Multi-omics analysis reveals distinct responses to light stress in photosynthesis and primary metabolism between maize and rice.

Abstract

High-light (HL) stress is a major environmental factor that limits crop productivity. Maize (Zea mays) and rice (Oryza sativa), two key global crops, can both grow under HL intensities but differ in photosynthetic metabolism; maize is a C₄ species, whereas rice is a C₃ species. However, the molecular mechanisms underlying their responses to HL stress remain poorly understood. To systematically dissect how HL affects maize and rice growth, we conducted time-resolved multi-omics analyses, examining the transcriptome, translatome, proteome, and metabolome in response to HL treatment. Integration of this multi-omics approach with physiological analyses revealed that rice exhibits a more rapid response to HL stress than maize, with significant alterations in photosynthetic electron transport, energy dissipation, reactive oxygen species (ROS) accumulation, and primary metabolism. In contrast, the higher tolerance of maize to HL stress is primarily attributed to increased cyclic electron flow (CEF) and non-photochemical quenching (NPQ), elevated sugar and aromatic amino acid accumulation, and enhanced antioxidant activity during 4 h of HL exposure. Transgenic experiments further validated key regulators of HL tolerance; for instance, knockout of OsbZIP18 enhanced HL tolerance in rice, whereas overexpression of ZmPsbS in maize significantly boosted photosynthesis and energy-dependent quenching (qE) after 4 h of HL treatment, underscoring its role in protecting C₄ crops from HL-induced photodamage. Taken together, these findings provide new insights into the molecular mechanisms of HL stress tolerance in C₄ versus C₃ species and highlight a set of candidate genes for engineering improved HL tolerance in crops.