Mirid bug feeding at the early fruit stage primes long-term systemic defenses in guava that suppress tephritid fruit...

Plants deploy inducible defense mechanisms that can be locally activated and systemically expressed following herbivore attack. While such induced responses are well characterized in model systems, their persistence and ecological consequences in perennial fruit crops remain poorly understood. We investigated whether early-season infestation of guava (Psidium guajava L.) fruits by the tea mosquito bug (Helopeltis antonii), a piercing-sucking herbivore, induces systemic defenses that influence subsequent colonization by the generalist tephritid fruit fly, Bactrocera dorsalis. Behavioral assays revealed that prior infestation by H. antonii significantly reduced attraction, oviposition, and larval performance of B. dorsalis. GC-MS profiling demonstrated a marked shift in volatile emissions from ester-dominated blends in healthy fruits to terpene- and hydrocarbon-rich profiles in infested fruits. Electrophysiological and molecular docking analyses indicated that these herbivory-induced volatile changes are differentially perceived within the fruit fly olfactory system. Concurrently, biochemical analyses showed depletion of primary metabolites (sugars and amino acids), accumulation of phenolics and flavonoids, and enhanced antioxidant enzyme activities and defense-related gene expression, indicating coordinated metabolic reprogramming. Collectively, these findings demonstrate that early piercing-sucking herbivory induces a durable systemic defense state in guava, reshaping fruit chemistry and semiochemical signaling in ways that suppress later colonization by a frugivorous pest. Understanding such sequential herbivore interactions provides mechanistic insight into plant defense plasticity and offers potential avenues for enhancing natural resistance in perennial fruit systems.