NADPH Oxidase 5 Is Essential for Molting and Oviposition in a Rice Planthopper Nilaparvata lugens

SIMPLE SUMMARY: The brown planthopper, Nilaparvata lugens, a plant phloem-sucking Hemipteran insect, has become the most destructive pest for rice—the major food source for half of the world’s population. Nilaparvata lugens possess robust fecundity, enabling population densities to increase quickly in a favorable environment. Nilaparvata lugens has also been used as a model system for ecological studies and for developing effective pest management. To better understand the regulation mechanisms of insect reproduction and to provide insights to improve pest control, we searched N. lugens genome and transcriptome databases and identified an NADPH oxidase 5 gene, which was specifically expressed in ovaries of female adults and freshly laid eggs in rice leaf sheaths. Although homologous NADPH oxidase 5 genes have been identified in many insect species, their reproductive functions remain unknown. In this work, our findings initially reveal a functional role of the NADPH oxidase 5 gene in molting and oviposition in N. lugens. This novel finding improves our understanding of the reproductive strategies in insects and provides a potential molecular target for effective pest control of the rice planthopper. ABSTRACT: The brown planthopper Nilaparvata lugens is a typical monophagous insect herbivore that feeds exclusively on rice sap. This insect pest causes serious damage to rice crops throughout East Asian countries. Chemical control remains the first choice for managing N. lugens populations; however, the use of insecticides has given rise to planthopper resurgence and additional environmental risks. Nilaparvata lugens is a model insect of Hemiptera because its whole genome sequence has been elucidated and is susceptible to RNA interference. In this study, our findings revealed that a superoxide-generating gene, NADPH oxidase 5 (Nox5), is essential for molting and oviposition in a Hemipteran insect Nilaparvata lugens. Knockdown of Nox5 transcript levels by RNA interference in 2nd–5th-instar nymphs results in significantly lethal deficits in the molting transitions from nymph–nymph and nymph–adult. Nox5 knockdown leads to a reduction of hydrogen peroxide in female ovaries and failure of oviposition from the insect ovipositor into the rice leaf sheath. Here, we provide in vivo evidence demonstrating that Nox5 is a key enzyme for regulating molting and oviposition in this insect species.