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BACKGROUND: The migratory brown planthopper (BPH), Nilaparvata lugens (Hemiptera: Delphacidae), is the most destructive pest affecting rice plants in Asia and feeds exclusively on rice. Studies have investigated the olfactory response of BPHs to the major rice volatile compounds in rice. The insect olfactory co‐receptor (Orco) is a crucial component of the olfactory system and is essential for odorant detection. Functional analysis of the Orco gene in BPHs would aid in the identification of their host preference. RESULTS: We identified the BPH Orco homologue (NlOrco) by Blast searching the BPH transcriptome with the Drosophila Orco gene sequence. Spatiotemporal analysis indicated that NlOrco is first expressed in the later egg stage, and is expressed mainly in the antennae in adult females. A NlOrco‐knockout line (NlOrco−/−) was generated through clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9‐mediated mutagenesis. The NlOrco−/− mutants showed no response to rice volatile compounds and consequently no host‐plant preference. In addition, NlOrco−/− mutants exhibited extended nymphal duration and impaired fecundity compared with wild‐type BPHs. CONCLUSION: Our findings indicated that BPHs exhibit strong olfactory responses to major rice volatile compounds and suggest that NlOrco is required for the maximal fitness of BPHs. Our results may facilitate the identification of potential target genes or chemical compounds for BPH control applications. © 2022 Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

Insect wing polyphenism is characterized by its ability to produce two or more distinct wing morphs from a single genotype in response to changing environments. However, the molecular basis of this phenomenon remains poorly understood. Here, we identified a zinc finger homeodomain transcription factor Zfh1 that acts as an upstream regulator for the development of long-winged (LW) or shorted-winged (SW) morphs in planthoppers. Knockdown of Zfh1 directs SW-destined nymphs to develop into LW morphs by down-regulating the transcriptional level of FoxO, a prominent downstream effector of the insulin/IGF signaling (IIS) pathway. The balance between transcriptional regulation via the Zfh1-FoxO cascade and post-translational regulation via the IIS-FoxO cascade provides a flexible regulatory mechanism for the development of alternative wing morphs. These findings help us understand how phenotypic diversity is generated by altering the activity of conserved proteins, and provide an extended framework for the evolution of wing morphological diversity in insects. The molecular mechanisms underlying wing polyphenism remain poorly understood. Here the authors use plant hoppers to show that the development of long and short wing morphs is balanced by the relative activities of the Zfh1-FoxO and insulin signaling cascades. [ABSTRACT FROM AUTHOR]

The homeotic complex gene Abdominal‐B (Abd‐B) is involved in regulating the development of posterior abdomens and has been extensively studied in holometabolous insects. However, the function of Abd‐B in hemimetabolous insects is not fully understood. Here, we functionally characterize an Abd‐B homologue in the brown planthopper (BPH), Nilaparvata lugens. The full‐length cDNA of the N. lugens Abd‐B homologue (NlAbd‐B) is 2334 nt, with an open reading frame of 1113 bp. NlAbd‐B has the highest expression level at the egg stage relative to the nymphal and adult stages and is mainly expressed in the fourth to the ninth abdominal segment of embryos. RNA interference (RNAi)‐mediated knockdown of NlAbd‐B in nymphs disrupted the development of genitalia both in females and males and caused a genitalia‐to‐leg transformation. Parental RNAi of NlAbd‐B in both female and male adults caused an extra abdominal segment in offspring nymphs, while parental RNAi of the N. lugens abdominal‐A homologue in both female and males adults led to embryos with leg‐like appendages on the second to the eighth abdominal segment. These findings suggest that NlAbd‐B plays a pivotal role in genital development and posterior abdominal patterning and thus highlight the conservational role of Abd‐B in holometabolous and hemimetabolous insects. [ABSTRACT FROM AUTHOR]

A single insulin receptor (InR) gene has been identified and extensively studied in model species ranging from nematodes to mice. However, most insects possess additional copies of InR, yet the functional significance, if any, of alternate InRs is unknown. Here, we used the wing-dimorphic brown planthopper (BPH) as a model system to query the role of a second InR copy in insects. NlInR2 resembled the BPH InR homologue (NlInR1) in terms of nymph development and reproduction, but revealed distinct regulatory roles in fuel metabolism, lifespan, and starvation tolerance. Unlike a lethal phenotype derived from NlInR1 null, homozygous NlInR2 null mutants were viable and accelerated DNA replication and cell proliferation in wing cells, thus redirecting short-winged–destined BPHs to develop into long-winged morphs. Additionally, the proper expression of NlInR2 was needed to maintain symmetric vein patterning in wings. Our findings provide the first direct evidence for the regulatory complexity of the two InR paralogues in insects, implying the functionally independent evolution of multiple InRs in invertebrates. Author summary: The highly conserved insulin/insulin-like growth factor signaling pathway plays a pivotal role in growth, development, and various physiological processes across a wide phylogeny of organisms. Unlike a single InR in the model species such as the fruit fly Drosophila melanogaster and the nematode Caenorhabditis elegans, most insect lineages have two or even three InR copies. However, the function of the alternative InRs remains elusive. Here, we created a homozygous mutation for a second insulin receptor (InR2) in the wing-dimorphic brown planthopper (BPH), Nilaparvata lugens, using the clustered regularly interspaced palindromic repeats/CRISPR-associated (CRISPR/Cas9) system. Our findings revealed that InR2 possesses functions distinct from the BPH InR homologue (NlInR1), indicating that multiple InR paralogues may have evolved independently and may have functionally diversified in ways more complex than previously expected in invertebrates. [ABSTRACT FROM AUTHOR]

Wing polymorphism is an evolutionary feature found in a wide variety of insects, which offers a model system for studying the evolutionary significance of dispersal. In the wing-dimorphic planthopper Nilaparvata lugens, the insulin/insulin-like growth factor signaling (IIS) pathway acts as a 'master signal' that directs the development of either long-winged (LW) or short-winged (SW) morphs via regulation of the activity of Forkhead transcription factor subgroup O (NlFoxO). However, downstream effectors of the IIS–FoxO signaling cascade that mediate alternative wing morphs are unclear. Here we found that vestigial (Nlvg), a key wing-patterning gene, is selectively and temporally regulated by the IIS–FoxO signaling cascade during the wing-morph decision stage (fifth-instar stage). RNA interference (RNAi)-mediated silencing of Nlfoxo increase Nlvg expression in the fifth-instar stage (the last nymphal stage), thereby inducing LW development. Conversely, silencing of Nlvg can antagonize the effects of IIS activity on LW development, redirecting wing commitment from LW to the morph with intermediate wing size. In vitro and in vivo binding assays indicated that NlFoxO protein may suppress Nlvg expression by directly binding to the first intron region of the Nlvg locus. Our findings provide a first glimpse of the link connecting the IIS pathway to the wing-patterning network on the developmental plasticity of wings in insects, and help us understanding how phenotypic diversity is generated by the modification of a common set of pattern elements. Author summary: Many insects are capable of developing into either long-winged or short-winged adults, but the underlying molecular basis remains largely unknown. Pioneer studies showed that the insulin/insulin-like growth factor signaling pathway acts as a 'master signal' that directs wing buds to develop into long or short wings in the wing-dimorphic planthopper, Nilaparvata lugens. However, downstream effectors mediating the IIS pathway effects are unknown. Our findings highlight that vestigial, a key wing-patterning gene, is a main downstream effector that mediates the IIS activity on the development of alternative wing morphs during the wing-morph decision stage. The molecular mechanism of wing formation, including the function of vestigial, has been studied in great depth in the model insect Drosophila melanogaster. Our data provide a first glimpse of the link connecting the IIS pathway to the wing-patterning network in regulating developmental plasticity of wings in insects. [ABSTRACT FROM AUTHOR]