Dissecting the roles of FTZ-F1 in larval molting and pupation, and the sublethal effects of methoxyfenozide on Helicoverpa armigera.

Abstract

In holometabolous insects, the major developmental transitions - larval molting and pupation - are triggered by a pulse of 20-hydroxyecdysone (20E) and coordinated by juvenile hormone. Methoxyfenozide (MF), an ecdysteroid agonist, represents a new class of insect growth regulators and is effective against lepidopteran pests. Fushi-tarazu factor 1 (FTZ-F1) is an ecdysone-inducible transcription factor. To date, the effect of MF on 20E-response genes remains unclear, and we speculate the involvement of FTZ-F1 in MF's growth regulating effect. MF at LC25 and LC10 caused severe ecdysis failure in Helicoverpa armigera, extended their larval duration, lowered their pupal weight, and reduced the respiratory, pupation and emergence rates. Furthermore, sublethal doses of MF inhibited ecdysteroidogenesis and lowered the intrinsic 20E titer, but showed an inductive effect on 20E-response genes including HaFTZ-F1. HaFTZ-F1, predominantly expressed in larval epidermis, was markedly upregulated before or right after larval ecdysis, and maintained a high level in prepupal stage. Knockdown of HaFTZ-F1 in 4th-instar larvae severely impaired larval ecdysis, whereas its knockdown in final-instar larvae caused abnormal pupation. Moreover, knocking down HaFTZ-F1 downregulated three critical ecdysteroidogenesis genes, lowered 20E titer, and suppressed the expression of 20E receptors and 20E-response genes. The introduction of 20E into HaFTZ-F1-RNAi larvae partly relieved the negative effects on the 20E-induced signaling cascade. Our findings reveal the adverse effects of sublethal doses of MF on the development of H. armigera and elucidate the resulting perturbations on the 20E-induced signaling cascade; we propose that HaFTZ-F1 regulates ecdysis and pupation by mediating 20E titer and its signaling pathway. © 2020 Society of Chemical Industry.