Dynamic changes to the plastoglobule lipidome and proteome in maize over a dehydration–rehydration cycle

Drought represents one of the most severe challenges faced by agriculture and leveraging resources to promote crop resilience is critical. The plastoglobule lipid droplets of chloroplasts, present in all photosynthetic eukaryotes, are suggested to be a major orchestrator of adaptive responses to environmental perturbations, thus representing a potentially significant, untapped target for enhancement of crop resilience. Yet, the functions of plastoglobules are unclear and their molecular composition is incompletely described. Here, we provide a thorough investigation of the protein and lipid compositions of plastoglobules and thylakoids at six time-points over the course of a water-deficit and recovery treatment in B73 inbred maize. Our results establish the prominent components of the plastoglobule polar lipid surface and neutral lipid interior in an important crop species, including the presence of mono- and di-galactosyl diacylglycerol lipids enriched in saturated acyl groups, and the prevalence of various triacylglycerols and plastoquinone-9 derivatives. Quantitative proteomics identifies prominent Fibrillins and Activity of bc1 Complex Kinases at the plastoglobule as well as many proteins with known or putative roles in prenyl-lipid and redox metabolism. A remarkably high proportion of the Fibrillin 4 on the plastoglobules coincided with a preponderance of plastoquinone-9, supporting a role for Fibrillin 4 in plastoquinone accumulation at plastoglobules. Collectively, our results provide a solid foundation for the study of plastoglobules in crop plants.