The glutamate receptor-like 3.3 and 3.6 mediate systemic resistance to insect herbivores in Arabidopsis

Abstract Herbivory activates responses in local and systemic leaves, and the glutamate receptor-like genes GLR3.3 and GLR3.6 are critical in leaf-to-leaf systemic signaling. However, whether and how they mediate plant systemic resistance to insects remain largely unexplored. We show that piercing-sucking insect Myzus persicae (green peach aphid, GPA) or chewing insect Spodoptera litura (cotton leafworm, CLW) feeding-induced systemic defenses were attenuated in the glr3.3 glr3.6 mutants. In response to herbivory from either insect, glr3.3 glr3.6 mutants exhibited reduced accumulation of the hormone jasmonic acid (JA) and defensive metabolites glucosinolates (GSs) in systemic (but not local) leaves. Transcriptome analysis indicated that GLR3.3 and GLR3.6 play an important role in regulating the transcriptional responses to GPA and simulated CLW feeding in both local and systemic leaves, including JA- and GS-related genes. Metabolome analysis also revealed that in response to GPA or simulated CLW feeding, GLR3.3 and GLR3.6 are involved in the regulation of various metabolites locally and systemically, including amino acids, carbohydrates, and organic acids. Taken together, this study provides new insight into the function of GLR3.3 and GLR3.6 in mediating transcripts and metabolites in local and systemic leaves under insect attack, and highlights their role in regulating insect resistance in systemic leaves.