Two fungicides alter reproduction of the small brown planthopper, Laodelphax striatellus by influencing gene and protein expression

Authors: WU, YOU - Yangzhou University; DING, JUN - Yangzhou University; XU, BING - Yangtze University; YOU, LINLIN - Yangzhou University; GE, LINQUAN - Yangzhou University; YANG, GUOQING - Yangzhou University; LIU, FANG - Yangzhou University; Stanley, David; SONG, QISHENG - University Of Missouri; WU, JINCAI - Yangzhou University

Submitted to: Journal of Proteome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/30/2018
Publication Date: 2/7/2018
Citation: Wu, Y., Ding, J., Xu, B., You, L., Ge, L., Yang, G., Liu, F., Stanley, D.W., Song, Q., Wu, J. 2018. Two fungicides alter reproduction of the small brown planthopper, Laodelphax striatellus by influencing gene and protein expression. Journal of Proteome Research. 17(3):978-986. https://doi.org/10.1021/acs.jproteome.7b00612.
DOI: https://doi.org/10.1021/acs.jproteome.7b00612

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 two fungicides, jinggangmycin (JGM) and carbendazim (CBM), on the small brown planthopper (SBPH), an insect rice pest in Asia. The fungicides have been used for decades to control rice fungal diseases. Exposure to CBM led to increased egg-laying, up by almost 80% and exposure to JGM decreased egg-laying by about half. At the molecular level, the fungicides act on at least two genes involved in fat metabolism that mediate these changes in reproduction. The significance of this work is that it highlights the unexpected influences of agricultural fungicides on pest insect populations. This information will be important to scientists developing novel fungal disease management technologies that will not positively influence pest insect populations and, ultimately, important to nutritional security for consumers.

Technical Abstract: Aside from their intended actions, fungicides can drive pest insect outbreaks and, due to virtually continuous use, evolution. Small brown planthopper (SBPH), Laodelphax striatellus, outbreaks occurred recently in many provinces in China, with devastating rice losses. Because exposure to the fungicide jinggangmycin (JGM) increased reproduction of the brown plant hopper, Nilaparvata lugens, via its influence on fatty acid synthase, we posed the hypothesis that JGM and CBM influence SBPH reproduction via their influence on enzymes involved in other aspects of lipid metabolism. Exposure to the fungicide carbendazim (CBM) stimulated SBPH reproduction (egg-laying ' by 78%) and to another fungicide, JGM, led to decreased egg-laying (' by 47.3%). These inverse effects are mediated by down-regulated expression of L-3-hydroxyacyl-Coenzyme A dehydrogenase (LCHAD) in JGM-treated females and up-regulated expression of hydroxysteroid dehydrogenase-like protein 2-like (HSD) in CBM-treated females. RNAi knockdown of , separately, LCHAD and HSD led to reduced egg laying (' by 53.5% for dsLCHAD and by 73% for dsHSD ). dsLCHAD, dsHSD and JGM treatments also led to severely reduced ovarian development in experimental SBPH, with shorted and thinned oviducts lacking egg cells. Oviducts of CBM-treated females were normal, with banana-shaped eggs. These data strongly support our hypothesis.