Adaptation of an herbivorous arthropod to green tea plants by overcoming catechin defenses

Green tea catechins are known antioxidants that benefit human health and protect tea plants from biotic stressors. However, some herbivores can counteract catechin defenses and can use tea plants as a host. Among herbivorous mites, an extreme generalist Tetranychus urticae has not been reported as a tea pest. Instead, T. kanzawai, another generalist, has some populations that thrive on tea plants. Here, we investigated the mechanism of the adaptation of these mites to tea plants. Comparative study of the intra- and inter-specific variations in mite performances uncovered differences in their behavioral and xenobiotic responsiveness to green tea catechins. We showed that green tea catechins exert complex defensive roles. They were repellent and toxic to T. urticae and tea non-adapted T. kanzawai mites. In addition, they had an antifeedant effect on tea non-adapted T. kanzawai mites. Matching the catechin structure, we identified an intradiol ring-cleavage dioxygenase DOG15, a gene horizontally transferred from fungi, as one required for the adaptation of T. kanzawai mites to tea plants. The DOG15 gene has an enhanced inducible expression in tea-adapted T. kanzawai mites, with mRNA and protein levels up to 31.6 and 12.1 times higher than in T. urticae mites fed on tea plants. Furthermore, we identified two amino acid substitutions in DOG15 between Tetranychus species leading to the increased efficacy of the T. kanzawai encoded enzyme toward cleavage of green tea catechins. Thus, we showed that mite adaptation to tea plants occurred in a two-step process. The amino acid substitutions in DOG15 predispose T. kanzawai but not T. urticae for the adaptation to tea plants. Further increased expression of modified DOG15 enables T. kanzawai mites to efficiently detoxify green tea catechins, leading to intra- and inter-specific differences in mites ability to use tea plants as a host. Our findings reveal how a horizontally transferred gene can be co-opted through structural and regulatory changes to overcome plant chemical defenses, with implications for herbivore host adaptation and tea pest management.