue-specific oDNA measurements from heteroplasmic Arabidopsis plant lines through development and between generations. Segregation proceeds gradually but continually during plant development, with a more rapid increase between inflorescence formation and the next generation. When MSH1 is compromised, the majority of observed segregation can be achieved through partitioning at cell divisions. When MSH1 is functional, mtDNA segregation is far more rapid; we show that increased oDNA gene conversion is a plausible mechanism quantitatively explaining this acceleration. These findings reveal the quantitative, time-dependent details of oDNA segregation in Arabidopsis. We also discuss the support for different models of the plant germline provided by these observations.