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juvenile hormone induces reproduction via miR-1175-3p in the red imported fire ant, Solenopsis invicta

Insect Science 2024年第2期31卷 371-386页

作者： Jie Chen Ziying Guan Yunjie Ma Qingxing Shi Ting Chen Muhammad Irfan WarisLihua Lyu Lihua Lyu Yongyue Lu Guojun Qi Institute of Plant Protection Guangdong Academy of Agricultural SciencesKey Laboratory of Green Prevention and Control on Fruits and Vegetables in South China Ministry of Agriculture and Rural AffairsGuangdong Provincial Key Laboratory of High Technology for Plant ProtectionGuangzhouChina Department of Entomology College of Plant ProtectionSouth China Agricultural UniversityGuangzhouChina

juvenile hormone(JH)acts in the regulation of caste differentiation between queens and workers(i.e.,with or without reproductive capacity)during vitellin synthesis and oogenesis in social insects.However,the regulatory mechanisms have not yet been elucidated.Here,we identified a highly expressed microRNA(miRNA),miR-1175-3p,in the red imported fire ant,Solenopsis invicta.We found that miR-1175-3p is prominently present in the fat bodies and ovaries of workers.Furthermore,miR-1175-3p interacts with its target gene,broad-complex core(Br-C),in the fat bodies.By utilizing miR-1175-3p agomir,we successfully suppressed the expression of the Br-C protein in queens,resulting in reduced vitellogenin expression,fewer eggs,and poorly developed ovaries.Conversely,decreasing miR-1175-3p levels led to the increased expression of Br-C and vitellogenin in workers,triggering the“re-development”of the ovaries.Moreover,when queens were fed with JH,the expression of miR-1175-3p decreased,whereas the expression of vitellogenin-2 and vitellogenin-3 increased.Notably,the suppression of fertility in queens caused by treatment with agomir miR-1175-3p was completely rescued by the increased vitellogenin expression induced by being fed with JH.These results suggest the critical role of miR-1175-3p in JH-regulated reproduction,shedding light on the molecular mechanism underlying miRNA-mediated fecundity in social insects and providing a novel strategy for managing S.invicta.

关键词： juvenile hormone miR-1175-3p red imported fire ant reproduction social insects vitellogenin

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juvenile hormone acts on male accessory gland function via regulating L-asparaginase expression and triacylglycerol mobilization in Aedes aegypti

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Insect Science 2023年第1期30卷 81-94页

作者： Xiang-Yang Lyu Xue-Li Wang Dan-Qian Geng Hong Jiang Zhen Zou State Key Laboratory of Integrated Management of Pest Insects and Rodents Institute of ZoologyChinese Academy of SciencesBejingChina CAS Center for Excellence in Biotic Interactions University of Chinese Academy of SciencesBejingChina

hormones control the reproductive development of Aedes aegypti mosquitoes.The adult male reproductive process and mating behavior require adequate nutrients and energy.Understanding the molecular mechanism linking hormones,energy metabolism,and reproduction in male mosquitoes is important.In this study,we found that the size of the male accessory gland,an essential part of the male reproductive system,gradually increased after eclosion.However,it was significantly reduced in male mosquitoes deficient in methoprene-tolerant(Met),the receptor of juvenile hormone.Likewise,egg hatchability of females that mated with Met-depleted males showed the same downward trend.The mRNA level of the gene encoding accessory gland protein,l-asparaginase(ASNase),was reduced in Met dsRNA-treated males.Electrophoretic mobility shift assay and quantitative reverse transcription-PCR results revealed that Met was capable of binding directly to the promoter of ASNase and activated its transcription.RNA interference of ASNase in males resulted in the reduction of egg hatchability of the females with which they mated.These results showed that Met influenced the fecundity of male mosquitoes by directly upregulating the expression of the ASNase gene.Moreover,the levels of triacylglycerol and the sizes of lipid droplets were decreased by 72-78 h after eclosion in the fat body cells,whereas both of them increased in Met-depleted male mosquitoes,indicating that Met knockdown reduced lipid catabolism.These data demonstrate that Met might influence the egg hatchability of females by regulating lipid metabolism and the development of the male accessory gland in male mosquitoes.

关键词： accessory gland protein energy juvenile hormone lipid metabolism male accessory gland male mosquito

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juvenile hormone regulates photoperiod-mediated male reproductive diapause via the methoprene-tolerant gene in the ladybeetle Harmonia axyridis

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Insect Science 2022年第1期29卷 139-150页

作者： Qiao Gao Bei Li Bing-Xin Wei Wen Liu Pan Wang Jia-Lu Wang Xing-Miao Zhou Xiao-Ping Wang Hubei Key Laboratory of Insect Resources Utilization and Sustainable Pest Management College of Plant Science and TechnologyHuazhong Agricultural UniversityWuhan430070China Department of Plant Protection Wuhan Vegetable Research InstituteWuhan430065China

juvenile hormone (JH) absence induces photoperiod-mediated reproductive diapause, which is characterized by reproductive cessation. Although the role of methoprene-tolerant (Met)-mediated JH signaling in photoperiod-mediated female reproduction has been well documented, its role in male reproduction remains unclear. In this study, we investigated the role of JH in regulating photoperiod-mediated development of the male internal reproductive system (IRS) in the predatory ladybeetle Harmonia axyridis (Pallas). In a previous study, we found that adult male H. axyridis reared under either a short-day (SD) or long-day (LD) photoperiod had obvious differences in IRS development, but we were unable to identify the regulators of male reproductive diapause. In this study, we found that beetles reared under an SD photoperiod had significantly lower JH titer and a relatively undeveloped male IRS compared with those reared under an LD photoperiod. Additionally, application of the JH analog (JHA) methoprene promoted IRS development. Furthermore, Met knockdown strongly blocked JH signaling in males reared under the LD photoperiod, thereby slowing IRS development. Moreover, exogenous JHA did not reverse the suppressed development of the male IRS caused by Met knockdown. These results indicate that photoperiod regulates male IRS development in H. axyridis through a conserved Met-dependent JH signaling pathway.

关键词： Harmonia axyridis juvenile hormone male reproductive diapause methoprene-tolerant photoperiod RNAi

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juvenile hormone signaling-a mini review

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Insect Science 2019年第4期26卷 600-606页

作者： Kang Li Qiang-Qiang Jia Sheng Li Guangzhou Key Laboratory of Insect Development Regulation and Application Research Institute of Insect Science and Technology&School of Life SciencesSouth China Normal UniversityGuangzhouChina

Since it was first postulated by Wigglesworth in 1934, juvenile hormone (JH) is considered a status quo hormone in insects because it prevents metamorphosis that is initiated by the molting hormone 20-hydroxyecdysone (20E). During the last decade, significant advances have been made regarding JH signaling. First, the bHLH-PAS transcription factor Met/Gce was identified as the JH intracellular receptor. In the presence of JH, with the assistance of Hsp83, and through physical association with a bHLH?PAS transcriptional co-activator, Met/Gce enters the nucleus and binds to E-box-like motifs in promoter regions of JH primary?response genes for inducing gene expression. Second, the zinc finger transcription factor Kr-hl was identified as the anti-metamorphic factor which transduces JH signaling. Via Kr-hl binding sites, Kr-hl represses expression of 20E primary?response genes (i.e. Bi\ E93 and E5) to prevent 20E-induced metamorphosis. Third, through the intracellular signaling, JH promotes differ ent aspects of female reproduction. Nevertheless, this action varies greatly from species to species. Last, a hypothetical JH membrane receptor has been predicted to be either a GPCR or a tyrosine kinase receptor. In future, it will be a great challenge to understand how the JH intracellular receptor Met/Gce and the yet unidentified JH membrane receptor coordinate to regulate metamorphosis and reproduction in insects.

关键词： intracellular receptor juvenile hormone (JH) Kr-h 1 membrane receptor Met/Gce metamorphosis reproduction

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Dual roles of juvenile hormone signaling during early oogenesis in Drosophila

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Insect Science 2020年第4期27卷 665-674页

作者： Wei Luo Sethuraman Veeran Jian Wang Sheng Li Kang Li Su-Ning Liu Guangzhou Key Laboratory of Insect Development Regulation and Application Research Institute of Insect Science and Technology&School of Life SciencesSouth China Normal UniversityGuangzhouChina and 2 Department of EntomologyUniversity of MarylandCollege ParkMDUSA

juvenile hormone(JH)signaling plays crucial roles in insect metamorphosis and reproduction.Function of JH signaling in germline stem cells(GSCs)remains largely unknown.Here,we found that the number of GSCs significantly declined in the ovaries of Met,Gee and JHAMT mutants.Then we inhibited JH signaling in selected cell types of ovaries by expressing Met and Gee or Kr-hl double-stranded RNAs(dsRNAs)using different Gal4 drivers.Blocking of JH signaling in muscle cells has no effect on GSC numbers.Blocking of JH signaling in cap cells reduced GSCs cells.Inductive expression of Met and Gee dsRNA but not Kr-hl by Nos-Gal4 increased GSC cells.These results indicate that JH signaling plays an important role in GSC maintenance.

关键词： cap cells germline stem cells juvenile hormone oogenesis ovary

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Methoprene does not affect juvenile hormone titers in honey bee （Apis mellifera） workers

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Insect Science 2018年第2期25卷 235-240页

作者： Huang, Zachary Y. Lin, Stephanie Ahn, Kiheung Department of Entomology Michigan State University East Lansing Michigan USA Ecology Evolutionary Biology and Behavior Michigan State University East Lansing Michigan USA BEACON Center for the Study of Evolution in Action Michigan State University East Lansing Michigan USA High School Honors Science Program 2007 Michigan State University East Lansing Michigan USA

Methoprene, a juvenile hormone （JH） analog, is a widely used insecticide that also accelerates behavioral development in honey bees （Apis mellifera）. JH regulates the transition from nursing to foraging in adult worker bees, and treatment with JH or methoprene have both been shown to induce precocious foraging. To determine how methoprene changes honey bee behavior, we compared JH titers ofmethoprene-treated and untreated bees. Behavioral observations confirmed that methoprene treatment significantly increased the number of precocious foragers in 3 out of 4 colonies. In only 1 out of 4 colonies, however, was there a significant difference in JH titers between the methoprene- treated and control bees. Further, in all 4 colonies, there was no significant differences in JH titers between precocious and normal-aged foragers. These results suggest that methoprene did not directly affect the endogenous JH secreted by corpora allata. Because methoprene caused early foraging without changing workers＇ JH titers, we conclude that methoprene most likely acts directly on the JH receptors as a substitute for JH.

关键词： behavioral development juvenile hormone analog juvenile hormone metho-prene precocious foraging

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Expression of juvenile hormone acid O-methyltransferase and juvenile hormone synthesis in Blattella germanica

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Insect Science 2018年第5期25卷 787-796页

作者： Claudia V. Dominguez Jose L. Maestro Institute of Evolutionary Biology CSIC-Universitat Pompeu Fabra Barcelona Spain

juvenile hormone （JH）, a sesquiterpenoid synthetized by the insect corpora allata （CA）, plays critical roles in metamorphosis and reproduction. Penultimate or last step of JH synthesis is catalyzed by juvenile hormone acid O-methyltransferase （JHAMT）. Here we report the cloning and expression analysis of the JHAMT orthologue in the cockroach, Blattella germanica （L.）（BgJHAMT）. BgJHAMT is mainly expressed in CA, with only expression traces in ovary. Three different isoforms, differing in the 3＇-UTR sequence, were identified. Isoform A shows between 35 and 65 times higher expression than B and C in CA from penultimate nymphal instar and adult females. RNAi-triggered knock down of BgJHAMT produces a dramatic reduction of JH synthesis, concomitant with a decrease of fat body viteUogenin expression and basal follicle length. BgJHAMT mRNA levels in CA of females along the gonadotrophic cycle parallel, with a slight advancement, JH synthesis profile. BgJHAMT mRNA levels were reduced in starved females and in females in which we reduced nutritional signaling by knocking down insulin receptor and target of rapamycin （TOR）. Results show that conditions that modify JH synthesis in adult B. germanica females show parallel changes of BgJHAMT mRNA levels and that the JH-specifie branch of the JH synthesis pathway is regulated in the same way as the mevalonate branch. Furthermore, we demonstrate that nutrition and its signaling through the insulin receptor and TOR pathways are essential for activating BgJHAMT expression, which suggests that this enzyme can be a checkpoint for the regulation of JH production in relation to nutritional status.

关键词： Blattella germanica corpora allata JHAMT juvenile hormone nutritionalsignaling

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Cloning and structural characterization of juvenile hormone diol kinase in Spodoptera litura

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Insect Science 2016年第6期23卷 819-828页

作者： Bao-Juan Zeng Yuan Lv Li-Li Zhang Li-Hua Huang Qi-Li Feng Guangzhou Key Laboratory of Insect Development Regulation and Application Research School of Life Sciences South China Normal University Guangzhou 510631 China

juvenile hormone （JH） is one of the key insect hormones that regulate metamorphosis. juvenile hormone diol kinase （JHDK） is an enzyme involved in JH metabolism and catalyzes JH diol to form a polar end product, JH diol phosphate that has no JH activity. In this study, a JHDK complementary DNA （cDNA） was cloned from Spodoptera litura and the structure and expression of the gene was characterized. The cDNA was 714 base pairs in length and encoded a protein of 183 amino acids with a molecular mass of 21 kDa and an isoelectric point of 4.55. Based on the structure, three putative calcium binding motifs and guanosine triphosphate-binding motifs were predicted in the protein. Modeling of the 3-D structure showed that the protein consisted of eight α-helixes linked with loops, with no β-sheets. The gene was expressed in the epidermis, fat body and midgut of fifth and sixth instar larvae. The expression level in the epidermis was lower than in the fat body and midgut. The gene was expressed at higher levels at the early stages than in the later stages of fifth and sixth instar midgut and fat body. The results suggest that this gene may be involved in the regulation of the JH titer in larvae ofS. litura.

关键词： juvenile hormone juvenile hormone diol kinase metabolism Spodoptera litura

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MicroRNA miR-2765-3p regulates reproductive diapause by targeting FoxO in Galeruca daurica

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Insect Science 2023年第2期30卷 279-292页

作者： Tian-Feng Duan Ling Li Hai-Chao Wang Bao-Ping Pang Research Center for Grassland Entomology Inner Mongolia Agricultural UniversityHohhotChina

The forkhead box O(FoxO),as a conserved transcription factor,plays an indispensable role in regulating insect diapause.However,how FoxO is regulated to control diapause in insects remains unknown.In this study,we discovered functional binding sites for miR-2765-3p in the 3′untranslated region of FoxO in Galeruca daurica.The luciferase reporter assay showed that miR-2765-3p targeted FoxO and suppressed its expression.The expression profiles of miR-2765-3p and FoxO displayed opposite patterns during the female developmental process.Overexpression of miR-2765-3p by the injection of the miR-2765-3p agomir into adult females reduced FoxO expression,leading to the suppression of lipid accumulation,promotion of ovarian development,and inhibition of reproductive diapause.This is similar to the phenotype that results from the depletion of FoxO by injecting dsFoxO into adult females.In addition,the repression of miR-2765-3p by injecting the miR-2765-3p antagomir increased the FoxO transcript level,leading to the stimulation of lipid accumulation,depression of ovarian development,and induction of reproductive diapause.A hormone injection assay showed that the juvenile hormone(JH)agonist(methoprene)upregulated miR-2765-3p and downregulated FoxO.Notably,injecting methoprene rescued ovarian development defects associated with miR-2765-3p inhibition.These findings indicate that the JH/miR-2765-3p/FoxO axis plays a vital role in the regulation of reproductive diapause in G.daurica.

关键词： diapause FoxO Galeruca daurica juvenile hormone microRNA

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Comparison of the signaling pathways of wing dimorphism regulated by biotic and abiotic stress in the brown planthopper

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Insect Science 2023年第4期30卷 1046-1062页

作者： Jing-Xiang Chen Wan-Xue Li Qin Su Jun Lyu Yi-Bing Zhang Wen-Qing Zha State Key Laboratory of Biocontrol and School of Life Sciences Sun Yat-sen UniversityGuangzhouChina

Wing polymorphism is an evolutionary trait that is widely present in various insects and provides a model system for studying the evolutionary significance of insect dispersal.The brown planthopper(BPH,Nilaparvata lugens)can alter its wing morphs un-der biotic and abiotic stress.However,whether differential signaling pathways are induced by the 2 types of stress remain largely unknown.Here,we screened a number of candidate genes through weighted gene co-expression network analysis(WGCNA)and found that ornithine decarboxylase(NIODC),a key enzyme in the synthesis of polyamines,was as-sociated with wing differentiation in BPH and mainly responded to abiotic stress stimuli.We analyzed the Kyoto Encyclopedia of Genes and Genomes enrichment pathways of dif-ferentially expressed genes under the 2 stresses by transcriptomic comparison,and found that biotic stress mainly influenced insulin-related signaling pathways while abiotic stress mainly influenced hormone-related pathways.Moreover,we found that insulin receptor 1(NllnRI)may regulate wing differentiation of BPH by responding to both biotic and abiotic stress,but NllnR2 only responded to biotic stress.Similarly,the juvenile hormone epoxide hydrolase associated with juvenile hormone degradation and NIODC may regu-late wing differentiation mainly through abiotic stress.A model based on the genes and stresses to modulate the wing dimorphism of BPH was proposed.These findings present a comprehensive molecular mechanism for wing polymorphism in BPH induced by biotic and abiotic stress.

关键词： insulin juvenile hormone Nilaparvata lugens ornithine decarboxylase stress wing dimorphism

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