Neofunctionalization of a second insulin receptor gene in the wing-dimorphic planthopper, Nilaparvata lugens.
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ABSTRACT:
SUBMITTER: Xue WH
PROVIDER: S-EPMC8270448 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Nuclear factor Y (NF-Y) is a heterotrimeric transcription factor with the ability to bind to a CCAAT box in nearly all eukaryotes. However, the function of NF-Y in the life-history traits of insects is unclear. Here, we identified three NF-Y subunits, NlNF-YA, NlNF-YB, and NlNF-YC, in the wing-dimorphic brown planthopper (BPH), Nilaparvata lugens. Spatio-temporal analysis indicated that NlNF-YA, NlNF-YB, and NlNF-YC distributed extensively in various body parts of fourth-instar nymphs, and were highly expressed at the egg stage. RNA interference (RNAi)-mediated silencing showed that knockdown of NlNF-YA, NlNF-YB, or NlNF-YC in third-instar nymphs significantly extended the fifth-instar duration, and decreased nymph-adult molting rate. The addition of 20-hydroxyecdysone could specifically rescue the defect in adult molting caused by NlNF-YA RNAi, indicating that NlNF-Y might modulate the ecdysone signaling pathway in the BPH. In addition, NlNF-YA RNAi, NlNF-YB RNAi, or NlNF-YC RNAi led to small and moderately malformed forewings and hindwings, and impaired the normal assembly of indirect flight muscles. Adult BPHs treated with NlNF-YA RNAi, NlNF-YB RNAi, or NlNF-YC RNAi produced fewer eggs, and eggs laid by these BPHs had arrested embryogenesis. These findings deepen our understanding of NF-Y function in hemipteran insects.
| S-EPMC7670041 | biostudies-literature
Project description:Many insects are capable of developing two types of wings (i.e., wing polyphenism) to adapt to various environments. Though the roles of microRNAs (miRNAs) in regulating animal growth and development have been well studied, their potential roles in modulating wing polyphenism remain largely elusive. To identify wing polyphenism-related miRNAs, we isolated small RNAs from 1st to 5th instar nymphs of long-wing (LW) and short-wing (SW) strains of the brown planthopper (BPH), Nilaparvata lugens. Small RNA libraries were then constructed and sequenced, yielding 158 conserved and 96 novel miRNAs. Among these, 122 miRNAs were differentially expressed between the two BPH strains. Specifically, 47, 2, 27 and 41 miRNAs were more highly expressed in the 1st, 3rd, 4th and 5th instars, respectively, of the LW strain compared with the SW strain. In contrast, 47, 3, 29 and 25 miRNAs were more highly expressed in the 1st, 3rd, 4th and 5th instars, respectively, of the SW strain compared with the LW strain. Next, we predicted the targets of these miRNAs and carried out Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway analysis. We found that a number of pathways might be involved in wing form determination, such as the insulin, MAPK, mTOR, FoxO and thyroid hormone signaling pathways and the thyroid hormone synthesis pathway. Thirty and 45 differentially expressed miRNAs targeted genes in the insulin signaling and insect hormone biosynthesis pathways, respectively, which are related to wing dimorphism. Among these miRNAs, Nlu-miR-14-3p, Nlu-miR-9a-5p and Nlu-miR-315-5p, were confirmed to interact with insulin receptors (NlInRs) in dual luciferase reporter assays. These discoveries are helpful for understanding the miRNA-mediated regulatory mechanism of wing polyphenism in BPHs and shed new light on how insects respond to environmental cues through developmental plasticity.
| S-EPMC7767257 | biostudies-literature
Project description:BackgroundThe brown planthopper (BPH) Nilaparvata lugens (Stål) is one of the most serious insect pests of rice in Asia. However, little is known about the mechanisms responsible for the development, wing dimorphism and sex difference in this species. Genomic information for BPH is currently unavailable, and, therefore, transcriptome and expression profiling data for this species are needed as an important resource to better understand the biological mechanisms of BPH.Methodology/principal findingsIn this study, we performed de novo transcriptome assembly and gene expression analysis using short-read sequencing technology (Illumina) combined with a tag-based digital gene expression (DGE) system. The transcriptome analysis assembles the gene information for different developmental stages, sexes and wing forms of BPH. In addition, we constructed six DGE libraries: eggs, second instar nymphs, fifth instar nymphs, brachypterous female adults, macropterous female adults and macropterous male adults. Illumina sequencing revealed 85,526 unigenes, including 13,102 clusters and 72,424 singletons. Transcriptome sequences larger than 350 bp were subjected to Gene Orthology (GO) and KEGG Orthology (KO) annotations. To analyze the DGE profiling, we mainly compared the gene expression variations between eggs and second instar nymphs; second and fifth instar nymphs; fifth instar nymphs and three types of adults; brachypterous and macropterous female adults as well as macropterous female and male adults. Thousands of genes showed significantly different expression levels based on the various comparisons. And we randomly selected some genes to confirm their altered expression levels by quantitative real-time PCR (qRT-PCR).Conclusions/significanceThe obtained BPH transcriptome and DGE profiling data provide comprehensive gene expression information at the transcriptional level that could facilitate our understanding of the molecular mechanisms from various physiological aspects including development, wing dimorphism and sex difference in BPH.
| S-EPMC2997790 | biostudies-literature
Project description:BackgroundThe insect gustatory system plays a central role in the regulation of multiple physiological behaviors and the co-evolution between insects and their hosts. The gustatory receptors (Gr) are important to allow insects to sense their environment. It is critical to the selection of foods, mates and oviposition sites of insects. In this study, the Gr family genes of the brown planthopper (BPH) Nilaparvata lugens Stål (Hemiptera: Delphacidae) were identified and analyzed, and their potential relationship to the fecundity of BPH was explored by RNA interference (RNAi).ResultsWe identified 32 putative Gr genes by analyzing transcriptome and genome data from BPH. Most of these Gr proteins have the typical structure of seven transmembrane domains. The BPH Gr genes (NlGrs) were expressed in virtually all tissues and stages, whilst higher transcript accumulations were found in adult stages and in the midguts of females. Based on the phylogenic analysis, we classified NlGrs into five potential categories, including 2 sugar receptors, 2 Gr43a-like receptors, 7 CO2 receptors, 5 bitter receptors and 13 NlGrs with unknown functions. Moreover, we found that 10 NlGrs have at least two alternative splicing variants, and obtained alternative splicing isoforms of 5 NlGrs. Finally, RNAi of 29 NlGrs showed that 27 of them are related to the transcript levels of two fecundity related genes vitellogenin and vitellogenin receptor.ConclusionsWe found 32 Gr genes in BPH, among which at least 27 are required for normal expression of fecundity markers of this insect pest. These findings provide the basis for the functional study of Grs and the exploration of potential genes involved in the monophagous character of BPH.
| S-EPMC6307266 | biostudies-literature
Project description:The brown planthopper (BPH), Nilaparvata lugens, can develop into either short-winged (SW) or long-winged (LW) adults according to environmental conditions, and has long served as a model organism for exploring the mechanisms of wing polyphenism in insects. The transcription factor NlFoxO acts as a master regulator that directs the development of either SW or LW morphs, but the underlying molecular mechanism is largely unknown. Here, we microinjected SW-destined morphs with double stranded-RNA (dsRNA) targeting NlFoxO (dsNlFoxO) to change them into LW-winged morphs. In parallel, SW-destined morphs microinjected with dsRNA targeting the gene encoding green fluorescence protein (dsGfp) served as a negative control. The forewing and hindwing buds of 5th-instar nymphs collected at 24, 36, and 48 h after eclosion (hAE) were used for RNA sequencing. We obtained a minimum of 43.4 million clean reads from forewing and hindwing buds at a single developmental time. Differentially expressed genes (DEGs) were significantly enriched in various Gene Ontology (GO) terms, including cellular process, binding, and cell part. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment pathway analysis showed that up-regulated genes in dsNlFoxO-treated forewing and hindwing buds were largely associated with the cell cycle and DNA replication. Furthermore, most up-regulated genes displayed higher expression at 24-, and 36-hAE relative to 48 hAE, indicating that wing cells in LW-destined wings might actively proliferate during the first 36 h in 5th-instar nymphs. Our findings indicated that LW development in BPH was likely dependent on the duration of cell proliferation in the 5th-instar stage, which sheds light on the molecular basis of wing polymorphism in insects.
| S-EPMC8148023 | biostudies-literature
Project description:Seminal fluid proteins (SFPs) are produced mainly in the accessory gland of male insects and transferred to females during mating, in which they induce numerous physiological and post-mating behavioral changes. The brown plant hopper (BPH), Nilaparvata lugens, is an economically important hemipterous pest of rice. The behavior and physiology of the female of this species is significantly altered by mating. SFPs in hemipteran species are still unclear.We applied high-throughput mass spectrometry proteomic analyses to characterize the SFP composition in N. lugens. We identified 94 putative secreted SFPs, and the expression levels of these proteins was determined from the male accessory gland digital gene expression database. The 94 predicted SFPs showed high expression in the male accessory gland. Comparing N. lugens and other insect SFPs, the apparent expansion of N. lugens seminal fluid trypsins and carboxylesterases was observed. The number of N. lugens seminal fluid trypsins (20) was at least twice that in other insects. We detected 6 seminal fluid carboxylesterases in N. lugens seminal fluid, while seminal fluid carboxylesterases were rarely detected in other insects. Otherwise, new insect SFPs, including mesencephalic astrocyte-derived neurotrophic factor, selenoprotein, EGF (epidermal growth factor) domain-containing proteins and a neuropeptide ion transport-like peptide were identified.This work represents the first characterization of putative SFPs in a hemipeteran species. Our results provide a foundation for future studies to investigate the functions of SFPs in N. lugens and are an important addition to the available data for comparative studies of SFPs in insects.
| S-EPMC4990865 | biostudies-literature
Project description:The brown planthopper (Nilaparvata lugens Stål), the most destructive pest of rice, has been identified, including biotypes with high virulence towards previously resistant rice varieties. There have also been many reports of a yeast-like symbiont of N. lugens, but little is known about the bacterial microbes. In this study, we examined the bacterial microbes in N. lugens and identified a total of 18 operational taxonomic units (OTUs) representing four phyla (Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes) by sequencing and analyzing 16S rRNA gene libraries obtained from three populations of N. lugens, which were maintained on the rice varieties TN1, Mudgo, and ASD7. Several of the OTUs were similar to previously reported secondary symbionts of other insects, including an endosymbiont of the psyllid Glycapsis brimblecombei, an Asaia sp. found in the mosquito Anopheles stephensi, and Wolbachia, found in the mite Metaseiulus occidentalis. However, the species and numbers of the detected OTUs differed substantially among the N. lugens populations. Further, in situ hybridization analysis using digoxigenin-labeled probes indicated that OTU 1 was located in hypogastrium tissues near the ovipositor and ovary in biotype 1 insects, while OTU 2 was located in the front of the ovipositor sheath in biotype 2 insects. In addition, masses of bacterium-like organisms were observed in the tubes of salivary sheaths in rice plant tissues that the insects had fed upon. The results provide indications of the diversity of the bacterial microbes harbored by the brown planthopper and of possible associations between specific bacterial microbes and biotypes of N. lugens.
| S-EPMC2838002 | biostudies-literature
Project description:Host plant resistance has been widely used for controlling the major rice pest brown planthopper (BPH, Nilaparvata lugens). However, adaptation of the wild BPH population to resistance limits the effective use of resistant rice varieties. Quantitative trait locus (QTL) analysis was conducted to identify resistance-breaking genes against the anti-feeding mechanism mediated by the rice resistance gene Bph1. QTL analysis in iso-female BPH lines with single-nucleotide polymorphism (SNP) markers detected a single region on the 10th linkage group responsible for the virulence. The QTL explained from 57 to 84% of the total phenotypic variation. Bulked segregant analysis with next-generation sequencing in F2 progenies identified five SNPs genetically linked to the virulence. These analyses showed that virulence to Bph1 was controlled by a single recessive gene. In contrast to previous studies, the gene-for-gene relationship between the major resistance gene Bph1 and virulence gene of BPH was confirmed. Identified markers are available for map-based cloning of the major gene controlling BPH virulence to rice resistance.
| S-EPMC4071553 | biostudies-literature
Project description:Transmembrane channel-like (TMC) genes encode a family of evolutionarily conserved membrane proteins. Mutations in the TMC1 and TMC2 cause deafness in humans and mice. However, their functions in insects are is still not well known. Here we cloned three tmc genes, Nltmc3, Nltmc5, and Nltmc7 from brown planthoppers. The predicted amino acid sequences showed high identity with other species homologs and have the characteristic eight or nine transmembrane domains and TMC domain architecture. We detected these three genes in all developmental stages and examined tissues. Interestingly, we found Nltmc3 was highly expressed in the female reproductive organ especially in the oviduct. RNAi-mediated silencing of Nltmc3 substantially decreased the egg-laying number and impaired ovary development. Our results indicate that Nltmc3 has an essential role in the ovary development of brown planthoppers.
| S-EPMC7649262 | biostudies-literature
Project description:Nilaparvata lugens, the brown planthopper (BPH) sucks the rice phloem sap containing high sucrose to obtain carbon source. The comparative gene expression analyses were perfomed during feeding against starvation in order to determine sugar transporter and other feeding related gene expression.
2015-04-22 | GSE68096 | GEO