Stochastic organelle genome segregation through Arabidopsis development and reproduction

Abstract

Summary 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.

Arabidopsis GENOMES UNCOUPLED PROTEIN1 binds to plastid RNAs and promotes their maturation

“…In addition, GUN1 protein accumulates at early stages of cotyledon development, and the timing of gene expression during development is known to influence penetrance (40). However, further analysis is needed and may include how stochastic factors – such as segregation of organelle genomes through development and reproduction (45) - in conjunction with environmental factors and transgenerational effects contribute to the development of individual phenotypes (46).…”

Heteroplasmy is rare in plant mitochondria compared to plastids despite similar mutation rates

“…Notably, the effect of drift and selection at multiple levels of organization has been recognized in other extrachromosomal genetic elements (ECEs), e.g., prokaryotic plasmids (Ilhan et al 2019). Indeed, efforts to model ECE dynamics and evolution typically encounter similar challenges (e.g., Hunter and Fusco 2022;Santer et al 2022;Broz et al 2023).…”

“…Here we assume that the considered neutral genome loci are independent and the de novo mutations occur only during the homoplasmic oDNA population state; this assumption is supported by the low mutation rates observed here. Additionally, we assume that the tissue sample is formed of one stem cell descendant and, thus, has the same frequency of the mutant allele as the stem cell itself regardless of the mutant copy distribution among cells (similar to recently published simulations by Broz et al 2023). We also assume no de novo mutations during tissue formation since the probability for such mutations to arise and reach the detectable AF is low.…”

Optimal organelle inheritance strategies under different changing environments and mutational pressures

“…Inheritance of mtDNA and chloroplast DNA (cpDNA, also called ptDNA for plastid DNA) in plants and algae is often maternal but sometimes paternal (Fauré et al, 1994;Greiner et al, 2015;Munasinghe & Ågren, 2023), and often involves leakage from the other parent (Breton & Stewart, 2015;McCauley, 2013). Plants show a dramatic amount of recombination in organelle DNA, involving templated repair and gene conversion processes (Broz et al, 2022(Broz et al, , 2024Khakhlova & Bock, 2006;Wu et al, 2020;Zwonitzer et al, 2024). Fungi and protists also use oDNA recombination (Barr et al, 2005), and diKerent lineages show diKerent modes of inheritance, including biparental inheritance (Birky, 2001), leakage (Wilson & Xu, 2012;Xu & Li, 2015) and even inheritance of mtDNA independently of either nuclear parent (three-parent oKspring (Bloomfield et al, 2019)).…”

“…A genetic bottleneck, manifest through a physical reduction in mtDNA copy number and parallel stochastic processes, is used to segregate mutational damage between oKspring in animals (Johnston, 2019b). Plants also induce a genetic bottleneck, likely using a mechanism involving gene conversion and more limited physical reduction (Broz et al, 2022(Broz et al, , 2024Edwards et al, 2021). The inheritance of mtDNA in animals involves purifying selection (Fan et al, 2008;Lieber et al, 2019;Palozzi et al, 2022;Stewart et al, 2008), which is itself dependent on environmental cues (Latorre-Pellicer et al, 2019).…”