Different detoxification strategies of fruit borers adaptation to quercetin

Abstract

During long-term plant-insect interactions, plants have evolved diverse plant secondary metabolites (PSMs) as defenses against herbivory, while insects have developed sophisticated detoxification mechanisms to neutralize these compounds. Invasive and native herbivorous species may employ distinct metabolic strategies to cope with PSMs, a phenomenon that remains incompletely characterized. Here, we report the differential detoxification strategies of two closely related fruit borers, the invasive Cydia pomonella and the native Grapholita molesta, which exhibit interspecific competition, in response to quercetin stress—a flavonoid present in their host fruits. C. pomonella requires more generations to adapt 70 μg/g quercetin, indicating differential tolerance to flavonoid toxicity. Metabolic profiling shows G. molesta primarily detoxifies quercetin mainly via synergistic cytochrome P450 (P450) and transmembrane transport, whereas C. pomonella shifts from transport to a predominant role of oxidation over time. Given that C. pomonella was not pre-adapted to high quercetin stress in its native habitat, its constitutive defense system was likely suppressed under quercetin exposure. This species compensated by upregulating ATP-binding cassette (ABC) transporter-mediated excretion, as evidenced by HPLC quantification which indicated that the fecal quercetin content exceeded 50 % of the administered dose. Correlation analysis suggests that C. pomonella employs a biphasic detoxification: initial short-term dominated by ABC transporter activity, followed by a long-term reliance on P450-mediated metabolism. Conversely, G.molesta primarily utilizes a synergistic enzymatic detoxification system involving multiple enzymes. These findings elucidate divergent adaptive mechanisms to quercetin stress in the two fruit borers and enhance understanding of herbivorous insect-plant co-evolution and the interspecific interactions between invasive and native pest species.