The antibiotic jinggangmycin increases brown planthopper (BPH) fecundity by enhancing rice plant sugar concentrations and BPH insulin-like signaling

Authors: GE, LINQUAN - Yangzhou University; ZHOU, ZE - Yangzhou University; SUN, KAIDI - Yangzhou University; HUANG, BO - Yangzhou University; Stanley, David; SONG, QI SHENG - University Of Missouri

Submitted to: Chemosphere
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/9/2020
Publication Date: 3/10/2020
Citation: Ge, L., Zhou, Z., Sun, K., Huang, B., Stanley, D.W., Song, Q. 2020. The antibiotic jinggangmycin increases brown planthopper (BPH) fecundity by enhancing rice plant sugar concentrations and BPH insulin-like signaling. Chemosphere. 249:126463. https://doi.org/10.1016/j.chemosphere.2020.126463.
DOI: https://doi.org/10.1016/j.chemosphere.2020.126463

Interpretive Summary: Climate change is exerting marked effects on the activities of insect pests. Most attention has focused on their geographical ranges. A central problem, however, is the potential risks of exposing pest populations to increasing, non-lethal temperatures. The risks include increased numbers of generations per year, longer daily and annual activity periods and increased geographical ranges. These changes in pest populations may have severe consequences, including increased crop losses and decreased food security at the global level. In this paper we investigated the influence of jinggangmycin (JGM), an antibiotic used broadly to control rice sheath blight disease on increased reproductive fitness of an insect pest, the brown planthopper. We found exposure to JGM leads to increases in brown planthopper fecundity via two mechanisms, one through increasing rice plant sugar concentrations and a second by upregulating reproduction and populations of an insect pest. Coupled with earlier reports that JGM also increases brown planthopper tolerance of increasing temperatures, JGM treatments to control a rice disease could create large increases in pest brown planthopper populations. The significance of this work is that it highlights an unexpected effect of treating a rice plant disease on increased reproduction of a pest insect species. This information will be important to scientists developing novel, molecular tools for insect pest management.

Technical Abstract: The brown planthopper (BPH), Nilaparvata lugens, is a resurgent pest with an unexpected response to jinggangmycin (JGM), a broadly applied antibiotic used to control rice sheath blight disease. JGM stimulates BPH fecundity, but the underlying molecular mechanisms remain unclear. Here we report that JGM sprays led to increased glucose concentrations, photosynthesis and gene expression, specifically Rubisco, sucrose phosphate synthase, invertase 2 (INV2) and INV3 in rice jplants. JGM sprays let to high-glucose rice plants. Feeding BPH on these plants led to increased insulin-like signaling and vitellogenin synthesis. Treating BPH with metformin, a gluconeogenesis inhibitor, reversed the influence of feeding on high-glucose rice, which was rescued by glucose injections. Silencing insulin-like peptide 2 using per os dsRNA led to reduction in juvenile hormone (JH) III titers and other fecundity parameters which were reversed by topical application of JH analog, methoprene. We infer that JGM acts via two broad mechanisms, one through increasing rice plant sugar concentrations and a second by upregulating BPH insulin-like signaling.