Collective mitochondrial dynamics resolve conflicting cellular tensions: From plants to general principles

Abstract

Mitochondria play diverse and essential roles in eukaryotic cells, and plants are no exception. Plant mitochondria have several differences from their metazoan and fungal cousins: they often exist in a fragmented state, move rapidly on actin rather than microtubules, have many plant-specific metabolic features and roles, and usually contain only a subset of the complete mtDNA genome, which itself undergoes frequent recombination. This arrangement means that exchange and complementation is essential for plant mitochondria, and recent work has begun to reveal how their collective dynamics and resultant “social networks” of encounters support this exchange, connecting plant mitochondria in time rather than in space. This review will argue that this social network perspective can be extended to a “societal network”, where mitochondrial dynamics are an essential part of the interacting cellular society of organelles and biomolecules. Evidence is emerging that mitochondrial dynamics allow optimal resolutions to competing cellular priorities; we will survey this evidence and review potential future research directions, highlighting that plant mitochondria can help reveal and test principles that apply across other kingdoms of life. In parallel with this fundamental cell biology, we also highlight the translational “One Health” importance of plant mitochondrial behaviour – which is exploited in the production of a vast amount of crops consumed worldwide – and the potential for multi-objective optimisation to understand and rationally re-engineer the evolved resolutions to these tensions.