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Functional characterization of sex pheromone receptors in Spodoptera frugiperda, S. exigua, and S. litura moths

Insect Science 2023年第2期30卷 305-320页

作者： Sai Zhang Fang Liu Bin Yang Yang Liu Gui-Rong Wang State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant ProtectionChinese Academy of Agricultural SciencesBejingChina College of Horticulture and Plant Protection Yangzhou UniversityYangzhouChina Shenzhen Branch Guangdong Laboratory for Lingnan Modern AgricultureGenome Analysis Laboratory of the Ministry of AgricultureAgricultural Genomics Institute at ShenzhenChinese Academy of Agricultural SciencesShenzhenChina

Moths possess an extremely sensitive and diverse sex pheromone processing system,in which pheromone receptors(PRs)are essential to ensure communication between mating partners.Functional properties of some PRs are conserved among species,which is important for reproduction.However,functional differentiation has occurred in some homologous PR genes,which may drive species divergence.Here,using genome analysis,17 PR genes were identified from Spodoptera frugiperda,S.exigua,and S.litura,which belong to 6 homologous groups(odorant receptor[OR]6,11,13,16,56,and 62);of which 6 PR genes(OR6,OR11,OR13,OR16,OR56,and OR62)were identified in S.frugiperda and S.exigua,and 5 PR genes were identified in S.litura,excluding OR62.Using heterologous expression in Xenopus oocytes,we characterized the functions of PR orthologs including OR6,OR56,and OR62,which have not been clarified in previous studies.OR6 orthologs were specifically tuned to(Z,E)-9,12-tetradecadienyl acetate(Z9,E12-14:OAc),and OR62 orthologs were robustly tuned to Z7-12:OAc in S.frugiperda and S.exigua.The optimal ligand for OR56 was Z7-12:OAc in S.frugiperda,but responses were minimal in S.exigua and S.litura.In addition,SfruOR6 was male antennae-specific,whereas SfruOR56 and SfruOR62 were male antennae-biased.Our study further clarified the functional properties of PRs in 3 Spodoptera moth species,providing a comprehensive understanding of the mechanisms of intraspecific communication and interspecific isolation in Spodoptera.

关键词： pheromone pheromone receptor Spodoptera Xenopus oocytes

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The expression of Spodoptera exigua P450 and UGT genes: tissue specificity and response to insecticides

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Insect Science 2019年第2期26卷 199-216页

作者： Bo Hu Shu-Heng Zhang Miao-Miao Ren Xiang-Rui Tian Qi Wei David Kibe Mburu Jian-Ya Su Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education) College of Plant Protection Nanjing Agricultural University Nanjing China

Cytochrome P450 and UDP-glucosyltransferase (UGT) as phase I and phase II metabolism enzymes, respectively, play vital roles in the breakdown of endobiotics and xenobiotics. Insects can in crease the expression of detoxificatio n enzymes to cope with the stress from xenobiotics including insecticides. However, the molecular mechanisms for insecticide detoxification in Spodoptera exigua remain elusive, and the genes conferring insecticide metabolisms in this species are less well reported. In this study, 68 P450 and 32 UGT genes were identified. Phylogenetic analysis showed gene expansions in CYP3 and CYP4 clans of P450 genes and UGT33 family of this pest. P450 and UGT genes exhibited specific tissue expression patterns. Insecticide treatments in fat body cells of S. exigua revealed that the expression levels of P450 and UGT genes were significantly influenced by challenges of abamectin, lambda-cyhalothrin, chlorantraniliprole, metaflumizone and indoxacarb. Multiple genes for detoxification were affected in expression levels after insecticide exposures. The results demonstrated that lambda-cyhalothrin, chlorantraniliprole, metaflumizone and indoxacarb induced similar responses in the expression of P450 and UGT genes in fat body cells;eight P450 genes and four UGT genes were co-up-regulated significantly, and no or only a few CYP/UGT genes were down-regulated significantly by these four insecticides. However, abamectin triggered a distinct response for P450 and UGT gene expression;more P450 and UGT genes were down-regulated by abamectin than by the other four compounds. In con elusion, P450 and UGT genes from S. exigua were identified, and different responses to abamectin suggest a different mechanism for insecticide detoxification.

关键词： abamectin cytochrome P450 monooxygenases gene expression insecticide Spodoptera exigua UDP-glycosyltransferase

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Identification and functional characterization of doublesex gene in the testis of Spodoptera litura

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Insect Science 2019年第6期26卷 1000-1010页

作者： Qian Du Liang Wen Si-Chun Zheng Hong-Lun Bi Yong-Ping Huang Qi-Li Feng Lin Liu Guangzhou Key Laboratory of Insect Development Regulation and Applied Research Institute of Insect Science and Technology School of Life Sciences South China Normal University GuangzhouChina Key Laboratory of Insect Developmental and Evolutionary Biology Institute of Plant Physiology and Ecology Shanghai Institutes for Biological Science Chinese Academy of Sciences ShanghaiChina

Fusion of the testis occurs in most Lepidoptera insects, including Spodoptera litura, an important polyphagous pest. Testicular fusion in S. litura is advantageous for male reproduction, and the molecular mechanism of fusion remains unknown. Doublesex influences the formation of genitalia, the behavior of courtship, and sexually dimorphic traits in fruit-fly and silkworm, and is essential for sexual differentiation. However, its purpose in the testis of S. litura remains unknown. The doublesex gene of S. litura (Sldsx) has male-specific SldsxM and female-specific SldsF isoforms, and exhibits a higher expression level in the male testis. At the testicular fusion stage (L6D6), Sldsx attained the highest expression compared to the pre-fusion and post-fusion periods. Moreover, Sldsx had a higher expression in the peritoneal sheaths of testis than that of germ cells in the follicle. CRISPR/Cas9 (Clustered Regularly Interspaced Short Palindromic Repeats/Cas9) was applied to S. litura to determine the role of Sldsx. A mixture of single guide RNA messenger RNA and Cas9 protein (300 ng/μL each) was injected into eggs within 2 h following oviposition. CRISPR/Cas9 successfully induced genomic mutagenesis of Sldsx at Go generation. The mutant males had smaller testis surrounded by less tracheae. Moreover, the mutant males had abnormal external genitalia and could not finish mating with wild-type females. Additionally, testes were fused for almost all mutant males. The results showed that Sldsx was not related to testicular fusion, and is required for both testis development and the formation and function of external genitalia in S. litura. The main roles of doublesex on the male are similar to other insects.

关键词： CRISPR/Cas9 system doublesex external genitalia Spodoptera litura testis

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Silencing JA hydroxylases in Nicotiana attenuata enhances jasmonic acid-isoleucine-mediated defenses against Spodoptera litura

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Plant Diversity 2020年第2期42卷 111-119页

作者： Jinxiang Tang Dahai Yang Jianqiang Wu Suiyun Chen Lei Wang Department of Economic Plants and Biotechnology Yunnan Key Laboratory for Wild Plant ResourcesKunming Institute of BotanyChinese Academy of SciencesKunming650201China Tobacco Breeding and Biotechnology Research Center Yunnan Academy of Tobacco Agricultural SciencesKey Laboratory of Tobacco Biotechnological BreedingNational Tobacco Genetic Engineering Research CenterKunming650021China School of Life Science Yunnan UniversityKunming650091China

Jasmonic acid(JA)plays important roles in plant resistance to insect herbivores.One important derivative of JA is 12-OH-JA,which is produced by two independent pathways:direct hydroxylation of JA by jasmonate-induced oxygenases(JOXs)or hydrolyzation of 12-OH-JA-Ile.Yet the function of 12-OH-JA in plant-herbivore interactions remains largely unknown.In this study,we silenced four JOX homologs independently in the wild tobacco Nicotiana attenuata by virus-induced gene silencing(VIGS),and found that all four JOX homologs are involved in JA hydroxylation.Simultaneously silencing the four JA hydroxylases in VIGS-NaJOXs plants decreased herbivory-induced 12-OH-JA by 33%,but JA and JA-Ile levels increased by 45%and 30%,respectively,compared to those in control plants.Compared to direct hydroxylation from JA,hydrolyzation from 12-OH-JA-Ile is equally important for herbivory-induced 12-OHJA accumulation:in the 12-OH-JA-Ile deficient irJAR4/6 plants,12-OH-JA decreased 34%.Moreover,VIGSNaJOXs plants exhibited enhanced resistance to the generalist herbivore Spodoptera litura.The poor larval performance was strongly correlated with high levels of several JA-Ile-dependent direct defense metabolites in the VIGS-NaJOXs plants.When we simultaneously silenced all four JA hydroxylases in the JAIle-deficient irJAR4/6 background,the enhanced herbivore resistance diminished,demonstrating that enhanced herbivore resistance resulted from elevated JA-Ile levels.Given that silencing these NaJOX-like genes did not detectably alter plant growth but highly increased plant defense levels,we propose that JOX genes are potential targets for genetic improvement of herbivore-resistant crops.

关键词： JA metabolism 12-OH-JA Spodoptera litura 2-Oxoglutarate oxygenase Herbivore defense Nicotiana attenuata

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Exposure to herbicides reduces larval sensitivity to insecticides in Spodoptera litura (Lepidoptera: Noctuidae)

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Insect Science 2019年第4期26卷 711-720页

作者： Shi-Wei Liu Mohammed Esmail Abdalla Elzaki Christian Staehelin Zhi-Hui Ma Zhong Qin Rui-Long Wang Guangdong Engineering Research Center for Modern Eco-agriculture and Circular Agriculture Guangzhou China Key Laboratory of Agro-Environment in the Tropics Ministry of Agriculture South China Agricultural University Guangzhou China College of Crop Science Fujian Agriculture and Forestry University Fuzhou China State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources School of Life Sciences Sun Yat-sen University East Campus Guangzhou China

Herbicides and insecticides are widely used in modern agriculture. It has been reported in various studies that application of insecticides can increase tolerance of herbivorous insects to insecticides. However, limited information exists on susceptibility to insecticides when insects are exposed to herbicides. This study was conducted to investigate the potential impact of the herbicides trifluralin and 2-methyl-4-chlorophenoxyacetic acid sodium salt (MCPA-Na) on the susceptibility of the nocturnal moth Spodoptera litura to the insecticides X-cyhalothrin, phoxim and bifenthrin. We found that larvae exposed to trifluralin or MCPA-Na became significantly less susceptible to both insecticides than nonexposed control larvae. Herbicide-treated larvae did not show altered growth under the used test conditions. However, heads of herbicide-treated larvae showed increased expression of the acetylcholinesterase genes SI Ace I and SI Ace 2. Moreover, the fat body and midgut of herbicide-treated larvae displayed elevated expression of detoxification genes (the carboxylesterase gene SI CarE;the glutathione S-transferase genes SlGSTe2 and SlGSTe3\ the cytochrome P450 monooxygenase genes CYP6B48, CYP9A40 and CYP321B1). The CYP6B48 gene exhibited highest inducibility. In conclusion, the data of this study suggest that exposure of S. litura larvae to herbicides may stimulate detoxification mechanisms that compromise the efficacy of insecticides.

关键词： herbicides insecticides insecticide detoxification insecticide susceptibility Spodoptera litura

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CRISPR/Cas9-mediated ebony knockout results in puparium melanism in Spodoptera litura

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Insect Science 2019年第6期26卷 1011-1019页

作者： Hong-Lun Bi Jun Xu Lin He Yong Zhang Kai Li Yong-Ping Huang College of Life Sciences East China Normal University Shanghai China Key Laboratory of Insect Developmental and Evolutionary Biology Institute of Plant Physiology and Ecology Shanghai Institutes for Biological Sciences Chinese Academy of SciencesShanghai China Department of Biology University of Nevada Reno NV USA

Insect body pigmentation and coloration are critical to adaption to the environment. To explore the mechanisms that drive pigmentation, we used the clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) genome editing system to target the ebony gene in the non-model insect Spodoptera litura. Ebony is crucial to melanin synthesis in insects. By directly injecting Cas9 messenger RNA and ebony-specific guide RNAs into S. litura embryos, we successfully induced a typical ebony-deficient phenotype of deep coloration of the puparium and induction of melanin formation during the pupal stage. Polymerase chain reaction-based genotype analysis demonstrated that various mutations had occurred at the sites targeted in ebony. Our study clearly demonstrates the function of ebony in the puparium coloration and also provides a potentially useful marker gene for functional studies in S. litura as well as other lepidopteran pests.

关键词： CR1SPR/Cas9 ebony marker gene Spodoptera litura

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Expression,regulation and binding affinity of fatty acid-binding protein 2 in Spodoptera litura

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Journal of Integrative Agriculture 2020年第6期19卷 1492-1500页

作者： WEN Liang GAO Gui-ping HUANG Zhi-qiang ZHENG Si-chun FENG Qi-li LIU Lin Institute of Insect Science and Technology School of Life SciencesSouth China Normal University/Guangzhou Key Laboratory of Insect Development Regulation and Applied Research/Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied TechnologyGuangzhou 510631P.R.China

Fatty acid-bindi ng proteins(FABPs)are a family of lipid chaper on es,which con tribute to systemic metabolic regulati on through diverse lipid signalings.In this study,a midgut-specific FABP gene(Slfabp2)was cloned from Spodoptera litura.RT-PCR and Western blot analysis indicated that RNA and protein levels of S/FABP2 gradually increased and reached a peak at the prepupal stage and maintained a high level during the pupal stage.The expression of S/FABP2 protein was induced by starvation treatment.In vitro binding assay revealed that the recombinant S/FABP2 had high mffinities of binding Iong-chain fatty acids,such as palmitic acid,arachidonate and oleic acid.The results suggest that S/FABP2 may have a unique function that transports intracellular fatty acids and can regulate the metabolism of lipids in metamorphosis.This work provides experimental clues for understanding the potential function of S/FABP2 in fatty acid metabolism in S.litura.

关键词： Spodoptera litura S/FABP2 starvation treatment binding assay

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Microsatellites reveal strong genetic structure in the common cutworm, Spodoptera litura

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Journal of Integrative Agriculture 2019年第3期18卷 636-643页

作者： WU Huai-heng WAN Peng HUANG Min-song LEI Chao-liang Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory Huazhong Agricultural University Key Laboratory of Integrated Pest Management on Crops in Central China Institute of Plant Protection and Soil ScienceHubei Academy of Agricultural Sciences

The common cutworm, Spodoptera litura(Lepidoptera: Noctuidae), is a voracious agricultural pest. To increase understanding of the migration patterns and genetic diversity of different geographic populations of this species, we analyzed genetic variation in nine microsatellite loci among 576 individuals collected from 17 locations in China and one in Myanmar during 2011–2012. We successfully identified 162 alleles, with an average of 18 alleles per locus and a range of 5 to 34. The mean observed heterozygosity of the 18 populations ranged from 0.18 to 0.98, and the expected heterozygosity ranged from 0.19 to 0.89. For the nine microsatellite markers studied, polymorphism information content ranged from 0.18 to 0.88(mean=0.64). We found low genetic differentiation among the 18 populations(mean F-statistics(F_(ST))=0.05) and high genetic diversity among individuals. Principle coordinates analysis indicated no significant correlation between geographic and genetic distance(r=0.04). The value of N_m(N_m>4) estimated using coalescent-based methods suggests strong gene flow with migration. The nine microsatellite markers identified in this study will be beneficial for further investigation of migration patterns and genetic diversity in S. litura.

关键词： Spodoptera litura microsatellite genetic diversity

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Transient expression of SbDhr2 and MeHNL in Gossypium hirsutum for herbivore deterrence assay with Spodoptera litura

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Journal of Cotton Research 2020年第1期3卷 1-12页

作者： MAHAJAN Chavi NASER Rafiuddin GUPTA Shantikumar Department of Botany Maulana Azad College of Arts Scienee and CommerceRauza BaghAurangabadMaharashtra 431001India Government Institute of Scienee AurangabadMaharashtra 431001India

Background:Spodoptera litura(Lepidoptera:Noctuidae),commonly known as tobacco cutworm or cotton leafworm,is a polyphagous pest which causes considerable damage to cotton(Gossypium hirsutum)and other crops.Herbivore-induced defence response is activated in plants against chewing pests,in which plant secondary metabolites play an important role.Dhurrinase2(SbDhr2),a cyanogenicβ-glucosidase from Sorghum bicolor,is the key enzyme responsible for the hydrolysis of dhurrin(cyanogenicβ-glucosidic substrate)to phydroxymandelonitrile.Hydroxynitrile lyase(Me HNL)from Mannihot esculanta catalyses the dissociation of cyanohydrins to hydrogen cyanide and corresponding carbonyl compound,both enzymes play a pivotal role in plant defence mechanism.Results:SbDhr2 and Me HNL genes were expressed individually and co-expressed transiently in cotton leaves.We examined the feeding response of S.litura to leaves in the choice assay.The S.litura population used in this study showed better feeding deterrence to leaves co-expressing both genes compared with the expression of an individual gene.Conclusion:Our results suggest that co-expression of SbDhr2 and Me HNL genes in cotton leaves demonstrate feeding deterrence to S.litura.Engineering cyanogenic pathway in aerial parts of cotton would be an additional defence strategy against generalist pests and can be enhanced against specialist pests.

关键词： SbDhr2 MeHNL HCNc(hydrogen cyanide concentration) HCNp(hydrogen cyanide potential) TRV(tobacco rattle virus) Spodoptera litura Plant defence

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Occurrence Regularity and Sexual Pheromone Trapping Effect of Spodoptera litura in Field in Central Guizhou

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Agricultural Biotechnology 2019年第1期8卷 69-72页

作者： Chengping FAN Enfa CHEN Junming YUE Wang YIN Rui ZUO Lishi ZUO Anshun Branch Company Institute of Biotechnology Guizhou Academy of Agricultural Sciences Nanjing Agricultural University

The Spodoptera litura occurrence quantity in Tianlong Town,Pingba County,Anshun City was dynamically monitored by an insect sex pheromone electronic measurement and forecast system in 2015 and 2016 and the trapped effect of S. litura was studied by the home-made S. litura sex pheromone traps in Baishiyan Town,Ziyun County and Tianlong Town,Pingba County in 2016 to accurately grasp the occurrence regularity of S. litura and apply insect sex pheromone for controlling S. litura in Central Guizhou tobacco-growing region. There are 5 generations of S. litura in a year in Central Guizhou region. The first generation of S.litura occurs from late April to middle May,the second from middle-to-late July to middle-to-late August,the third from early-to-middle August to the end of September,the fourth is in the end of October and the fifth in the end of November. S. litura emigrates or enters into the overwintering stage in December. S. litura is almost in active in the daytime during the peak occurrence period of S. litura adults. The first mating time of S. litura is at 17: 30 and its peak mating time is about 22: 00. The second mating time of S. litura is at 1: 00-5: 00 and its peak mating time is about 2: 30. The trapped S. litura quantity presents an obvious layer-belt distribution that the number in the outer ring is significantly higher than that in the middle ring,and the number in the middle ring is significantly higher than that in the inner ring. The number of trapped S. litura is higher around the outer ring of the testing field and at the draught position than in the low-lying land and inner flat ground.

关键词： Tobacco Spodoptera litura Occurrence regularity Sex pheromone Central Guizhou

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