FoxO is required for optimal fitness of the migratory brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae)

The forkhead box O (FoxO) protein is the main transcriptional effector downstream of the insulin/insulin-like signaling pathway and regulates many developmental and physiological processes. Holometabolous insects with loss-of-function mutations in FoxO exhibit phenotypes distinct from those of hemimetabolous insects in which RNA interference was used. Despite the functional importance of FoxO, whether hemimetabolous insects share an evolutionally conserved function of FoxO with holometabolous insects remains to be clarified. We used the clustered regularly interspaced short palindromic repeats/CRISPR-associated 9 (CRISPR/Cas9) genome editing-system to establish a homozygous FoxO-null mutant (NlFoxO4E ) of the wing-dimorphic brown planthopper (BPH) Nilaparvata lugens, an economically important insect pest of rice fields. The phenotypes of NlFoxO4E mutants included extended nymphal duration, shortened lifespan, reduced reproduction, and decreased stress resistance. In addition, depletion of NlFoxO promoted cell proliferation in wing buds and led to 100% long-winged morphs, in stark contrast to short-winged wild-type BPHs. These findings indicate that NlFoxO is highly functionally conserved with its counterpart in holometabolous insects, and is required for optimal fitness of N. lugens. The insights from FoxO studies may facilitate the identification of potential target genes for BPH control applications.