Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity

Abstract

Network analysis of Arabidopsis mitochondrial dynamics reveals a resolved tradeoff between physical distribution and social connectivity Graphical abstract Highlights d Dynamic social networks of plant mitochondria reflect physical organellar encounters d Network analysis and modeling show priorities and tradeoffs for mitochondrial motion d Mitochondria in plant cells trade off physical spacing against social connectivity d Plant cells favor efficient networks with high potential for information exchange

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

“…Following the creation of mtGFP-msh1, we used confocal microscopy to characterise mitochondrial dynamics in single hypocotyl cells of 4-5 day seedlings in this mutant, and compared these dynamics to the mtGFP transgenic line, representing wildtype mitochondrial motion. This imaging approach followed the protocol from (Chustecki et al, 2021). Briefly, we recorded timelapse videos of mitochondrial motion in single cells, and computationally identified trajectories of individual mitochondria using TrackMate (Tinevez et al, 2017).…”

“…Briefly, we recorded timelapse videos of mitochondrial motion in single cells, and computationally identified trajectories of individual mitochondria using TrackMate (Tinevez et al, 2017). From these trajectories we can analyse individual and collective behaviour of mitochondria, including speeds, colocalisations, and many more statistics (Chustecki et al, 2021). Fig.…”

“…4). Akin to social networks, describing social interactions between individuals in a population, these encounter networks shape the potential for exchange of contents across the mitochondrial population (Chustecki et al, 2021). Salient features of these encounter networks for collective mitochondrial behaviour are the degree distribution (the number of different mitochondria each mitochondrion encounters); the diameter of the network (the length in edges of the longest direct route across the network) and the network efficiency.…”

“…Recent work suggested that the collective cellular dynamics of plant mitochondria can resolve a tension between mitochondrial proximity and spacing (Chustecki et al, 2021).…”

“…The mitochondrial population thus faces a hypothesised tension between maintaining even spacing of mitochondria and supporting inter-mitochondrial encounters. Chustecki et al (2021) explored this tradeoff between even spacing and supporting encounters by characterising the 'social networks' of the dynamic cellular population, allowing the characterisation of connectivity across the chondriome --the whole population of mitochondria in a cell (Logan, 2010). Physical and network analysis revealed that wildtype Arabidopsis uses mitochondrial dynamics to resolve this tension, with mitochondrial motion allowing transient encounters between organelles --and facilitating efficient exchange through the population --while also retaining physical spacing.…”