Systemic root-shoot signaling drives jasmonate-based root defense against nematodes

Shoot-root communication is crucial for plant adaptation to environmental changes. However, the extensive crosstalk between shoots and roots that controls the synthesis of jasmonates (JAs), in order to enhance defense responses against rhizosphere herbivores, remains poorly understood. Here, we report that the root-knot nematode (RKN) Meloidogyne incognita induces the systemic transmission of electrical and reactive oxygen species (ROS) signals from attacked tomato roots to the leaves, leading to an increased accumulation of JAs in the leaves. Grafting of 1.0-cm stem sections from mutants lacking GLUTAMATE RECEPTOR-LIKE 3.5 or the mutants deficient in RESPIRATORY BURST OXIDASE HOMOLOG 1 abolished the RKN-induced electrical signals and associated ROS and JA accumulation in the upper stems and leaves with attenuated resistance to RKN. Furthermore, the absence of systemic transmission of electrical and ROS signals compromised the activation of mitogen-activated protein kinases (MPKs) 1/2 in leaves. Silencing MPK1 or MPK2 abolished RKN-induced accumulation of JAs and associated resistance. These findings reveal a systemic signaling loop that integrates electrical, ROS, and JA signals to enhance the resistance in distal organs via root-shoot-root communication.