The Key Glutathione S-Transferase Family Genes Involved in the Detoxification of Rice Gramine in Brown Planthopper Nilaparvata lugens

SIMPLE SUMMARY: Plant defensive compounds are the effective measures for host plants to defend against herbivorous insects, whereas in turn insects evolve an array of detoxifying enzymes to overcome the resistance of these compounds. However, the molecular mechanisms underlying the resistance of plant toxins to herbivores are still unclear. This study uses an integrative approach to investigate the molecular basis of how brown planthopper uses glutathione S-transferases to detoxify gramine, an important defensive toxin in rice. We show here that gramine can induce the activity and increase the transcripts of glutathione S-transferase in brown planthopper. Knockdown of seven glutathione S-transferase family genes of brown planthopper increases its sensitivity to gramine. The glutathione S-transferase activity is regulated by the expression of three key genes (NlGST1-1, NlGSTD2, and NlGSTE1), as silencing of these genes significantly inhibits this enzyme’s activity. The current study identifies a few key glutathione S-transferase genes involved in the detoxification of gramine in brown planthopper. Our findings unravel the molecular mechanisms of the detoxification of plant defensive chemicals by glutathione S-transferases, providing a new potential pest control strategy that uses the method of RNA interference to deplete this gene family to increase the efficiency of host resistance to herbivores. ABSTRACT: Phytochemical toxins are considered a defense measure for herbivore invasion. To adapt this defensive strategy, herbivores use glutathione S-transferases (GSTs) as an important detoxification enzyme to cope with toxic compounds, but the underlying molecular basis for GST genes in this process remains unclear. Here, we investigated the basis of how GST genes in brown planthopper (BPH, Nilaparvata lugens (Stål)) participated in the detoxification of gramine by RNA interference. For BPH, the LC(25) and LC(50) concentrations of gramine were 7.11 and 14.99 μg/mL at 72 h after feeding, respectively. The transcriptions of seven of eight GST genes in BPH were induced by a low concentration of gramine, and GST activity was activated. Although interferences of seven genes reduced BPH tolerance to gramine, only the expression of NlGST1-1, NlGSTD2, and NlGSTE1 was positively correlated with GST activities, and silencing of these three genes inhibited GST activities in BPH. Our findings reveal that two new key genes, NlGSTD2 and NlGSTE1, play an essential role in the detoxification of gramine such as NlGST1-1 does in BPH, which not only provides the molecular evidence for the coevolution theory, but also provides new insight into the development of an environmentally friendly strategy for herbivore population management.