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Cold stress is a major environmental factor that detrimentally affects plant growth and development. Melatonin has been shown to confer plant tolerance to cold stress through activating the C-REPEAT BINDING FACTOR (CBF) pathway; however, the underlying modes that enable this function remain obscure. In this study, we investigated the role of H 2 O 2 and Ca 2+ signaling in the melatonin-induced CBF pathway and cold tolerance in watermelon ( Citrullus lanatus L.) through pharmacological, physiological, and genetic approaches. According to the results, melatonin induced H 2 O 2 accumulation, which was associated with the upregulation of respiratory burst oxidase homolog D ( ClRBOHD ) during the early response to cold stress in watermelon. Besides, melatonin and H 2 O 2 induced the accumulation of cytoplasmic free Ca 2+ ([Ca 2+ ] cyt ) in response to cold. This was associated with the upregulation of cyclic nucleotide-gated ion channel 2 ( ClCNGC2 ) in watermelon. However, blocking of Ca 2+ influx channels abolished melatonin- or H 2 O 2 -induced CBF pathway and cold tolerance. Ca 2+ also induced ClRBOHD expression and H 2 O 2 accumulation in early response to cold stress in watermelon. Inhibition of H 2 O 2 production in watermelon by RBOH inhibitor or in Arabidopsis by AtRBOHD knockout compromised melatonin-induced [Ca 2+ ] cyt accumulation and melatonin- or Ca 2+ -induced CBF pathway and cold tolerance. Overall, these findings indicate that melatonin induces RBOHD -dependent H 2 O 2 generation in early response to cold stress. Increased H 2 O 2 promotes [Ca 2+ ] cyt accumulation, which in turn induces H 2 O 2 accumulation via RBOHD , forming a reciprocal positive-regulatory loop that mediates melatonin-induced CBF pathway and subsequent cold tolerance.

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)