Metabolic compartmentation of maize endosperm for efficient synthesis and storage of carbon and nitrogen assimilates

Carbon and nitrogen metabolism underpin the development and assimilate storage of the endosperm, with spatiotemporal nonuniformities exemplified by a basipetal movement of the milk line from the apical to the basal end within maize grain. However, the metabolic characteristics and implications of this nonuniformity remain unclear. This study combined transcriptomics, metabolomics, enzyme activity analyses, and ¹⁵N tracing to investigate the compartmentation of carbon and nitrogen metabolism during maize endosperm development. The basal endosperm (BE) exhibited distinct metabolic features, with consistently higher activities in sucrose synthesis, amino acids transamination, glycolysis, and the tricarboxylic acid cycle, compared to the upper regions of the endosperm. This unique characteristic of BE supports its function in supplying raw materials for efficient synthesis and storage of assimilates with a basipetal pattern in the endosperm. Interestingly, water-deficit suppressed the metabolic activity in the BE but enhanced the assimilation in the upper endosperm and the overall protein : starch ratio, revealing the spatial differences and the importance of metabolic compartmentation in determining endosperm quality in response to environmental stimulus. Collectively, these findings emphasize the basipetal pattern in coordinating metabolic networks for efficient carbon and nitrogen assimilation and the quality determination of the endosperm.