Altered collective mitochondrial dynamics in an Arabidopsis msh1 mutant compromising organelle DNA maintenance

Abstract

Mitochondria form highly dynamic populations in the cells of plants (and all eukaryotes). The characteristics of this collective behaviour, and how it is influenced by nuclear features, remain to be fully elucidated. Here, we use a recently-developed quantitative approach to reveal and analyse the physical and collective "social" dynamics of mitochondria in an Arabidopsis msh1 mutant where organelle DNA maintenance machinery is compromised. We use a newly-created line combining the msh1 mutant with mitochondrially-targeted GFP, and characterise mitochondrial dynamics with a combination of single-cell timelapse microscopy, computational tracking and network analysis. The collective physical behaviour of msh1 mitochondria is altered from wildtype in several ways: mitochondria become less evenly spread, and networks of inter-mitochondrial encounters become more connected with greater potential efficiency for inter-organelle exchange. We find that these changes are similar to those observed in friendly, where mitochondrial dynamics are altered by a physical perturbation, suggesting that this shift to higher connectivity may reflect a general response to mitochondrial challenges.

Sorting of mitochondrial and plastid heteroplasmy in Arabidopsis is extremely rapid and depends on MSH1 activity

“…Another way in which MSH1 could alter sorting dynamics is through changing the physical interactions and fusion events between mitochondria. Hypocotyl cells of msh1 mutants show increased mitochondrial connectivity over wild type ( 85 ), suggesting an increased capacity for genome mixing and homogenization. Under existing models ( 14 , 37 ), increased rates of fusion are predicted to accelerate mitochondrial sorting, the opposite of what we see in msh1 mutants.…”

Exchange on dynamic encounter networks allows plant mitochondria to collect complete sets of mitochondrial DNA products despite their incomplete genomes

“…The previous research presenting plant mitochondrial encounter networks (Chustecki, 2021a;2021b) hypothesised that the collective dynamics of plant mitochondria allow the cell to balance two priorities. The first is an even physical distribution of mitochondria, ensuring a uniform energy supply, potential for colocalisation with other organelles throughout the cell, and avoiding heterogeneity in concentration of metabolites and signalling molecules.…”

“…Recent work has characterised the 'encounter networks' between mitochondria in plant cells, describing which mitochondria encounter which others over time (Chustecki, 2021a;2021b). Here, mitochondria are nodes, with two nodes linked by an edge if the corresponding mitochondria have been recorded within a threshold distance.…”

“…Here, mitochondria are nodes, with two nodes linked by an edge if the corresponding mitochondria have been recorded within a threshold distance. Chustecki et al showed that these encounter networks have structures which have the potential to facilitate efficient exchange of content, while also allowing mitochondria to spread evenly through the cell (Chustecki 2021b), and to adapt in the face of challenges (Chustecki 2021a). Hence, mitochondrial dynamics have the potential to resolve a tension between competing cell priorities: even spacing of mitochondria (with metabolic and energetic advantages) and colocalisation of mitochondria (for beneficial exchange of contents).…”