Supplementing the Nuclear-Encoded PSII Subunit D1 Induces Dramatic Metabolic Reprogramming in Flag Leaves during Grain Filling in Rice

Our previous study has demonstrated that the nuclear-origin supplementation of the PSII core subunit D1 protein stimulates growth and increases grain yields in transgenic rice plants by enhancing photosynthetic efficiency. In this study, the underlying mechanisms have been explored regarding how the enhanced photosynthetic capacity affects metabolic activities in the transgenic plants of rice harboring the integrated transgene RbcS(PTP)-OspsbA cDNA, cloned from rice, under control of the AtHsfA2 promoter and N-terminal fused with the plastid-transit peptide sequence (PTP) cloned from the AtRbcS. Here, a comparative metabolomic analysis was performed using LC-MS in flag leaves of the transgenic rice plants during the grain-filling stage. Critically, the dramatic reduction in the quantities of nucleotides and certain free amino acids was detected, suggesting that the increased photosynthetic assimilation and grain yield in the transgenic plants correlates with the reduced contents of free nucleotides and the amino acids such as glutamine and glutamic acid, which are cellular nitrogen sources. These results suggest that enhanced photosynthesis needs consuming more free nucleotides and nitrogen sources to support the increase in biomass and yields, as exhibited in transgenic rice plants. Unexpectedly, dramatic changes were measured in the contents of flavonoids in the flag leaves, suggesting that a tight and coordinated relationship exists between increasing photosynthetic assimilation and flavonoid biosynthesis. Consistent with the enhanced photosynthetic efficiency, the substantial increase was measured in the content of starch, which is the primary product of the Calvin–Benson cycle, in the transgenic rice plants under field growth conditions.