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Omoto, C.

Publications and source records attributed to Omoto, C..

9 recordsLinked to original sources

A shared molecular target hides distinct genetic routes to diamide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae)

Diamide insecticides target insect ryanodine receptors (RyRs) and are widely used against lepidopteran pests, yet it remains unclear whether compounds sharing this molecular target evolve resistance through the same genetic routes. Here, we integrated RyR sequencing, structural modelling and population genomics to investigate resistance to chlorantraniliprole and flubendiamide in the global agricultural pest Helicoverpa armigera. We identified G4946E together with F4947I, a previously undescribed resistance-associated RyR substitution, in a chlorantraniliprole-resistant strain. Structural modelling indicated that F4947I may modify G4946E's effects on the diamide-binding pocket, while field and population-genomic evidence independently implicated the RyR-containing chromosome 28 region in chlorantraniliprole resistance. By contrast, high-level flubendiamide resistance occurred without amino acid substitutions in the RyR region examined, and field survival was predominantly associated with chromosome 2, independently recapitulating a previously identified resistance locus. Together, our findings reveal that resistance to insecticides sharing the same molecular target can evolve through distinct but potentially overlapping genetic routes, highlighting the limitations of predicting cross-resistance from target-site variation alone and the need for broader genomic approaches to resistance surveillance.

molecular biology↗

The collision of two genomes threatens global food security

Human activity alters selection pressures and redistributes biodiversity, creating opportunities for hybridization when dilerent species come into secondary contact. It is now well-established that ancient hybridization plays an important role in adaptive radiation 1, but its role in recent anthropogenic adaptation remains unclear. We investigated this in a study of hybridizing native and invasive Helicoverpa moths in Brazil, which are among the most economically damaging crop pests globally. Native H. zea has recently evolved Bt resistance and is better adapted to maize as a host plant, while invasive H. armigera is resistant to pyrethroid pesticides and is better adapted to soybean. Using a decade-long time series of 975 genomes from both species, we demonstrate rapid, bidirectional adaptive introgression of structural variants that cause resistance to two distinct pesticides. In one direction, a pyrethroid resistance gene from H. armigera (CYP337B3) is now almost fixed in native H. zea. In the other direction, ~30% of recently-sampled invasive H. armigera carry a H. zea-derived trypsin repeat cluster. Using controlled crosses, we show that this trypsin repeat cluster confers resistance to Bt (Cry1Ac) soy in the H. armigera genomic background. Thus, hybridization has combined H. armigera adaptation to soy with H. zea Cry1Ac resistance to facilitate exploitation of Brazilian Bt soy monoculture -- a vast anthropogenic habitat exceeding the area of Germany. Our results show that the combinatorial mechanisms that produce biodiversity can also drive rapid anthropogenic adaptation on ecological timescales, with consequences for global food security.

evolutionary biology↗

The genetic architecture of resistance to flubendiamide insecticides in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

Insecticide resistance is a major problem in food production, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is a globally distributed crop pest affecting over 300 crop species. H. armigera has rapidly evolved insecticide resistance, making it one of the most damaging pests worldwide. Understanding the genetic basis of insecticide resistance provides insights to develop tools, such as molecular markers, that can be used to slow or prevent the evolution of resistance. We explore the genetic architecture of H. armigera resistance to a widely used insecticide, flubendiamide, using two complementary approaches: genome-wide association studies (GWAS) in wild-caught samples and quantitative trait locus (QTL) mapping in a controlled cross of susceptible and resistant laboratory strains. Both approaches identified one locus on chromosome 2, revealing two SNPs within 976 bp that can be used to monitor field resistance to flubendiamide. This was the only region identified using linkage mapping, though GWAS revealed additional sites associated with resistance. Other loci identified by GWAS in field populations contained known insecticide detoxification genes from the ATP-binding cassette family, ABCA1, ABCA3, ABCF2 and MDR1. Our findings revealed an oligogenic genetic architecture, in contrast to previous reports of monogenic resistance associated with the ryanodine receptor. This work elucidates the genetic basis of rapidly evolving insecticide resistance and will contribute to the development of effective insecticide resistance management strategies. Author summaryInsecticide resistance in agricultural pests challenges food security, environmental sustainability, and human health. The cotton bollworm Helicoverpa armigera is resistant to various insecticide classes as well as Bacillus thuringiensis toxins. Understanding the genetic basis of this resistance is crucial for developing effective insecticide resistance management (IRM) strategies. Our study investigated the genetic architecture of resistance of H. armigera to flubendiamide and identified SNPs associated with resistance. We used two approaches: association mapping in wild-derived samples and QTL mapping in a controlled backcross of susceptible and resistant laboratory strains. One specific region on chromosome 2 was found in both GWAS and QTL mapping analysis and showed significant potential as a PCR-based marker for monitoring resistance to flubendiamide in H. armigera. Additionally, the GWAS identified five more SNPs in the field populations. The candidate genes identified are primarily associated with insecticide detoxification mechanisms and calcium homeostasis. Our study advances the understanding of the complex genetic architecture of flubendiamide resistance in H. armigera, providing valuable tools for IRM programs and establishing a basis for future studies.

genetics↗

Genome-wide exploration of metabolic-based pyrethroid resistance mechanism in Helicoverpa armigera

To elucidate the deltamethrin resistance mechanism in Helicoverpa armigera, we explored mutations at the deltamethrin target site, genomic level variations between insecticide-susceptible and -resistant strains, and differences in gene expression patterns between the strains. Known pyrethroid resistance-associated point mutations within the voltage-gated sodium channel were undetected in the cDNA and gDNA of resistant strains or field populations. The whole-genome de novo assembly of a Korean resistant strain was performed (GCA_026262555.1), and 13 genomes of susceptible and resistant individuals were re-sequenced using field populations. Approximately 3,369,837 variants (SNPs and indels) were compared with our reference H. armigera genome, and 1,032,689 variants were identified from open reading frames. A resistance-specific CYP3 subfamily gene with five variants (CYP321A1v1-v5) was identified in the resistant strains, indicating the potential role of these variants in resistance. RNA-seq analysis identified 36,720 transcripts from 45 Illumina RNA-seq datasets of the fat body, gut, and the rest of the body. Differential gene expression analysis revealed some differently overexpressed detoxification enzyme genes in the resistant strains, particularly cytochrome P450 genes. This finding was consistent with the results of bioassay tests using PBO-based synergists, further supporting the role of detoxification enzymes in resistance. Therefore, H. armigera may acquire deltamethrin resistance through a combination of actions, including the overexpression of various detoxification enzymes, such as CYP3 subfamilies (CYP321A5) and cuticular proteins. The five variants of CYP321A subfamily identified in this study may serve as a basis for understanding insecticide resistance at the molecular level and can be applied as diagnostic markers for resistance. Key MessagesO_LIKnown resistance-related mutations were undetected in all the resistant strains or field populations. C_LIO_LINo specific resistance-associated variations were identified at the genomic level. C_LIO_LIThe expression pattern of the CYP3 subfamily genes was strongly correlated with the level of resistance. C_LIO_LIGenes other than CYP337B3 are also involved in the development of high-level resistance. C_LIO_LIResistance developed as a result of changes in the expression of detoxification genes rather than target site modification through mutation. C_LI

ecology↗

Transcriptomic investigation of the molecular mechanisms underlying resistance to the neonicotinoid thiamethoxam and the pyrethroid lambda-cyhalothrin in Euschistus heros (Hemiptera: Pentatomidae)

Strains of Euschistus heros (Hemiptera: Pentatomidae) with resistance to thiamethoxam (NEO) and lambda-cyhalothrin (PYR), generated by selection with these insecticides in the laboratory, have been recently reported in Brazil. However, the mechanisms conferring resistance to these insecticides in E. heros remain unresolved. We utilized comparative transcriptome profiling and single nucleotide polymorphism (SNP) variant calling of susceptible and laboratory-selected resistant strains of E. heros to investigate the molecular mechanism(s) underlying resistance. The E. heros transcriptome was assembled using approximately 190.1 million paired-end reads, which generated 91,673 transcripts with a mean length of 720 bp and N50 of 1795 bp. Approximately, 54.8% of the assembled transcripts ware functionally annotated against the NCBI nr database, with most sequences (43%) being similar to the pentatomids Halyomorpha halys (43%) and Nezara viridula (29%). Comparative gene expression analysis between the susceptible (SUS) and NEO strains identified 215 significantly differentially expressed (DE) transcripts. DE transcripts associated with the metabolism of xenobiotics were all up-regulated in the NEO strain. The comparative analysis of the SUS and PYR strains identified 204 DE transcripts, including an esterase (esterase FE4), a glutathione-S-transferase, an ABC transporter (ABCC1), and aquaporins that were up-regulated in the PYR strain. We identified 9,588 and 15,043 non-synonymous SNPs in the PYR and NEO strains respectively in comparisons with the SUS strain. One of the variants (D70N) detected in the NEO strain occurs in a subunit (5) of the nicotinic acetylcholine receptor, the target-site of neonicotinoid insecticides. Nevertheless, the position of this residue was found very variable among 5 from insect species. In conclusion, neonicotinoid and pyrethroid resistance in laboratory-selected strains of E. heros is associated with a potential metabolic resistance mechanism mediated by the overexpression of several proteins commonly involved in the three phases of xenobiotic metabolism. Together these findings provide insight into the potential basis of resistance in E. heros and will inform the development and implementation of resistance management strategies against this important pest. HighlightsO_LI419 DE genes were observed in E. heros insecticide-resistant strains C_LIO_LI24,631 SNPs were identified in E. heros insecticide-resistant strains C_LIO_LIE. heros insecticide-resistant strains overexpress metabolic resistance genes C_LIO_LILambda-cyhalothrin-resistant E. heros overexpresses cuticular proteins C_LIO_LIThiamethoxam-resistant E. heros carries the target-site mutation D70N in nAChRalpha5 C_LI

physiology↗

Host plant affects the larval gut microbial communities of the generalist herbivores Helicoverpa armigera and Spodoptera frugiperda

Investigations on symbiotic associations between Lepidoptera and bacteria have been inconclusive as to whether these microorganisms represent transient or persistent associations. One reason for this is that most studies have sampled the microbiota from only a few species and frequently from laboratory-reared animals. We sequenced the 16S rRNA gene to profile the gut microbiome of the field collected, agricultural pests Helicoverpa armigera and Spodoptera frugiperda. We found that variation in the structure of bacterial communities is in great part associated with their host diet. Moreover, Enterococcus, among a few other taxa, is consistently present in all samples regardless of the plant hosts were collected. The larval gut bacteria composition matches previously published data in the same or related species, indicating that associations with bacteria taxa such as Enterococcus are persistent despite geographical variation and sampling techniques. Based on our phylogenetic analysis it is not clear, however, if Enterococci associated with Lepidoptera are necessarily different from environmental bacteria. We conclude that to fully understand the nature of Lepidoptera - gut bacteria associations it will be necessary to conduct larger sampling efforts and combine them with identification methods of bacterial strains that go beyond screening of the 16S rRNA gene.

microbiology↗

Fitness costs associated with spinetoram resistance in Spodoptera frugiperda is driven by host plants

Insecticide resistance is usually associated with fitness costs. The magnitude of fitness costs is affected by environmental and ecological factors. Here, we explored how host plants could affect fitness costs associated with insecticide resistance. Initially, spinetoram-resistant (RR) and susceptible (SS) strains of Spodoptera frugiperda were selected using F2 screen from a population collected in Sao Desiderio, Bahia State, Brazil in 2018. Besides de RR and SS strains, fitness costs were also assessed for a heterozygous strain (RS). Life-history traits were evaluated to estimate population growth parameters of neonate larvae of each strain fed on corn, soybean and cotton plants. Compared to the SS strain, the relative fitness of the RR strain, based on intrinsic rate of population increase, was 1.06, 0.84 and 0.67 on plants of corn, soybean and cotton respectively. The relative fitness of the RS strain was similar to the SS strain regardless the host plant, suggesting a recessive fitness cost. No differences were found between the strains fed on corn plants. The larval development time was greater for RR strain fed on soybean and cotton plants compared to RS and SS strain. Low survival rate and fecundity of the RR strain were found when larvae fed on plants of soybean and cotton. The results of this study demonstrated that fitness costs of spinetoram resistance in S. frugiperda depend strongly on the host plants that S. frugiperda larvae fed on. Such information can be used to design resistance management strategies considering the host plants of the agricultural landscape. Key messagesO_LIThe presence of fitness costs associated with resistance can be exploited in resistance management strategies. C_LIO_LIHost plant influences the fitness costs associated with spinetoram resistance in S. frugiperda. C_LIO_LIInformation considering the host plants in an agricultural landscape is essential to design effective resistance management programs. C_LI

evolutionary biology↗

Susceptibility monitoring and the molecular characterization of resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to lambda-cyhalothrin and chlorpyrifos

Spodoptera frugiperda (J. E. Smith) is a serious and widespread agricultural pest with several records of resistance to different insecticides and Bt proteins, including the neurotoxic insecticides chlorpyrifos (organophosphate) and lambda-cyhalothrin (pyrethroid). In this study, we (i) characterized and monitored the susceptibility of field populations of S. frugiperda to chlorpyrifos (194 populations) and lambda-cyhalothrin (197 populations) collected from major maize-growing regions of Brazil from 2003 to 2016, and (ii) compared gene expression levels of chlorpyrifos- and lambda-cyhalothrin-resistant strains to a susceptible reference strain (Sf-ss) of S. frugiperda. Laboratory-guided assays to monitor larval susceptibility detected average survival ranging from 29.3% to 36.0% to chlorpyrifos, and 23.1% to 68.0% to lambda-cyhalothrin at diagnostic concentration, based on LC99 of the susceptible reference strain of each insecticide. The resistance ratio of the chlorpyrifos-resistant strain (Clo-rr) was 25.4-fold and of the lambda-cyhalothrin-resistant strain (Lam-rr) was 217-fold. Differential gene expression analyses between resistant vs susceptible strains identified 1,098 differentially expressed genes (DEGs) between Clo-rr and Sf-ss, and 303 DEGs between Lam-rr and Sf-ss. Functional analyses of the DEGs revealed the up-regulation of several detoxification enzymes, mainly cytochrome P450 belonging to the CYP3 and CYP6 clans. Genes associated with regulatory processes, such as the forkhead box O (FoxO) were also up-regulated. Our data points that the resistance mechanisms of Clo-rr and Lam-rr strains of S. frugiperda to chlorpyrifos and lambda-cyhalothrin are mainly mediated by enzyme detoxification.

zoology↗

There is more than chitin synthase in insect resistance to benzoylureas: Molecular markers associated with teflubenzuron resistance in Spodoptera frugiperda

Chitin synthesis inhibitors are successfully used in pest control and are an excellent option for use in integrated pest management programs due to their low non-target effects. Reports on field-evolved resistance of lepidopteran pests to chitin synthesis inhibitors and the selection of laboratory resistant strains to these products require a detailed investigation on the resistance mechanisms and on the identification of molecular markers to support the implementation of efficient monitoring and resistance management programs. Teflubenzuron is a chitin synthesis inhibitor highly effective in controlling lepidopteran pests, including nowadays the world widely distributed fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith, 1797) (Lepidoptera: Noctuidae). We report the selection of a laboratory strain of S. frugiperda resistant to teflubenzuron, and its use for the characterization of the inheritance of resistance, evaluation of cross-resistance to other chitin-synthesis inhibitors and the identification of a set of single nucleotide polymorphisms (SNPs) for use as candidate molecular markers for monitoring the evolution of resistance of S. frugiperda to teflubenzuron. The resistance of the selected strain of S. frugiperda to teflubenzuron was characterized as polygenic, autosomal, and incompletely recessive. The resistance ratio observed was nearly 1,365-fold. Teflubenzuron-resistant strain showed some cross-resistance to lufenuron and novaluron but not to chlorfluazuron. We also detected a set of 72 SNPs that could support monitoring of the resistance frequency to teflubenzuron in field populations. Our data contribute to the understanding of the resistance mechanisms and the inheritance of polygenic resistance of S. frugiperda to benzoylureas. We also contribute with candidate markers as tools for monitoring the emergence and spread of teflubenzuron resistance in S. frugiperda.

evolutionary biology↗