Jasmonate‐Mediated Systemic Signaling Triggered by Local Herbivory Coordinates Systemic Stomatal Closure in Tomato ( <i>Solanum lycopersicum</i> L.)

Upon attack by insect herbivores, plants can perceive herbivore-derived physical and chemical cues and rapidly reallocate their resources for growth and defense. Insect herbivory specifically induces rapid systemic down-regulation of plant photosynthesis, characterized by whole-plant systemic stomatal closure. However, its underlying mechanism is not fully understood. Here, we found that the simulated herbivory (wounding + oral secretion, WOS) in tomato local (treated) leaflets triggered a decrease of more than 45.0% in stomatal conductance (g_s) in the systemic (adjacent and distal) uninjured leaflets 3 h after the treatment. Local WOS treatment also induced local upregulation of jasmonic acid (JA) biosynthesis genes and systemic JA accumulation in wild-type tomato. Consistently, the systemic stomatal closure response was severely compromised in JA synthesis-deficient mutants (spr2 and spr8). Grafting experiments with wild-type and spr8 mutant proved that the local JA biosynthesis triggered by WOS is essential for systemic stomatal closure. In addition, JA-mediated H₂O₂ bursts in the systemic guard cells is vital for systemic stomatal closure triggered by local WOS treatment. Our findings reveal a crucial role of local JA biosynthesis and systemic JA-mediated H₂O₂ bursts in systemic stomatal responses triggered by insect herbivory in tomato.