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

ABSTRACT 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 H 2 O 2 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 H 2 O 2 bursts in systemic stomatal responses triggered by insect herbivory in tomato.