HY5 integrates light and electrical signaling to trigger a jasmonate burst for nematode defense in tomato

Plants have evolved sophisticated defense systems to protect against herbivory, including the systemic induction of jasmonic acid (JA) synthesis. However, the molecular mechanisms underlying this process remain poorly understood. Here, we report that root-knot nematode (RKN) attack induced a phyB-dependent accumulation of ELONGATED HYPOCOTYL 5 (HY5) in the leaves, which activates the expression of JA biosynthesis genes and HY5 itself in tomato. In addition, the systemic transmission of GLUTAMATE RECEPTOR-LIKE 3.5 (GLR3.5)-dependent electrical signals induced by RKN triggers the physical interaction between CALMODULIN 2 (CaM2) and HY5 to amplify the transcriptional regulation of HY5 and JA synthesis. HY5 functions as a systemic signal that moves from leaves to roots to maintain the electrical signaling from roots to leaves by activating GLR3.5 expression. Together, these results reveal a HY5-dependent systemic signaling cascade that integrates light and electrical signals to activate JA-mediated defense against nematodes in tomato. Sun et al. reveal that root-knot nematode attack activates a phyB-HY5 cascade that integrates light and GLR3.5-CaM2 signals to boost JA synthesis in tomato, with HY5 moving from leaves to roots to sustain signaling and trigger JA-mediated defense.