Abstract
SummaryMitochondria 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.
Highlights
Mitochondria are key organelles in eukaryotic cells
Plant mitochondria usually exist as separate discrete entities, presumably more resembling their alphaproteobacterium-like ancestors (Logan, 2010b). Exceptions to this rule do exist, such as in the cage-like mitochondrial formation observed in mitosis of shoot apical meristem cells (Seguı-Simarro et al, 2008), but generally, the mitochondrial population consists of dynamic, fragmented individuals, with transient fission and fusion events (Logan, 2010a)
The mitochondria captured within each video were tracked and quantified using TrackMate (Tinevez et al, 2017), building a set of manually verified physical trajectories over time (Figure 1B)
Summary
Mitochondria are key organelles in eukaryotic cells. They typically produce the majority of cellular ATP, the energy currency of the cell, and are involved in many other metabolic pathways as well as stress responses and cell death (Yoshinaga et al, 2005; Jacoby et al, 2012; Wang et al, 2018). Plant mitochondria usually exist as separate discrete entities, presumably more resembling their alphaproteobacterium-like ancestors (Logan, 2010b) Exceptions to this rule do exist, such as in the cage-like mitochondrial formation observed in mitosis of shoot apical meristem cells (Seguı-Simarro et al, 2008), but generally, the mitochondrial population consists of dynamic, fragmented individuals, with transient fission and fusion events (Logan, 2010a). These events have been likened to kiss-and-run dynamics seen in bacterial cells (Liu et al, 2009)
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