Photosynthetic and Transcriptional Regulation Reveals Divergent Mechanisms of Active Adaptation in C4 Maize and Passive Regulation in C3 Rice Under Long-Term Fluctuating Light

Fluctuating light is a key factor limiting crop photosynthetic efficiency, with C₄ maize (Zea mays) and C₃ rice (Oryza sativa) crops exhibiting distinct acclimation responses. However, the systemic differences in physiological and transcriptional regulatory mechanisms between C₃ and C₄ crops under long-term fluctuating light remain poorly understood. Herein, maize variety “Yunrui 408” and rice variety “Dianheyou 615,” both widely cultivated in Southwest China, were used to investigate responses to long-term fluctuating light (FL) versus steady light (SL) via integrated analyses of phenotypic traits, photosynthetic physiology, transcriptomics, and protein–protein interaction (PPI) networks. Results showed that long-term FL causes greater yield losses (> 30%) in rice, including reduced 100-grain weight and shoot dry weight, whereas maize exhibited milder yield suppression (< 20%) and enhanced starch/sucrose accumulation in grains and leaves. Maize maintained stable photosystem function via a synergistic mechanism. A large plastoquinone (PQ) pool buffered electron transport fluctuations, while the transcription factor ZmMYB93 coordinated the upregulation of carbon storage (ZmAGPS1), energy supply (ZmGAPC3), and carbon assimilation (ZmFBA3) pathways to sustain metabolic homeostasis. In contrast, rice showed decreased photosynthesis under long-term FL, characterized by downregulated core photosynthetic genes (OsPsaA, OsPsbA) and ATP synthase genes (OsAtpB). This suppression was driven by the PEL-GLK inhibitory module; subcellular localization assays confirmed that OsPEL1 is a nuclear-resident protein that physically interacts with GLK transcription factors within the nucleus to repress the transcriptional activation of core photosynthetic genes. Rice also relied on passive cyclic electron flow (CEF) and exhibited increased dark respiration, forming a negative feedback loop that impaired carbon assimilation. Overall, C₄ crop maize exhibits stronger adaptability to long-term FL than C₃ crop rice. It adopts an active adaptation strategy by integrating PQ pool-mediated electron transport buffering and ZmMYB93-coordinated nuclear transcriptional regulation. In contrast, rice adopts a passive and inefficient regulatory strategy, where OsPEL1-mediated nuclear inhibition of GLK and enhanced dark respiration lead to photosynthetic apparatus damage and carbon assimilation suppression, ultimately resulting in severe yield loss. These findings provide a blueprint for improving C₃ crop light-use efficiency by leveraging the active regulatory mechanisms identified in maize to mitigate yield losses in dynamic field environments.