Drought stress is a major agricultural problem restricting the growth, development, and productivity of plants. Calcineurin B-like proteins (CBLs) and CBL-interacting protein kinases (CIPKs) significantly influence the plant response to different stresses. However, the molecular mechanisms of CBL–CIPK in the drought stress response of pepper are still unknown. Here, the function of CaCIPK3 in the regulation of drought stress in pepper (Capsicum annuum L.) was explored. Transcriptomic data and quantitative real-time PCR (qRT-PCR) analysis revealed that CaCIPK3 participates in the response to multiple stresses. Knockdown of CaCIPK3 in pepper increased the sensitivity to mannitol and methyl jasmonate (MeJA). Transient overexpression of CaCIPK3 improved drought tolerance by enhancing the activities of the antioxidant system and positively regulating jasmonate (JA)-related genes. Ectopic expression of CaCIPK3 in tomato also improved drought and MeJA resistance. As the CaCIPK3-interacting partner, CaCBL2 positively influenced drought resistance. Additionally, CaWRKY1 and CaWRKY41 directly bound the CaCIPK3 promoter to influence its expression. This study shows that CaCIPK3 acts as a positive regulator in drought stress resistance via the CBL–CIPK network to regulate MeJA signaling and the antioxidant defense system.

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