A proteomic approach identifies novel proteins and metabolites for lesion mimic formation and disease resistance enhancement in rice

•The mutated OsCUL3a can cause cell death related lesion mimic formation with dynamic chloroplast degradation and signal molecule SA and H2O2 accumulation in different leaf positions.•Proteomic approach identified differentially expressed proteins that mainly located in the chloroplast and cytoplasm, with enhanced lipid metabolism, but suppressed carbon/nitrogen metabolism.•Some new identified natural chemicals in secondary metabolic pathways can be used for disease control in crop plants. Lesion mimic mutants are ideal genetic materials to study programmed cell death and defense signaling in plants. However, the molecular basis of lesion mimic formation remains largely unknown. Here, we first used a proteomic approach to identify differentially expressed proteins during dynamic lesion mimic formation in the rice oscul3a mutant, then electron microscope observation and physiological assays were used to analyze the mutant. The oscul3a mutant had disrupted cell metabolism balance, and the identified differentially expressed proteins were mainly located in the chloroplast and cytoplasm, which caused enhanced lipid metabolism, but suppressed carbon/nitrogen metabolism with reduced growth and grain quality. The oscul3a mutant had higher salicylic acid (SA) concentration in leaves, and H2O2 was shown to accumulate late in the formation of lesions. The secondary metabolite coumarin induced reactive oxygen species (ROS) and had rice blast resistance activity. Moreover, the cell death initiated lesion mimic formation of oscul3a mutant was light-sensitive, which might be associated with metabolite biosynthesis and accumulation. This study sheds light on the metabolic transition associated with cell death and defense response, which is under tight regulation by OsCUL3a and metabolism-related proteins, and the newly identified chemicals in the secondary metabolic pathway can potentially be used to control disease in crop plants.