Stromule Geometry Allows Optimal Spatial Regulation of Organelle Interactions in the Quasi-2D Cytoplasm

Abstract

In plant cells, plastids form elongated extensions called stromules, the regulation and purposes of which remain unclear. Here, we quantitatively explore how different stromule structures serve to enhance the ability of a plastid to interact with other organelles: increasing the effective space for interaction and biomolecular exchange between organelles. Interestingly, electron microscopy and confocal imaging showed that the cytoplasm in Arabidopsis thaliana and Nicotiana benthamiana epidermal cells is extremely thin (around 100 nm in regions without organelles), meaning that inter-organelle interactions effectively take place in 2D. We combine these imaging modalities with mathematical modelling and new in planta experiments to demonstrate how different stromule varieties (single or multiple, linear or branching) could be employed to optimise different aspects of inter-organelle interaction capacity in this 2D space. We found that stromule formation and branching provide a proportionally higher benefit to interaction capacity in 2D than in 3D. Additionally, this benefit depends on optimal plastid spacing. We hypothesize that cells can promote the formation of different stromule architectures in the quasi-2D cytoplasm to optimise their interaction interface to meet specific requirements. These results provide new insight into the mechanisms underlying the transition from low to high stromule numbers, the consequences for interaction with smaller organelles, how plastid access and plastid to nucleus signaling are balanced, as well as the impact of plastid density on organelle interaction.

Macromolecular Crowding, Phase Separation, and Homeostasis in the Orchestration of Bacterial Cellular Functions

“…For example, the two most common model systems to represent prokaryotes and eukaryotes, E. coli and HeLa cells, differ significantly in size, but some plant cells have a cytosol that is only 100 nm in diameter, as the vacuole takes up most of the cytoplasm. 256 This cytosol is almost 10 times smaller than the diameter of E. coli, and hence more similar to those of Pelagibacter species, which is one of the smallest (and most abundant) bacterial species on Earth. Eukaryotic organelles such as the endoplasmic reticulum (ER) and mitochondria have dimensions similar to bacteria, but there is a tremendous diversity among organelles depending on cell function.…”

“…Prokaryotes and eukaryotes are enormously diverse, and comparison based on model systems can become anecdotal. For example, the two most common model systems to represent prokaryotes and eukaryotes, E. coli and HeLa cells, differ significantly in size, but some plant cells have a cytosol that is only 100 nm in diameter, as the vacuole takes up most of the cytoplasm . This cytosol is almost 10 times smaller than the diameter of E. coli , and hence more similar to those of Pelagibacter species, which is one of the smallest (and most abundant) bacterial species on Earth.…”