PERSPECTIVE: organelle positioning as a principle of metabolic regulation and stress tolerance

Plants have evolved elaborate acclimation strategies to withstand adverse environments, involving all levels of their function and organization. While macroscopic movements through differential growth that enable the physical re-shaping and -positioning of organs have been a major field of study, the highly active dynamics of cell organelles within the immobile plant cell hold major unresolved questions. Here, we argue that the precise positioning of cell organelles is not only critical for cell division and development but also represents a fundamental principle in regulating cellular metabolism and underpinning effective responses to biotic and abiotic stresses. Although the positioning of individual organelles, such as nuclei and chloroplasts, and probably to a lesser extent, mitochondria, peroxisomes, endoplasmic reticulum tubules, Golgi bodies, and lipid droplets, is clearly controlled by developmental and environmental stimuli, the underlying mechanisms and functional significance remain unclear in many instances. We discuss steps required to improve our understanding of how intracellular positioning of organelles in general, and of chloroplasts and mitochondria in particular, contributes to metabolic regulation. Drawing on the recent discovery that three glycolytic enzymes can physically tether mitochondria and chloroplasts, we highlight approaches and concepts to establish how the spatial arrangement of organelles relative to one another underpins regulation of metabolism and stress responses.