Temporal Regulation of the Metabolome and Proteome in Photosynthetic and Photorespiratory Pathways Contributes to Maize Heterosis.

Heterosis or hybrid vigor is widespread in plants and animals. Despite the molecular basis for heterosis has been extensively studied, metabolic and proteomic contributions to heterosis remain elusive. Here we report integrative analysis of time-series metabolome and proteome data in maize hybrids and their inbred parents. A large fraction of maize metabolites and proteins is diurnally regulated, many of which show nonadditive abundance in the hybrids, including key enzymes and metabolites involved in carbon assimilation. Compared with high levels of trait heterosis, metabolic heterosis is relatively mild. Interestingly, most amino acids display negative mid-parent heterosis (MPH), while metabolites in sugars, alcohols and nucleosides show positive MPH. From the network perspectives, metabolites in the photosynthetic pathway show positive MPH, whereas metabolites in the photorespiratory pathway show negative MPH, which correspond to nonadditive protein abundance and enzyme activities of key enzymes in the respective pathways in the hybrids. Moreover, rhythmic proteins that are upregulated in the hybrids are enriched in photosynthetic related Gene Ontology terms. Hybrids may more effectively remove toxic metabolites generated during photorespiration, and thus maintain higher photosynthetic efficiency. These metabolic and proteomic results provide novel insights into heterosis and its utilization for high yielding maize and other crop plants.