Intracellular Ca2+ accumulation triggered by caffeine provokes resistance against a broad range of biotic stress in rice

Chemical pesticides are still frequently overused to diminish such crop loss caused by biotic stress despite the threat to humans and the environment. Thus, it is urgent to find safer and more effective defense strategies. In this study, we report that caffeine, implanted through a transgenic approach, enhances resistance against variable biotic stresses in rice without fitness cost. Caffeine‐producing rice (CPR) was generated by introducing three N‐methyltransferase genes involved in the biosynthesis of caffeine in coffee plants. The CPR plants have no differences in morphology and growth compared to their wild‐type counterparts, but they show strongly enhanced resistance to both bacterial leaf blight, rice blast, and attack of white‐backed planthoppers. Caffeine acts as a repellent agent against rice pathogens. Moreover, caffeine triggers a series of Ca2+ signalling‐like processes to synthesize salicylic acid (SA), a hormone associated with plant resistance. In CPR, phosphodiesterase was inhibited by caffeine, cAMP and cGMP increased, intracellular Ca2+ increased, phenylalanine lyase (PAL) was activated by OsCPK1, and SA synthesis was activated. This finding is a novel strategy to improve resistance against the biotic stresses of crops with a special type of defense inducer. Summary statement In the present study, we report a broad range of resistance of transgenic rice against variable biotic stresses caused by Xanthomonas oryzae, Magnaporthe oryzae and white‐backed planthopper. The transgenic rice produces caffeine and shows evidence that Ca2+ signalling triggered by the produced caffeine plays a key role in the versatile resistance without fitness costs. This finding provides a breakthrough in the development and cultivation of stress‐resistant crops using caffeine as a novel type of defense inducer agent.