搜索结果：Insect molecular biology

Aphids are major agricultural pests that cause severe crop damage. While chemical pesticides remain the dominant control strategy, their associated environmental contamination and resistance issues necessitate the development of eco-friendly biopesticides. This study employed network pharmacology and structural biology to elucidate the molecular mechanism by which Macrolactin A protects against aphids, with validation through molecular docking, 100-ns molecular dynamics (MD) simulations, and enzymatic assays. Target prediction identified five aphid proteins as potential targets of Macrolactin A: somatostatin receptor 5 (J9JQH0), allatostatin-A receptor (J9K6V2), cyclin-dependent kinase 2 (J9JTH4), histone deacetylase Rpd3 (J9JSB6), and DNA-(apurinic or apyrimidinic) site lyase APEX-1 (J9K3U4). Molecular docking and MD simulations confirmed stable binding to all five targets, with binding free energies ranging from -43.18 to -14.12 kcal/mol. Enzymatic assays showed that APEX-1 activity was significantly suppressed in Rhopalosiphum padi and Hyalopterus amygdali after 24 h and 48 h exposure to 300 mg/L and 500 mg/L Macrolactin A. Concurrent bioassays demonstrated strong aphicidal efficacy against R. padi, with corrected mortalities reaching 76.00% and 86.67% at 48 h, respectively. Acute toxicity tests on the silkworm (Bombyx mori) and common carp (Cyprinus carpio) revealed low non-target toxicity (96-h LC50 > 500 mg/L). These findings demonstrate that network-pharmacology-based approaches can improve the accuracy of key target prediction in aphids, and provide an experimental foundation for developing Macrolactin A as an efficient and environmentally friendly microbial aphicide.

This review examines how pharmaceutical-inspired discovery logic can help revitalize insecticide innovation by integrating target-based design, chemoinformatics, and artificial intelligence into a more structured discovery pipeline. It outlines the innovation deficit in insecticide discovery and explains why pharmaceutical concepts such as validated target selection, hit-to-lead progression, multi-parameter optimization, and Design-Make-Test-Analyze cycles provide a useful conceptual model for insect-control discovery. The review evaluates established and emerging insect molecular targets, including classical neurophysiological targets and underexploited insect-selective pathways, with attention to structural tractability, ortholog-based selectivity, and resistance relevance. It further synthesizes the roles of chemoinformatics and artificial intelligence in molecular representation, virtual screening, activity prediction, structure-based design, active learning, generative design, and safety-aware optimization. Particular attention is given to the opportunities and limitations of these approaches in the context of sparse insect-specific datasets, uneven assay standardization, applicability-domain constraints, and the persistent gap between computational promise and field-usable products. The review also considers repurposing strategies, scaffold innovation, selectivity and pollinator safety, environmental sustainability, resistance-informed design, and the translational barriers that limit movement from in silico leads to deployable insecticides. Overall, the evidence suggests that the strongest future for insecticide discovery lies not in artificial intelligence alone, but in a connected discovery ecosystem that links target biology, structural insight, chemistry, predictive modeling, validation practice, and sustainability-oriented design.

Intensifying insecticide resistance in the malaria vector Anopheles gambiae poses a serious threat to the progress achieved the last decades in reducing malaria deaths in Africa. The genetic basis of insecticide resistance is often complex, involving multiple genes and mutations. However, we still lack a clear understanding of how each mechanism contributes to overall resistance and how highly resistant phenotypes arise. In this study, we generated a suite of transgenic An. gambiae strains carrying either individual mechanisms or combinations that frequently co-occur in nature. We show that co-overexpression of different detoxification enzymes (CYP6P3, CYP6M2, CYP9K1, ABCH2, GSTE2, and COEAE6G), as well as the overexpression of detoxification enzymes in the presence of target site resistance mutations, can lead to substantially greater levels of resistance. Our findings suggest that increased resistance strength is a primary driver for selection of multimechanism resistance and are transformative for the scientific insight required to design robust molecular diagnostics for timely and reliable resistance detection in the field. We further show that P450 based resistance can constitute an Achilles heel for highly resistant mosquitoes, making them more vulnerable to proinsecticides; compounds that typically require P450 activation. Our results advance our understanding of the mechanistic basis of insecticide resistance and have important implications for the design and implementation of effective and evidence-based resistance management strategies.

RNA N6-methyladenosine (m6A) modification is a pivotal post-transcriptional regulator of diverse biological processes. Despite the growing interest in insect epitranscriptomics, a systematic evaluation of research trends and hotspots remains lacking. Here, we conducted a bibliometric analysis to map the global landscape of METTL3 and m6A research in entomology over the past decade. Our results reveal a steady increase in publications, signaling a phase of rapid expansion in this field. Notably, the number of studies on METTL3 is significantly lower than that of general m6A research, suggesting that current efforts prioritize phenotypic over the mechanistic roles of core regulatory components. Keyword co-occurrence analysis identifies Bombyx mori, Locusta migratoria, and Drosophila melanogaster as the primary model systems. Research hotspots predominantly center on METTL3-mediated regulation of development, behavioral plasticity, immunity, and host-pathogen interactions. These findings highlight insect METTL3 as a burgeoning research frontier. Future studies should emphasize cross-species comparisons and the systematic dissection of regulatory networks to provide novel theoretical frameworks and molecular targets for sustainable pest management and resource insect utilization.

Gamma irradiation is one of the techniques widely authorized for the decontamination of dried herbs and spices. Its effect on the functional properties of essential oils, however, remains incompletely characterized. In this study, we examined the impact of gamma irradiation (at 5, 15, and 25 kGy) on the phytochemical composition, antimicrobial activity, antioxidant capacity, and insect-repellent activity of Cymbopogon citratus essential oil. The GC-MS analysis revealed that the citral-dominant chemotype remained stable across all irradiation doses, with geranial and neral constituting approximately 62-63% of the volatile profile. The antibacterial assays were done on five bacterial strains (Staphylococcus aureus, Bacillus subtilis, Streptococcus spp., Pseudomonas aeruginosa, and Klebsiella pneumoniae). Inhibition zones showed no statistically significant differences across irradiation doses (p ≥ 0.05), while MIC (75-100 µg/mL) and MBC (125-150 µg/mL) values remained constant across all doses. DPPH, ABTS, and FRAP antioxidant assays revealed no dose-dependent changes (DPPH IC50: 688-703 µg/mL; ABTS IC50: 18-22 µg/mL; FRAP: 505-517 µg/mL ascorbic-acid equivalents). The essential oil exhibited pronounced repellent activity (87-99%) against adult Tribolium confusum beetles at 0.125 µL/cm2, persisting for 24 h and unaffected by irradiation. Molecular docking of the major constituents (geranial, neral, geraniol, and β-myrcene) against key target proteins (3N7H, 3NVY, 4URM, and 8BN6) provided predictive support consistent with the observed activities, indicating plausible molecular interactions rather than confirmed target engagement. In silico ADME and toxicity profiling indicated favorable predicted pharmacokinetic properties and no major in silico toxicity alerts for the four modeled constituents. Taken together, these findings indicate that, under the conditions tested, gamma irradiation at food-decontamination doses produced no major shifts in composition and no statistically detectable changes in the measured bioactivities of C. citratus essential oil.

Pest insects represent a major challenge to agriculture and global food security. Existing insect control methods such as chemical insecticides are under increasing scrutiny because of their environmental impacts, and once-effective methods are facing reduced acceptance due to insect pests evolving resistance and increasing regulation. This review summarizes recent advances in transgenic approaches to insect pest control over the last five years. Transgenic crops and molecular approaches play an important role in integrated pest management strategies. Integration of gene drive and transgene-generated resistance offers new strategies for targeted pest suppression, while novel platforms for delivery of dsRNA and CRISPR have broadened the range of molecular approaches. We analyze the ethical and ecological considerations, including biosafety concerns related to species interactions and gene flow. In addition, we examine the potential and limitations of RNAi and CRISPR, including regulatory challenges and public perception of genetic engineering. Synthetic biology, precision agriculture and good risk governance are central to genetic pest control strategies. Advances at the interface of biotechnology and natural systems offer a pathway toward more sustainable and resilient agricultural practices.

Nereistoxin (NTX) and its derivative insecticides cartap and monosultap have been used for decades to control lepidopteran pests by targeting nicotinic acetylcholine receptors (nAChRs). Unlike neonicotinoid agonists that induce excitatory neurotoxicity, nereistoxin insecticides act as antagonists, blocking cholinergic neurotransmission. However, the molecular target and mechanism of action of these compounds remain incompletely understood. Here, we elucidated the mode of action of cartap and monosultap in Drosophila melanogaster through integrated genetic and computational approaches. Bioassays with Drosophila nAChR subunit mutants demonstrated that the α6 subunit is critically required for insecticidal activity of both compounds, with α6 knockout conferring approximately 10-fold resistance to monosultap and 7-fold resistance to cartap. Molecular docking of protonated NTX into an α6 homopentameric channel model revealed a "dual-anchor" blocking mechanism: the protonated amine forms electrostatic interactions with residue Glu267, while the dithiolane ring creates steric hindrance at residue Thr270. Pore diameter measurements showed an optimal binding cavity of 5.96-6.22 Å in the 267-270 region, narrowing dramatically to 1.64 Å at the deep gate (Ser278), explaining how NTX binding physically occludes the channel. Collectively, these results identify α6-containing nAChRs as the primary target of nereistoxin insecticides and provide a structural framework for understanding channel blockade, with important implications for resistance monitoring and the development of next-generation channel-blocking insecticides.

Protein N-glycosylation is a fundamental post-translational modification that shapes protein folding, stability, trafficking, and biological function. In arthropods, current understanding of N-glycosylation is largely derived from insect models, whereas chelicerates, including mites and ticks, remain poorly characterized despite their ecological and economic importance. Here, we present the first comprehensive, site-specific N-glycoproteomic analysis of a chelicerate arthropod, the two-spotted spider mite Tetranychus urticae, a globally important agricultural pest characterized by rapid development, high fecundity, extreme polyphagy, and exceptional resistance to chemical control. Using intact glycopeptide enrichment coupled with high-resolution Orbitrap LC-MS/MS, and following fragment-level validation of glycan compositions, we identified 2535 intact N-glycopeptides (glycoforms) corresponding to 815 N-glycosylation sites across 543 glycoproteins. The T. urticae N-glycome is strongly dominated by oligomannose-type glycans, which account for 89.2% of the total glycopeptide signal intensity. Notably, high-mannose structures (56.2%) are more abundant than paucimannose glycans, a pattern that contrasts with the canonical insect glycosylation paradigm. Fucosylation is comparatively modest, representing 13.5% of the total glycopeptide signal intensity, and difucosylated structures, common in insects, are rare and restricted to small core-difucosylated paucimannosidic glycans. Despite this overall simplicity, T. urticae retains the enzymatic capacity to synthesize hybrid- and complex-type N-glycans, including branched structures, indicating selective deployment of advanced glycan processing, consistent with this, orthologs of the relevant glycosyltransferases are present in the T. urticae genome. Comparative analysis with multiple insect species places T. urticae at the low-fucosylation end of the arthropod range, alongside a distinctive Man5/Man4 oligomannose signature. We hypothesize that these features may reflect an ancestral or lineage-restricted glycosylation phenotype associated with ametabolous development, although confirmation will require glycoproteomic sample of additional chelicerate species. Functional annotation reveals strong enrichment of N-glycoproteins involved in proteolysis, lipid transport and metabolism, lysosomal function, cuticle-associated processes, and acetylcholinesterase activity, linking glycosylation to key aspects of mite feeding biology, molting, rapid growth, and insecticide resistance. Together, the present study establishes a foundational, site-specific N-glycoproteomic resource for Acari, expands current understanding of arthropod glycan evolution, and provides a molecular framework for exploring glycosylation-dependent mechanisms underlying mite development, host-plant interactions, and resistance to chemical control.

Entomopathogenic fungi (EPF) are well established as biological control agents, but their emerging role as endophytes reveals a broader and more powerful function in crop protection. By colonizing plant tissues, endophytic entomopathogenic fungi (EEPF) create a dynamic tripartite interaction between plants, fungi, and herbivores, enabling systemic, plant-mediated pest suppression. This review synthesizes current knowledge on the behavioral and ecological responses of herbivorous arthropods to EEPF-colonized plants, with an emphasis on the mechanisms and implications for integrated pest management (IPM). Growing evidence indicates that EEPF consistently modify herbivore behavior and performance across diverse crops and insect taxa. Colonization frequently alters feeding, host selection, and oviposition, often deterring pests, although mediated responses may vary among fungal species, host plants, insect taxa, and environmental conditions. These responses are driven by EEPF-induced changes in plant chemistry, including shifts in volatile organic compounds (VOCs) and defensive metabolites. In parallel, EEPF impair insect fitness by delaying development, reducing survival, and lowering fecundity, thereby suppressing pest populations. These plant-mediated and behavioral changes extend to multitrophic interactions, potentially affecting associations with natural enemies and the transmission efficiency of some insect vectors of plant viruses. Despite rapid progress, critical gaps remain in resolving the mechanistic basis of these interactions and their stability under field conditions. Advancing the application of EEPF will require integrated approaches combining microbial ecology, chemical ecology, and insect behavioral biology. Harnessing these interactions offers a compelling pathway to reduce reliance on synthetic pesticides while enhancing the resilience and sustainability of agricultural systems.

Juvenile hormone (JH) analog insecticides are widely used in pest management because of their ability to disrupt insect growth and metamorphosis; however, the molecular mechanisms linking endocrine disruption to metabolic dysregulation remain incompletely understood. In addition to their established roles in diapause and developmental regulation, JH signaling pathways have also been implicated in carbohydrate and lipid metabolism. In the present study, we investigated the effects of two JH analogs, pyriproxyfen and hydroprene, on the migratory locust, Locusta migratoria, with particular emphasis on lipid metabolic regulation and the function of midgut-enriched fatty acid-binding protein gene (Mg-FABP). Bioassays were performed to evaluate insecticidal activity, and transcriptomic analyses were conducted to identify differentially expressed genes associated with endocrine signaling and lipid metabolism. Functional characterization of Mg-FABP was further performed using RNA interference (RNAi) and Oil Red O staining assays. In addition, the tertiary structure of LmMg-FABP was predicted using AlphaFold 3, and molecular docking analyses were carried out to investigate its interactions with fatty acid ligands. Both pyriproxyfen and hydroprene caused approximately 70% mortality in locust nymphs and induced significant transcriptional changes in pathways related to hormone signaling and lipid metabolism. Transcriptomic analysis revealed pronounced downregulation of Mg-FABP following JH analog exposure. RNAi-mediated silencing of Mg-FABP significantly reduced lipid droplet accumulation in the fat body, indicating that Mg-FABP plays an essential role in lipid transport and metabolic homeostasis in L. migratoria. Structural analyses further demonstrated that LmMg-FABP possesses a conserved tertiary structure highly similar to FABP homologs from other insect species. Molecular docking identified key amino acid residues involved in fatty acid binding and suggested that hydrophobic interactions are critical for ligand stabilization within the binding cavity. Collectively, our findings demonstrate that pyriproxyfen and hydroprene disrupt insect development not only through endocrine imbalance but also through perturbation of Mg-FABP-associated lipid metabolic pathways. This study provides new mechanistic insight into the coordinated interaction between hormonal signaling and lipid metabolism during JH analog exposure and identifies FABP-mediated lipid transport as a potential molecular target for the development of more selective insect growth regulators.

Ascoviruses, as obligate insect pathogens that exclusively infect lepidopteran hosts, are highly reliant on the precise modulation of key host physiological processes, including metabolism, developmental signaling, and immune homeostasis, to facilitate successful infection, subsequent viral replication and transmission. The corazonin signaling pathway serves as a key regulatory pathway in insect development and molting. Herein, we found that ascoviruses modulate the Corazonin signaling pathway to affect the host molting process, thereby influencing viral replication. Therefore, understanding the molecular mechanisms between ascovirus and the corazonin signaling pathway is of particular importance. In this study, we found that corazonin (HaCrz) and the receptor (HaCrzR) were essential for promoting the molting process in response to HvAV infection. Silencing of HaCrz or HaCrzR via RNAi extended larval instar stages, elevated host mortality, reduced transcript levels of downstream molting-related genes (HaTH and HaDDC), and substantially enhanced viral replication. In contrast, exogenous injection of synthetic mature HaCrz peptide, which interacts structurally with HaCrzR as validated by molecular docking, accelerated host molting and improved antiviral responses. These findings not only revealed the mechanism by which viruses manipulate the host molting process but more importantly, demonstrated that viruses create favorable conditions for viral replication and transmission by interfering with host developmental behaviors.

Development, physiology, and reproduction in insects require juvenile hormones (JHs). Given these essential functions, the availability of these potent small molecules is tightly controlled by synthesis, transportation, and degradation. Insects possess two classes of enzymes to degrade JHs: the canonically extracellular JH esterases (JHEs) and intracellular JH epoxide hydrolases (JHEHs). While the biochemical activities of JHEs and JHEHs have been investigated in over sixty insect species in the last fifty years, functional studies have been hindered, until recently, by extensive genetic redundancies. This review highlights how increased availability of 'omics datasets and advances in genetic manipulation have revealed novel and sometimes unexpected insights into the functions of each class of JH degradation enzymes during development and beyond. These studies provide the tools and framework to not only answer many longstanding questions regarding where, when and how each JH degradation enzyme regulates JH availability, but also hold promise to reveal the molecular mechanisms by which JHs impart diverse functions across development.

Drosophila melanogaster, widely known as the fruit fly, has emerged as a pivotal model organism for studying development and signaling transduction. Its fully sequenced genome, short generation time, and powerful genetic toolkit-including the Gal4/UAS system, RNA interference, and CRISPR-Cas9-enable precise, tissue-specific manipulation and high-throughput functional analyses. Despite differences in anatomy, the internal organ systems of Drosophila melanogaster, including the nervous system, heart, fat body, oenocytes, and nephrocytes, exhibit conserved molecular pathways and physiological functions comparable to those of humans. The morphological differences between invertebrates and vertebrates have long led researchers to undervalue the studies of insects in underlying the pathogenesis of human diseases. Over the past decades, the fruit fly has been widely validated for modeling the pathogenesis of neurodegenerative, cardiovascular, metabolic, renal, and muscular disorders. In this review, we systematically summarize the conserved molecular pathways and organ functions between the fruit fly and human, and provide examples of recent studies that use the fruit fly as a model system to answer questions associated with human diseases. We also discuss how Drosophila help researchers to fulfill the gap from mechanistic study toward translational research, and provide methodological considerations regarding the utility of Drosophila models in drug screening.

Rhabdoviridae includes many viruses, among which rabies virus is notable. Other genera in this family can infect mammals, birds, reptiles, fish, and plants. Between October 2022 and July 2023, mosquitoes were collected from some municipalities in the Córdoba and Cesar departments, Colombian Caribbean. Pools were formed according to taxonomic identification and geographic area. RNA was extracted, and sequencing was performed using MGI-G50 platform. Bioinformatics analyses were performed using the Galaxy platform and the Diamond-MEGAN program. The MAFFT program was used for sequence alignment. The Prokka program was used for genome annotation, IQ-TREE was used for phylogenetic reconstruction, and iTOL was used to visualize and edit the tree. The Clustal Omega program of the European Molecular Biology Laboratory (EMBL-EBI) was used to construct a percent similarity matrix, and Unipro UGENE was used to align the amino acids of the L protein with the conserved consensus sequence (GDNQ). Two new genomes showing high similarity to Almendravirus arboretum (ABTV), and Almendravirus chico (RCHV) were identified in a single pool of Johnbelkinia ulopus mosquitoes collected in Córdoba. Additionally, a third genome with a low similarity percentage to the L segment of the Almendravirus menghai (MRV) from China was detected in Anopheles apicimacula from Cesar. This is the first study in Colombia that reports the ABTV and RCHV in Jb. ulopus mosquitoes and the first report of a phylogenetically similar sequence to the MRV, which could be a new virus of the Rhabdoviridae family.

Squash leaf curl China virus (SLCCNV) is an important geminivirus that infects cucurbit crops and is widely distributed across Asia. To elucidate its population structure and molecular evolution, 101 DNA-A and 67 DNA-B strain sequences of SLCCNV that were publicly available from 2001 to 2024 were analyzed. The strains clustered into three major geographic clades, including South Asia, the Malay Archipelago, and Mainland Southeast Asia. Recombination analysis revealed breakpoints mainly concentrated in the AC2 and BC1 regions. Signals of positive selection were indicated for AC4 and AC5 by selection pressure analysis. Significant genetic differentiation among SLCCNV populations from different geographic origins, but frequent gene flow was observed between among populations from South Asia, the Malay Archipelago, and Mainland Southeast Asia. In addition, AC5 and AV2 exhibited high variability at both the nucleotide and amino acid levels, while AC1, AC2, and AC3 were relatively conserved. Collectively, the evolutionary dynamics of SLCCNV are shaped by geographic isolation, recombination events, and differential selection pressures. This study provides important insights into the molecular evolution of SLCCNV and offers valuable guidance for region-specific surveillance, quarantine strategies, and the deployment of durable resistance against emerging viral variants.

The striped mealybug, Ferrisia virgata (Cockerell), is a destructive invasive pest infesting more than 234 genera across 83 families and established in over 122 countries, posing serious threats to agriculture and forestry. To clarify the drivers governing the distribution and future dispersal risk, this study employed a Maximum Entropy (MaxEnt) model to conduct its global potential distribution under current and future climate scenarios, incorporating climate and topographic variables. The established models demonstrated strong reliability and accuracy, with an average AUC of 0.903, a mean TSS of 0.705, and only 17.08% of the total suitable habitats classified as extrapolation areas. The temperature-related variables (85.2%) were the dominant variables shaping the current potential distribution model, followed by precipitation-related variables (13.5%), while the contribution of elevation contributed only 1.3%. The current potential distribution of this pest mainly concentrated in North America, South America, Africa, Oceania, and Asia. Under future climate scenarios, the suitable habitats of F. virgata exhibited divergent invasion risks, and low-emission climate pathways could constrain the pest's long-term suitable ranges. We put forward three targeted strategies for prevention and control, existing-area governance, forward-looking early warning, and cross-regional coordinated prevention. Our findings clarify the key role of thermal conditions in driving the dispersal of F. virgata and propose targeted control strategies, thereby offering a scientific basis for the early warning and precise management of congeneric invasive insects.

Insects that pollinate essential crops are frequently exposed to neurotoxic insecticides. Although most pollinators belong to insect lineages that diverged hundreds of millions of years ago, insecticide safety tests focus on a few model bee species. Here, we used comparative whole-brain transcriptomics to test whether sulfoxaflor and clothianidin elicit similar or distinct responses across four phylogenetically diverse pollinators: Bombus terrestris, Osmia bicornis, Lucilia sericata, and Vanessa cardui. Within each species, both insecticides produce broadly similar gene regulatory profiles, with more than 70% of differentially expressed genes shared. By contrast, transcriptional responses differed sharply across species, with no shared genes or pathways consistently disrupted. Unexpectedly, sulfoxaflor, promoted as a "bee-safe" alternative, provokes broader gene regulatory changes in non-bee species than clothianidin, a restricted neonicotinoid. Our findings reveal extensive transcriptional divergence in insecticide responses across pollinators, suggesting that risk assessments would benefit from greater phylogenetic diversity and novel molecular approaches.

Careful dissection of insect gut tissues is essential for microbiome studies to ensure accurate characterization of internal microbial communities and preservation of DNA integrity. Because insect-associated microbiomes are highly sensitive to contamination, effective removal of external microbes prior to dissection is critical to minimize bias in downstream analyses. While ethanol- and bleach-based surface sterilization methods are commonly used, standardized workflows integrating field collection, sterilization, and dissection remain limited. Here, we present a step-by-step protocol for the field collection, surface sterilization, and dissection of gut tissues from the agricultural pest Diaprepes abbreviatus (Coleoptera: Curculionidae), optimized for genomic DNA extraction and microbiome analyses. Using wild-caught specimens, this workflow incorporates a rigorous surface sterilization and dissection strategy that minimizes external contamination while preserving biologically relevant microbial signatures and DNA integrity for downstream microbiome analyses. The protocol provides a standardized framework for insect gut microbiome studies and can be broadly adapted to other wild-caught insect species requiring careful collection, disinfection, and sterile dissection prior to molecular analysis. The protocol integrates field collection and laboratory processing steps into a streamlined workflow that minimizes contamination while preserving tissue integrity for downstream applications. Key features • Designed for wild-caught Diaprepes abbreviatus collected directly from agricultural host trees, this protocol can also be adapted for other insect species. • Integrates field collection, surface sterilization, and sterile gut dissection into a single workflow to minimize contamination. • Sequential ethanol and diluted bleach treatment effectively removes external microbes prior to dissection. • Enables isolation of intact gut tissues suitable for high-quality DNA extraction and downstream microbiome sequencing.

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