Characterization of UDP-Glucuronosyltransferases and the Potential Contribution in Nicotine Tolerance in Myzus persicae

Uridine diphosphate (UDP)-glycosyltransferases (UGTs) are major phase II detoxification enzymes involved in glycosylation of lipophilic endobiotics and xenobiotics, including phytoalexins. Nicotine, one of the most abundant secondary plant metabolites, is highly toxic to herbivorous insects. Plant-herbivore competition has been the major impetus for evolution of large superfamilies of UGTs and other detoxification enzymes. However, UGT functions in Myzus persicae adaptation have remained unknown. In this study, UGT inhibitors (sulfinpyrazone and 5-nitrouracil) significantly increased nicotine toxicity in M. persicae nicotianae, suggesting UGTs may be involved in nicotine tolerance. One hundred one UGT transcripts identified from the M. persicae genome/transcriptome were renamed according to UGT Nomenclature Committee guidelines and clustered into 11 families: UGT329, UGT330, UGT339, UGT341-UGT345, and UGT348-UGT350. UGT344 contained the most UGTs (fifty-seven). Ten UGTs (UGT330A3, UGT339A2, UGT341A6, UGT342B3, UGT343C3, UGT344D5, UGT344D8, UGT348A3, UGT349A3 and UGT350A3) were overexpressed in M. persicae nicotianae compared with M. persicae sensu stricto. UGT330A3/UGT344D5/UGT348A3/UGT349A3 knockdown significantly increased M. persicae nicotianae nicotine sensitivity, suggesting UGT upregulation in this subspecies may be associated with nicotine tolerance and thus host adaptation. This study reveals possible UGTs relevant to nicotine adaptation in tobacco-consuming M. persicae nicotianae and might facilitate further validation of the roles of these UGTs in nicotine tolerance.