Spray-induced and nanocarrier-delivered gene silencing system targeting juvenile hormone receptor components: Potential application as fertility inhibitors for Adelphocoris suturalis management

Authors: ZHENG, WANYING - Huazhong Agricultural University; XU, XIAONA - Huazhong Agricultural University; HUANG, XINGXING - Huazhong Agricultural University; PENG, JIE - Huazhong Agricultural University; MA, WEIHUA - Huazhong Agricultural University; Hull, Joe; HUA, HONGXIA - Huazhong Agricultural University; CHEN, LIZHEN - Huazhong Agricultural University

Submitted to: Pest Management Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2024
Publication Date: 3/12/2024
Citation: Zheng, W., Xu, X., Huang, X., Peng, J., Ma, W., Hull, J.J., Hua, H., Chen, L. 2024. Spray-induced and nanocarrier-delivered gene silencing system targeting juvenile hormone receptor components: Potential application as fertility inhibitors for Adelphocoris suturalis management. Pest Management Science. 80(8):3743-3751. https://doi.org/10.1002/ps.8077.
DOI: https://doi.org/10.1002/ps.8077

Interpretive Summary: Although targeted disruption of insect reproduction has enormous potential for pest management, full implementation requires a complete understanding of the underlying molecular mechanisms. For most insects, reproduction is tightly regulated by juvenile hormone (JH) and 20-hydroxyecdysone (20E). The actions of both are mediated by dimeric nuclear receptors, JH with methoprene-tolerant (Met) and Taiman, and 20E with ecdysone receptor and ultraspiracle, that bind to specific DNA sequences to drive expression of reproduction associated genes. In some insect species, this can include fatty acyl reductases (FAR), which have largely been studied within a biological context of sex pheromone biosynthesis but have also been reported to impact ovarian development and female fecundity. To determine how these genes impact female reproduction in a plant bug pest of cotton, Met and Taiman functionality was disrupted by RNAi-mediated knockdown. In both cases, knockdown resulted in impaired ovaries and reduced fertility. Similar results were seen when the FAR gene was knocked down. Met and Taiman disruption also reduced FAR expression, whereas addition of a JH analog stimulated expression. However, the JH analog was unable to rescue impaired ovarian development following FAR knockdown. Disruption of the 20E receptors had no effect on FAR and addition of 20E was unable to rescue the FAR phenotype. These findings confirm the functional conservation of the JH receptors in plant bug reproduction and suggest that FAR impacts on reproduction occur downstream of JH activity rather than 20E.

Technical Abstract: BACKGROUND: Although RNA interference (RNAi) has potential to be a viable alternative to conventional pesticide-based pest management, the lack of efficient dsRNA delivery systems and effective candidate genes are currently limiting factors for field applications. The emergence of Adelphocoris suturalis as one of the most destructive pests in cotton-growing regions of China has increased the need to develop more efficient population management methods. Among the more intriguing targets proposed for pest control are the insect-specific juvenile hormones (JHs), which play critical roles in reproduction. The utility of targeting key JH signaling genes for hemipteran pest control, however, has yet to be fully explored. RESULTS: In this study, the JH receptor components methoprene-tolerant (Met) and Taiman (Tai) were identified from the A. suturalis genome. RNAi of either Met and Tai in A. suturalis suppressed ovarian development and reduced fertility. Based on this reproductive role, we targeted A. suturalis Met and Tai for knockdown by coupling nanomaterial-dsRNA complexes with a transdermal spray delivery system. Within 12 h of adult emergence, females were sprayed with star polycation (SPc)–dsRNA formulations and the RNAi effects were assessed over time. RNAi knockdown efficiencies of 39-58% were observed at 5 days post-treatment and abnormal ovarian development was apparent by 10 days post-treatment. CONCLUSION: Our results show that the JH signaling pathway plays a critical role in A. suturalis reproduction, and that coupling SPc nanoparticle-dsRNA complexes with a spray-based delivery system gene effectively impaired oviposition. These results have broad applications for further development of A. suturalis functional genomics and deployment for field application.