Positive interaction between melatonin and methyl jasmonate enhances Fusarium wilt resistance in Citrullus lanatus

<i>Fusarium</i> wilt, caused by the soil-borne fungal pathogen <i>Fusarium oxysporum</i> (Fo), is widely recognized as one of the most devastating fungal diseases, inflicting significant damage on a wide range of agricultural and horticultural crops. Despite melatonin has recently emerged as a potential enhancer of plant resistance against Fo, the underlying mechanisms remain elusive. In this study, our results demonstrate that exogenous melatonin and MeJA enhance watermelon resistance against <i>Fusarium oxysporum</i> f. sp. <i>Niveum</i> race 2 (FON2) in a dose-dependent manner. The optimal concentration for melatonin and MeJA was determined to be 10 μM and 1 μM, respectively. Both melatonin and MeJA inhibited FON2 mycelial growth on PDA medium in a dose-dependent manner. Furthermore, exogenous melatonin significantly stimulated upregulation of MeJA synthesis genes and increased MeJA content upon FON2 infection. However, pretreatment with a MeJA synthesis inhibitor (DIECA) suppressed the induction of melatonin-induced resistance against FON2. Furthermore, MeJA also induced the upregulation of melatonin biosynthetic gene <i>caffeic acid O-methyltransferase 1</i> (<i>ClCOMT1</i>) and increased melatonin accumulation in response to FON2. Notably, the reduction in FON2 resistance caused by <i>ClCOMT1</i> deletion was completely restored through exogenous application of MeJA. These results suggest that melatonin facilitates MeJA accumulation, which provides feedback to promote melatonin accumulation, forming a reciprocal positive regulatory loop in response to FON2 infection. Additionally, polyphenol oxidase, phenylalanine ammonia lyase, and lignin are involved in the MeJA-induced resistance against FON2. The growing concern over minimizing pesticide usage and transitioning to sustainable and natural control strategies underscores the significant potential of such a mechanism in combating Fo.