The zig-zag model of molecular defense and counterdefense in plant-herbivore interactions.

Abstract

Main conclusion: Plant-herbivore interactions follow zig-zag-like cycles in which herbivore- and damage-derived cues activate conserved defense signaling hubs, while insect effectors suppress or redirect these pathways, creating recurrent molecular bottlenecks that shape plant resistance. Plant-herbivore interactions are orchestrated through a dynamic molecular dialogue at the feeding interface, wherein insect attack triggers the generation of damage-derived signals from plant tissues and herbivore-derived signals from oral or salivary secretions. These cues can activate plant defense by sensing the damage- and herbivore-associated molecular patterns; however, they may also be mitigated by salivary effectors that suppress, redirect, or modulate host defense signaling. This review examines how plants interpret herbivory to synthesize defense decisions through receptor-mediated recognition, calcium and reactive oxygen species dynamics, membrane depolarization, mitogen-activated protein kinase signaling, and downstream hormonal integration, with a particular focus on the crosstalk among jasmonate, salicylic acid, and ethylene pathways. Additionally, we highlighted how insect-derived elicitors and effectors repeatedly converge on a limited set of defense-regulatory bottlenecks, including receptor proximal signaling, hormonal balance, callose deposition, and cell death-associated defense responses. Rather than categorizing elicitors and effectors as fixed molecular entities, we underscore that their biological significance is often context-dependent and influenced by host species, feeding mode, associated microbes, and the temporal dynamics of attack. Collectively, these patterns portray plant-insect interactions as a coevolutionary process involving signal generation, interpretation, and counterdefense. A comprehensive understanding of this molecular dialogue will facilitate the identification of key control points in defense and support the development of durable, ecologically informed strategies to enhance crop resistance against pests.