Gustatory Receptors Research Articles

Oxalic Acid Inhibits Feeding Behavior of the Brown Planthopper via Binding to Gustatory Receptor Gr23a.

Plants produce diverse secondary compounds as natural protection against microbial and insect attack. Most of these compounds, including bitters and acids, are sensed by insect gustatory receptors (Grs). Although some organic acids are attractive at low or moderate levels, most acidic compounds are potentially toxic to insects and repress food consumption at high concentrations. At present, the majority of the reported sour receptors function in appetitive behaviors rather than aversive taste responses. Here, using two different heterologous expression systems, the insect Sf9 cell line and the mammalian HEK293T cell line, we started from crude extracts of rice (Oryza sativa) and successfully identified oxalic acid (OA) as a ligand of NlGr23a, a Gr in the brown planthopper Nilaparvata lugens that feeds solely on rice. The antifeedant effect of OA on the brown planthopper was dose dependent, and NlGr23a mediated the repulsive responses to OA in both rice plants and artificial diets. To our knowledge, OA is the first identified ligand of Grs starting from plant crude extracts. These findings on rice-planthopper interactions will be of broad interest for pest control in agriculture and also for better understanding of how insects select host plants.

Circulating fructose regulates a germline stem cell increase via gustatory receptor-mediated gut hormone secretion in mated Drosophila.

Oogenesis is influenced by multiple environmental factors. In the fruit fly, Drosophila melanogaster, nutrition and mating have large impacts on an increase in female germline stem cells (GSCs). However, it is unclear whether these two factors affect this GSC increase interdependently. Here, we report that dietary sugars are crucial for the GSC increase after mating. Dietary glucose is required for mating-induced release of neuropeptide F (NPF) from enteroendocrine cells (EECs), followed by NPF-mediated enhancement of GSC niche signaling. Unexpectedly, dietary glucose does not directly act on NPF-positive EECs. Rather, it contributes to elevation of hemolymph fructose generated through the polyol pathway. Elevated fructose stimulates the fructose-specific gustatory receptor, Gr43a, in NPF-positive EECs, leading to NPF secretion. This study demonstrates that circulating fructose, derived from dietary sugars, is a prerequisite for the GSC increase that leads to enhancement of egg production after mating.

Molecular sensors in the taste system of Drosophila.

Most animals, including humans and insects, consume foods based on their senses. Feeding is mostly regulated by taste and smell. Recent insect studies shed insight into the cross-talk between taste and smell, sweetness and temperature, sweetness and texture, and other sensory modality pairings. Five canonical tastes include sweet, umami, bitter, salty, and sour. Furthermore, other receptors that mediate the detection of noncanonical sensory attributes encoded by taste stimuli, such as Ca2+, Zn2+, Cu2+, lipid, and carbonation, have been characterized. Deorphanizing receptors and interactions among different modalities are expanding the taste field. Our study explores the taste system of Drosophila melanogaster and perception processing in insects to broaden the neuroscience of taste. Attractive and aversive taste cues and their chemoreceptors are categorized as tables. In addition, we summarize the recent progress in animal behavior as affected by the integration of multisensory information in relation to different gustatory receptor neuronal activations, olfaction, texture, and temperature. We mainly focus on peripheral responses and insect decision-making. Drosophila is an excellent model animal to study the cellular and molecular mechanism of the taste system. Despite the divergence in the receptors to detect chemicals, taste research in the fruit fly can offer new insights into the many different taste sensors of animals and how to test the interaction among different sensory modalities.

Structural screens identify candidate human homologs of insect chemoreceptors and cryptic Drosophila gustatory receptor-like proteins.

Insect odorant receptors and gustatory receptors define a superfamily of seven transmembrane domain ion channels (referred to here as 7TMICs), with homologs identified across Animalia except Chordata. Previously, we used sequence-based screening methods to reveal conservation of this family in unicellular eukaryotes and plants (DUF3537 proteins) (Benton et al., 2020). Here, we combine three-dimensional structure-based screening, ab initio protein folding predictions, phylogenetics, and expression analyses to characterize additional candidate homologs with tertiary but little or no primary structural similarity to known 7TMICs, including proteins in disease-causing Trypanosoma. Unexpectedly, we identify structural similarity between 7TMICs and PHTF proteins, a deeply conserved family of unknown function, whose human orthologs display enriched expression in testis, cerebellum, and muscle. We also discover divergent groups of 7TMICs in insects, which we term the gustatory receptor-like (Grl) proteins. Several Drosophila melanogaster Grls display selective expression in subsets of taste neurons, suggesting that they are previously unrecognized insect chemoreceptors. Although we cannot exclude the possibility of remarkable structural convergence, our findings support the origin of 7TMICs in a eukaryotic common ancestor, counter previous assumptions of complete loss of 7TMICs in Chordata, and highlight the extreme evolvability of this protein fold, which likely underlies its functional diversification in different cellular contexts.

Ligand dose-dependent activation of signaling pathways through the gustatory receptor NlGr11 linked to feeding efficacy in Nilaparvata lugens.

Insects often face both conditions with sufficient nutrients and conditions of undernutrition in the field. Through gustatory receptors, insects sense nutrients and regulate their physiological functions such as feeding and reproduction. However, it remains unclear whether signaling pathways activated by gustatory receptors depend on the concentration of nutrients and whether the difference in signaling pathways directly affects insects' physiological functions. Herein, we found that a sugar gustatory receptor, NlGr11, from the brown planthopper (BPH), Nilaparvata lugens, activated Gprotein-coupled signaling and ionotropic pathways when bound to high galactose concentration. BPHs subsequently demonstrated longer feeding times, feeding loads, and higher vitellogenin (NlVg) expression than BPHs exposed to high galactose concentrations, which only activated the ionotropic pathway. For the first time, our findings link plant nutrient conditions, signaling pathways activated by nutrients, and their gustatory receptors, and nutrient dose-dependent feeding efficacy and vitellogenin (Vg) expression in an insect. This will help us to better understand the molecular mechanism for insect feeding strategies on plants at different stages of nutritional conditions.

A chromosome-level genome assembly of the beet armyworm Spodoptera exigua

BackgroundThe beet armyworm Spodoptera exigua is a polyphagous caterpillar that causes serious damage to many species of crops and vegetables. To gain insight into how this polyphagous insect differs from less harmful oligophagous species, we generated a chromosome-level assembly and compared it to closely related species with the same or different feeding habits. ResultsBased on Illumina and Pacific Biosciences data and Hi-C technology, 425.6 Mb of genome sequences were anchored and oriented into 31 linkage groups, with an N50 length of 14.8 Mb. A total of 24,649 gene models were predicted, of which 97.4% were identified in the genome assembly. Chemosensory genes are vital for locating food: of the four main families, odorant-binding proteins, chemosensory proteins and olfactory receptors showed little difference, whereas gustatory receptors are greatly expanded in S. exigua. Examination of other polyphagous insects confirmed this difference from oligophagous congeners and further identified the bitter receptor subfamily as being particularly affected. ConclusionOur high-quality genome sequence for beet armyworm identified a key expansion of the bitter gustatory receptor subfamily in this and other pests that differs crucially from more benign relatives and offers insight into the biology and possible future means of control for these economically important insects.

Taste adaptations associated with host specialization in the specialist Drosophila sechellia.

Chemosensory-driven host plant specialization is a major force mediating insect ecological adaptation and speciation. Drosophila sechellia, a species endemic to the Seychelles islands, feeds and oviposits on Morinda citrifolia almost exclusively. This fruit is harmless to D. sechellia but toxic to other Drosophilidae, including the closely related generalists D. simulans and D. melanogaster, because of its high content of fatty acids. While several olfactory adaptations mediating D. sechellia's preference for its host have been uncovered, the role of taste has been much less examined. We found that D. sechellia has reduced taste and feeding aversion to bitter compounds and host fatty acids that are aversive to D. melanogaster and D. simulans. The loss of aversion to canavanine, coumarin and fatty acids arose in the D. sechellia lineage, as its sister species D. simulans showed responses akin to those of D. melanogaster. Drosophila sechellia has increased taste and feeding responses towards M. citrifolia. These results are in line with D. sechellia's loss of genes that encode bitter gustatory receptors (GRs) in D. melanogaster. We found that two GR genes which are lost in D. sechellia, GR39a.a and GR28b.a, influence the reduction of aversive responses to some bitter compounds. Also, D. sechellia has increased appetite for a prominent host fatty acid compound that is toxic to its relatives. Our results support the hypothesis that changes in the taste system, specifically a reduction of sensitivity to bitter compounds that deter generalist ancestors, contribute to the specialization of D. sechellia for its host.

Genome-wide identification and transcriptome-based expression pattern of chemosensory genes in two wild silkmoths,Antheraea pernyi andAntheraea yamamai

Antheraea pernyi Guérin-Méneville andAntheraea yamamai Guérin-Méneville are two closely related wild silkmoths belonging to the family Saturniidae with highly edible and silk-producing value. In this study, we characterised candidate chemosensory genes from the genomes of the two silkmoths. InA. pernyi, 38 odorant-binding proteins (OBPs), 21 chemosensory proteins (CSPs), 3 sensory neuron membrane proteins (SNMPs), 28 ionotropic receptors (IRs), 54 odorant receptors (ORs) and 53 gustatory receptors (GRs) were identified. InA. yamamai, 36 OBPs, 21 CSPs, 3 SNMPs, 30 IRs, 50 ORs and 54 GRs were identified. Phylogenetic analysis showed that the OBP, OR and GR genes were significantly expanded or contracted in the two silkmoths when compared to lepidopteran modelBombyx mori L., while the CSP genes were only expanded. The SNMP and IR genes were greatly conserved in the two silkmoths andB. mori. Most OBP, CSP, SNMP, IR and OR genes had the expression in the antennal transcriptome, but most GR genes showed no expression. This is the first study to characterise chemosensory genes of Saturniidae species in the genome and antennal transcriptome.

First chromosome scale genomes of ithomiine butterflies (Nymphalidae: Ithomiini): Comparative models for mimicry genetic studies.

The ithomiine butterflies (Nymphalidae: Danainae) represent the largest known radiation of Müllerian mimetic butterflies. They dominate by number the mimetic butterfly communities, which include species such as the iconic neotropical Heliconius genus. Recent studies on the ecology and genetics of speciation in Ithomiini have suggested that sexual pheromones, colour pattern and perhaps hostplant could drive reproductive isolation. However, no reference genome was available for Ithomiini, which has hindered further exploration on the genetic architecture of these candidate traits, and more generally on the genomic patterns of divergence. Here, we generated high-quality, chromosome-scale genome assemblies for two Melinaea species, M. marsaeus and M. menophilus, and a draft genome of the species Ithomia salapia. We obtained genomes with a size ranging from 396 to 503 Mb across the three species and scaffold N50 of 40.5 and 23.2Mb for the two chromosome-scale assemblies. Using collinearity analyses we identified massive rearrangements between the two closely related Melinaea species. An annotation of transposable elements and gene content was performed, as well as a specialist annotation to target chemosensory genes, which is crucial for host plant detection and mate recognition in mimetic species. A comparative genomic approach revealed independent gene expansions in ithomiines and particularly in gustatory receptor genes. These first three genomes of ithomiine mimetic butterflies constitute a valuable addition and a welcome comparison to existing biological models such as Heliconius, and will enable further understanding of the mechanisms of adaptation in butterflies.

The Chromosome-Level Genome of Hestina assimilis (Lepidoptera: Nymphalidae) Reveals the Evolution of Saprophagy-Related Genes in Brush-Footed Butterflies.

Most butterflies feed on nectar, while some saprophagous butterflies forage on various non-nectar foods. To date, little is known about the genomic and molecular shifts associated with the evolution of the saprophagous feeding strategy. Here, we assembled the high-quality chromosome-level genome of Hestina assimilis to explore its saprophagous molecular and genetic mechanisms. This chromosome-level genome of H. assimilis is 412.82 Mb, with a scaffold N50 of 15.70 Mb. In total, 98.11% of contigs were anchored to 30 chromosomes. Compared with H. assimilis and other Nymphalidae butterflies, the genes of metabolism and detoxification experienced expansions. We annotated 80 cytochrome P450 (CYP) genes in the H. assimilis genome, among which genes belonging to the CYP4 subfamily were significantly expanded (p < 0.01). These P450 genes were unevenly distributed and mainly concentrated on chromosomes 6-9. We identified 33 olfactory receptor (OR), 20 odorant-binding protein (OBP), and six gustatory receptor (GR) genes in the H. assimilis genome, which were fewer than in the nectarivorous Danaus plexippus. A decreased number of OBP, OR, and GR genes implied that H. assimilis should resort less to olfaction and gustation than their nectarivorous counterparts, which need highly specialized olfactory and gustatory functions. Moreover, we found one site under positive selection occurred in residue 996 (phenylalanine) of GR genes exclusive to H. assimilis, which is conservative in most lineages. Our study provides support for the adaptive evolution of feeding habits in butterflies.

Identification and expression analyses of the olfactory-related genes in different tissues' transcriptome of a predacious soldier beetle, Podabrus annulatus (Coleoptera, Cantharidae).

We sequenced and analyzed the transcriptomes from different tissues of the soldier beetle, Podabrus annulatus (Coleoptera: Cantharidae), and obtained 75.74 Gb clean reads which were assembled into 95,274 unigenes. Among these transcripts, 25,484 unigenes of highly quality were annotated. Based on annotation and tBLASTn results, we identified a total of 101 candidate olfactory-related genes for the first time, including 11 putative odorant-binding proteins (OBPs), 6 chemosensory proteins (CSP), 50 olfactory receptors (ORs), 25 gustatory receptors (GRs), 6 ionotropic receptors (IRs), and 3 sensory neuron membrane proteins (SNMPs). BLASTX best-hit results indicated that these chemosensory genes were most identical to their respective orthologs from Photinus pyralis. Phylogenetic analyses also revealed that the ORs, GRs, and IRs of Podabrus annulatus are closely related to those of Photinus pyralis. The fragment per kilobase per million mapped fragments (FPKM) values showed that the PannOBP2, PannOBP3, and PannOBP10 were predominantly expressed in the antennae, PannOBP1 in the abdomen-thorax, while others were not identified to be tissue-specific. These olfactory-related differentially expressed genes (DEGs) demonstrated different roles in the olfactory system of Podabrus annulatus. This study establishes the groundwork for future research into the molecular mechanism of olfactory recognition in Podabrus annulatus.

Sugar perception in honeybees.

Honeybees (Apis mellifera) need their fine sense of taste to evaluate nectar and pollen sources. Gustatory receptors (Grs) translate taste signals into electrical responses. In vivo experiments have demonstrated collective responses of the whole Gr-set. We here disentangle the contributions of all three honeybee sugar receptors (AmGr1-3), combining CRISPR/Cas9 mediated genetic knock-out, electrophysiology and behaviour. We show an expanded sugar spectrum of the AmGr1 receptor. Mutants lacking AmGr1 have a reduced response to sucrose and glucose but not to fructose. AmGr2 solely acts as co-receptor of AmGr1 but not of AmGr3, as we show by electrophysiology and using bimolecular fluorescence complementation. Our results show for the first time that AmGr2 is indeed a functional receptor on its own. Intriguingly, AmGr2 mutants still display a wildtype-like sugar taste. AmGr3 is a specific fructose receptor and is not modulated by a co-receptor. Eliminating AmGr3 while preserving AmGr1 and AmGr2 abolishes the perception of fructose but not of sucrose. Our comprehensive study on the functions of AmGr1, AmGr2 and AmGr3 in honeybees is the first to combine investigations on sugar perception at the receptor level and simultaneously in vivo. We show that honeybees rely on two gustatory receptors to sense all relevant sugars.

Conserved orthology in termite chemosensory gene families

Termites are eusocial insects known to use a variety of pheromones in tasks necessary for maintenance of their societies. As such, olfaction and pheromone communication in termites has been an object of intense study; trail-following pheromones (TFPs) and sex-pairing pheromones (SPPs), for example, have been identified in many termite species. In contrast, the molecular basis of olfactory detection is understudied in the group. Here, we present chemosensory genes of three species of termites belonging to three distinct lineages, Neotermes cubanus (Kalotermitidae), Prorhinotermes simplex (Rhinotermitidae), and Inquilinitermes inquilinus (Termitidae). Using antennal transcriptome screening of termite workers, we identified the chemosensory genes, which allowed us to perform phylogenetic analysis. We found a comparatively large repertoires of odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), odorant binding proteins (OBPs), chemosensory proteins (CSPs), and sensory neuron membrane proteins (SNMPs). The evolutionary analysis of termite chemosensory genes revealed Isoptera-specific expansions with a 1:1 orthologous pattern, indicating the existence of conserved olfactory functions. Our findings on basal eusocial insects will further enhance our understanding of the molecular underpinnings of eusociality and the evolution of olfactory communication in termites.

Selection and Comparative Gene Expression of Midgut-Specific Targets for Drosophila suzukii

Spotted-wing drosophila (SWD), Drosophila suzukii, is a destructive and invasive pest that attacks most small fruits and cherries. The current management for SWD involves the use of conventional insecticides. In an effort to develop a biologically based control option, the application of RNA interference (RNAi) has been investigated. To develop an RNAi approach, suitable targets must be identified, and an efficient delivery method must be developed for introducing the double-stranded RNA (dsRNA) in the midgut. In D. suzukii, we previously found that dsRNA nucleases actively degrade dsRNA molecules in the midgut. In this study, we focused on identifying biological targets focused on the midgut membrane. The profile of midgut-specific genes was analyzed and compared with the genes expressed in the whole-body using transcriptome analysis. Differential gene expression analysis revealed that 1921 contigs were upregulated and 1834 contigs were downregulated in the midgut when compared to genes from other body tissues. We chose ten midgut-specifically upregulated genes and empirically confirmed their expressions. We are particularly interested in the midgut membrane proteins, including G protein-coupled receptors (GPCRs) such as diuretic hormone 31 (DH31) receptor, neuropeptide F (NPF) recepror, toll-9, adhesion receptors, methuselah (mth), and gustatory receptor, because insect GPCRs have been offered great potential for next-generation pest management.

The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal

BackgroundTriatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation.ResultsThe sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of pickpocket receptor subfamilies IV and VII, together with clearly expanded takeout repertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2,122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) was detected.ConclusionsWe propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified may represent unknown features of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease.

A pleiotropic chemoreceptor facilitates the production and perception of mating pheromones

Optimal mating decisions depend on the robust coupling of signal production and perception because independent changes in either could carry a fitness cost. However, since the perception and production of mating signals are often mediated by different tissues and cell types, the mechanisms that drive and maintain their coupling remain unknown for most animal species. Here, we show that in Drosophila, behavioral responses to, and the production of, a putative inhibitory mating pheromone are co-regulated by Gr8a, a member of the Gustatory receptor gene family. Specifically, through behavioral and pheromonal data, we found that Gr8a independently regulates the behavioral responses of males and females to a putative inhibitory pheromone, as well as its production in the fat body and oenocytes of males. Overall, these findings provide a relatively simple molecular explanation for how pleiotropic receptors maintain robust mating signaling systems at the population and species levels.

Transcriptome analysis and identification of chemosensory genes in the larvae of Plagiodera versicolora

BackgroundIn insects, the chemosensory system is crucial in guiding their behaviors for survival. Plagiodera versicolora (Coleoptera: Chrysomelidae), is a worldwide leaf-eating forest pest in salicaceous trees. There is little known about the chemosensory genes in P. versicolora. Here, we conducted a transcriptome analysis of larvae heads in P. versicolora.ResultsIn this study, 29 odorant binding proteins (OBPs), 6 chemosensory proteins (CSPs), 14 odorant receptors (ORs), 13 gustatory receptors (GRs), 8 ionotropic receptors (IRs) and 4 sensory neuron membrane proteins (SNMPs) were identified by transcriptome analysis. Compared to the previous antennae and foreleg transcriptome data in adults, 12 OBPs, 2 CSPs, 5 ORs, 4 IRs, and 7 GRs were newly identified in the larvae. Phylogenetic analyses were conducted and found a new candidate CO2 receptor (PverGR18) and a new sugar receptor (PverGR23) in the tree of GRs. Subsequently, the dynamic expression profiles of various genes were analyzed by quantitative real-time PCR. The results showed that PverOBP31, OBP34, OBP35, OBP38, and OBP40 were highly expressed in larvae, PverOBP33 and OBP37 were highly expressed in pupae, and PverCSP13 was highly expressed in eggs, respectively.ConclusionsWe identified a total of 74 putative chemosensory genes based on a transcriptome analysis of larvae heads in P. versicolora. This work provides new information for functional studies on the chemoreception mechanism in P. versicolora.

Comparative transcriptomic assessment of the chemosensory receptor repertoire of Drosophila suzukii adult and larval olfactory organs

The spotted wing Drosophila, Drosophila suzukii, has emerged within the past decade as an invasive species on a global scale, and is one of the most economically important pests in fruit and berry production in Europe and North America. Insect ecology, to a strong degree, depends on the chemosensory modalities of smell and taste. Extensive research on the sensory receptors of the olfactory and gustatory systems in Drosophila melanogaster provide an excellent frame of reference to better understand the fundamentals of the chemosensory systems of D. suzukii. This knowledge may enhance the development of semiochemicals for sustainable management of D. suzukii, which is urgently needed. Here, using a transcriptomic approach we report the chemosensory receptor expression profiles in D. suzukii female and male antennae, and for the first time, in larval heads including the dorsal organ that houses larval olfactory sensory neurons. In D. suzukii adults, we generally observed a lack of sexually dimorphic expression levels in male and female antennae. While there was generally conservation of antennal expression of odorant and ionotropic receptor orthologues for D. melanogaster and D. suzukii, gustatory receptors showed more distinct species-specific profiles. In larval head tissues, for all three receptor gene families, there was also a greater degree of species-specific gene expression patterns. Analysis of chemosensory receptor repertoires in the pest species, D. suzukii relative to those of the genetic model D. melanogaster enables comparative studies of the chemosensory, physiology, and ecology of D. suzukii.

Bioelectronic Tongues Mimicking Insect Taste Systems for Real-Time Discrimination between Natural and Artificial Sweeteners.

A bioelectronic tongue (B-ET) mimicking insect taste systems is developed for the real-time detection and discrimination of natural and artificial sweeteners. Here, a carbon nanotube field-effect transistor (CNT-FET) was hybridized with nanovesicles including the honeybee sugar taste receptor, gustatory receptor 1 of Apis mellifera (AmGr1). This strategy allowed us to detect glucose, a major component of nectar, down to 100 fM in real time and identify sweet tastants from other tastants. It could also be utilized for the detection of glucose in dextrose tablet solutions. Importantly, we demonstrated the discrimination between natural and artificial sweeteners down to 10 pM even in real beverages such as decaffeinated coffee using our hybrid platform. In this respect, our B-ET mimicking insect taste systems can be a powerful tool for various applications such as food screening and basic studies on insect taste systems.

The oriental armyworm genome yields insights into the long-distance migration of noctuid moths.

The oriental armyworm, Mythimna separata, is known for its long-distance seasonal migration and environment-dependent phase polymorphisms. Here, we present a chromosome-level genome reference and integrate multi-omics, functional genetics, and behavioral assays to explore the genetic bases of the hallmark traits of M.separata migration. Gene family comparisons show expansion of gustatory receptor genes in this cereal crop pest. Functional investigation of magnetoreception-related genes and associated flight behaviors suggest that M.separata may use the geomagnetic field to guide orientation in its nocturnal flight. Comparative transcriptome characterizes a suite of genes that may confer the observed plasticity between phases, including genes involved in protein processing, hormone regulation, and dopamine metabolism. We further report molecular signatures that underlie the dynamic regulation of a migratory syndrome coordinating reproduction and flight. Our study yields insights into environment-dependent developmental plasticity in moths and advances our understanding of long-distance migration in nocturnal insect pests.