Dissecting the roles of Taiman in pupation and female reproduction of Helicoverpa armigera.

Abstract

In insects, metamorphosis and reproduction are coordinated by juvenile hormone (JH) and 20-hydroxyecdysone (20E). A transcription factor Taiman (Tai) serves as a coactivator of the functional 20E receptor and heterodimerizes with JH receptor Methoprene-tolerant (Met) to form an active receptor complex, encoding a key modulator of JH and 20E signaling pathways. However, direct evidence for the participation of Tai in metamorphic actions and vitellogenesis is quite limited. Herein, 1 isoform of Tai was identified from Helicoverpa armigera, named HaTai; the transcription of HaTai was stimulated by either JH or 20E ingestion. Knocking down HaTai in 5th instar larvae caused severe pupation failure and weight loss, wherein 69.44% of HaTai-RNAi (RNA interference) larvae died from pupation failure within 6 d. The HaTai-RNAi larvae exhibited attenuated JH signaling but intensified ecdysteroidogenesis, whereas supplementation with JH or 20E failed to recover the expression of HaTai. In female adults, depleting HaTai blocked vitellogenin transcription and caused atrophied ovaries with deficient yolk protein deposition. The HaTai-depleted females exhibited a substantial decrease in egg production. Moreover, the HaTai-depleted fat body became remarkably loose and partly vacuolated, accompanied by a reduction of triglyceride content. To explore the feasibility of oral-ingested RNAi, feeding chitosan-wrapped double-stranded RNA targeting Tai induced a pronounced silencing effect in larvae, causing a significant increase in larval mortality and a decrease in pupation rate. Our study therefore unveiled the complex roles of HaTai in pupation and JH-mediated vitellogenesis, and explored an effective RNAi method applicable in H. armigera.