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

Mitochondria in plant cells exist largely as individual organelles which move, colocalize, and interact, but the cellular priorities addressed by these dynamics remain incompletely understood. Here, we elucidate these principles by studying the dynamic "social networks" of mitochondria in Arabidopsis thaliana wildtype and mutants, describing the colocalization of individuals over time. We combine single-cell live imaging of hypocotyl mitochondrial dynamics with individual-based modeling and network analysis. We identify an inevitable tradeoff between mitochondrial physical priorities (an even cellular distribution of mitochondria) and "social" priorities (individuals interacting, to facilitate the exchange of chemicals and information). This tradeoff results in a tension between maintaining mitochondrial spacing and facilitating colocalization. We find that plant cells resolve this tension to favor efficient networks with high potential for exchanging contents. We suggest that this combination of physical modeling coupled to experimental data through network analysis can shed light on the fundamental principles underlying these complex organelle dynamics. A record of this paper's transparent peer review process is included in the supplemental information.