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Journal of Integrative Agriculture  2023, Vol. 22 Issue (8): 2470-2482    DOI: 10.1016/j.jia.2023.02.028
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The combination of NlMIP and Gαi/q coupled-receptor NlA10 promotes abdominal vibration production in female Nilaparvata lugens (Stål)

SU Qin1, 2, LÜ Jun1, LI Wan-xue1, CHEN Wei-wen1, LUO Min-shi1, ZHANG Chuan-chuan1, ZHANG Wen-qing1#

1 State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R.China

2 Department of Forensic Medicine, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, P.R.China

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摘要  

对于某些性成熟昆虫包括褐飞虱)而言,腹部振动(abdominal vibration,AV)是交配过程的启动信号,对成功交配至关重要。目前,关于调控AV的遗传和分子机制的研究很少。我们以往与AV相关的转录组学研究表明,肌抑制肽(myoinhibitory peptide,NlMIP调控雌性褐飞虱AV的潜在基因,但其对AV的调控机制尚未报道本文证实NlMIP参与调控雌性褐飞虱的AV和交配行为。当NlMIP敲低效率为59.00%时,雌性褐飞虱在1小时内产生AV频率和交配成功率分别下降了38.89%61.11%。此外,6NlMIP成熟肽能够调控雌性褐飞虱AV的产生及其交配行为,其中NlMIP2的作用最强。基于系统发育树分析和NlMIP成熟肽有效激活A家族神经肽G蛋白偶联受体10(A-family neuropeptide GPCR 10NlA10的结果表明NlA10NlMIP的潜在受体。NlA10被敲低后,雌性褐飞虱1小时内产生AV频率和交配成功率分别下降了28.89%43.33%。当NlA10NlMIP2激活时,NlA10偶联到Gαi/q信号通路,从而抑制下游AC/cAMP/PKA激活PLC/Ca2+/PKC信号通路,进而级联激活MEK1/2介导ERK1/2的磷酸化,最终调控雌性褐飞虱的AV。这些结果为通过干扰雌性褐飞虱的AV进行害虫防治提供了依据。



Abstract  

For various sexually mature insects, including the brown planthopper (BPH, Nilaparvata lugens), the abdominal vibration (AV) signal is the initiation of the mating process, and it is critical to the success of mating.  Currently, there are few studies on the genetic and molecular mechanisms of AV regulation.  Our previous AV-related transcriptomic study in female BPH identified myoinhibitory peptide (NlMIP) as a gene that potentially affects AV status in females, but how NlMIP affects AV status remains unknown.  In this study, we confirmed that NlMIP regulates AV production and mating behavior in female BPH.  When the RNAi knockdown efficiency of NlMIP was 59.00%, the probability of females producing AV and the mating rate in 1 h decreased by 38.89 and 61.11%, respectively.  In addition, six mature peptides of NlMIP were synthesized and they were able to regulate AV production and mating behavior in females, with NlMIP2 having the strongest effect.  The A-family neuropeptide GPCR 10 (NlA10) was found to be a potential receptor for NlMIP based on a phylogenetic tree analysis and the fact that NlMIP mature peptides effectively activated NlA10.  After NlA10 was knocked down, the probability of females producing AV and the mating rate in 1 h had reductions of 28.89 and 43.33%, respectively.  When activated by NlMIP2, NlA10 coupled the Gαi/q signalling pathways, thereby inhibiting the downstream AC/cAMP/PKA, activating the PLC/Ca2+/PKC signalling pathways and then activating MEK1/2 in a cascade to mediate the phosphorylation of ERK1/2, and finally regulating the AV of females.  These results provide a basis for the prevention and control of the brown planthopper pest by disrupting female AV.

Keywords:  abdominal vibration        mating disruption        myoinhibitory peptide (MIP)        NlA10        GPCR        brown planthopper  
Received: 24 September 2022   Accepted: 20 December 2022
Fund: 

The study was funded by the National Natural Science Foundation of China (31730073).

About author:  SU Qin, E-mail: 470457020@qq.com; #Correspondence ZHANG Wen-qing, Tel: +86-20-39332963, Fax: +86-20-39943515, E-mail: lsszwq@mail.sysu.edu.cn

Cite this article: 

SU Qin, LÜ Jun, LI Wan-xue, CHEN Wei-wen, LUO Min-shi, ZHANG Chuan-chuan, ZHANG Wen-qing. 2023. The combination of NlMIP and Gαi/q coupled-receptor NlA10 promotes abdominal vibration production in female Nilaparvata lugens (Stål). Journal of Integrative Agriculture, 22(8): 2470-2482.

Aguilar R, Maestro J L, BellÉS X. 2006. Effects of myoinhibitory peptides on food intake in the German cockroach. Physiological Entomology31, 257–261.

Ahmed A M, Muhamad R, Omar D, Grozescu I V, Majid D L, Manjeri G. 2016. Mating behaviour of brown planthopper Nilaparvata lugens Stål (Homoptera: Delphacidea) under certain biological and environmental factors. Pakistan Journal of Zoology48, 11–23.

Baggerman G, Cerstiaens A, De Loof A, Schoofs L. 2002. Peptidomics of the larval Drosophila melanogaster central nervous system. Journal of Biological Chemistry277, 40368–40374.

Blackburn M B, Jaffe H, Kochansky J, Raina A K. 2001. Identification of four additional myoinhibitory peptides (MIPs) from the ventral nerve cord of Manduca sextaArchives of Insect Biochemistry and Physiology48, 121–128.

Blackburn M B, Wagner R M, Kochansky J P, Harrison D J, Thomas-Laemont P, Raina A K. 1995. The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Manduca sextaRegulatory Peptides57, 213–219.

Chen W W, Kang K, Yang P, Zhang W Q. 2019. Identification of a sugar gustatory receptor and its effect on fecundity of the brown planthopper Nilaparvata lugensInsect Science26, 441–452.

Chen X, Zhang M Q, Wang X Q, Guo J S, Li D T, Xue J, Pan W D, Zhang C X. 2019. The flightin gene is necessary for the emission of vibrational signals in the rice brown planthopper (Nilaparvata lugens Stǻl). Journal of Insect Physiology112, 101–108.

Choo H Y, Kim H H, Kaya H K. 1998. Effects of selected chemical pesticides on Agamermis unka (Nematoda: Mermithidae), a parasite of the brown plant hopper, Nilaparvata lugensBiocontrol Science and Technology8, 413–427.

Conzelmann M, Williams E A, Tunaru S, Randel N, Shahidi R, Asadulina A, Berger J, Offermanns S, Jékely G. 2013. Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. Proceedings of the National Academy of Sciences of the United States of America110, 8224–8229.

Dias A M, Borges M, Blassioli Moraes M C, Figueira Coelho M L, Čokl A, Laumann R A. 2021. Inhibitory copulation effect of vibrational rival female signals of three Stink Bug species as a tool for mating disruption. Insects12, 1–16.

Eishingdrelo H, Kongsamut S. 2013. Minireview: Targeting GPCR activated ERK pathways for drug discovery. Current Chemical Genomics and Translational7, 9–15.

Foster S P, Harris M O. 1997. Behavioral manipulation methods for insect pest-management. Annual Review of Entomology42, 123–146.

Han Y, Wu C, Yang L, Zhang D, Xiao Y. 2018. Resistance to Nilaparvata lugens in rice lines introgressed with the resistance genes Bph14 and Bph15 and related resistance types. PLoS ONE13, e0198630.

He X, Zang J, Yang H, Huang H, Shi Y, Zhu C, Zhou N. 2015. Bombyx mori prothoracicostatic peptide receptor is allosterically activated via a Gαi/o-protein-biased signalling cascade by Drosophila sex peptide. Biochemical Journal466, 391–400.

He Y, Zhou Z, Tian L, Liu Y, Luo X. 2020. Brown rice planthopper (Nilaparvata lugens Stål) detection based on deep learning. Precision Agriculture21, 1385–1402.

Hua Y J, Tanaka Y, Nakamura K, Sakakibara M, Nagata S, Kataoka H. 1999. Identification of a prothoracicostatic peptide in the larval brain of the silkworm, Bombyx moriJournal of Biological Chemistry274, 31169–31173.

Ichikawa T. 1976. Mutual communication by substrate vibrations in the mating behavior of planthoppers (Homoptera: Delphacidae). Applied Entomology and Zoology11, 8–21.

Ichikawa T. 1982. Density-related changes in male–male competitive behavior in the rice brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Applied Entomology and Zoology17, 439–452.

Jang Y H, Chae H S, Kim Y J. 2017. Female-specific myoinhibitory peptide neurons regulate mating receptivity in Drosophila melanogasterNature Communications8, 1630.

Kim Y J, Bartalska K, Audsley N, Yamanaka N, Yapici N, Lee J Y, Kim Y C, Markovic M, Isaac E, Tanaka Y, Dickson B J. 2010. MIPs are ancestral ligands for the sex peptide receptor. Proceedings of the National Academy of Sciences of the United States of America107, 6520–6525.

Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution33, 1870–1874.

Lange A B, Alim U, Vandersmissen H P, Mizoguchi A, Vanden Broeck J, Orchard I. 2012. The distribution and physiological effects of the myoinhibiting peptides in the kissing bug, Rhodnius prolixusFrontiers in Neuroscience6, 1–9.

Laumann R A, Maccagnan D H B, Čokl A, Blassioli-Moraes M C, Borges M. 2018. Substrate-borne vibrations disrupt the mating behaviors of the neotropical brown stink bug, Euschistus heros: Implications for pest management. Journal of Pest Science91, 995–1004.

Li B, Predel R, Neupert S, Hauser F, Tanaka Y, Cazzamali G, Williamson M, Arakane Y, Verleyen P, Schoofs L, Schachtner J, Grimmelikhuijzen C J, Park Y. 2008. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneumGenome Research18, 113–122.

Liao X, Xu P F, Gong P P, Wan H, Li J H. 2021. Current susceptibilities of brown planthopper Nilaparvata lugens to triflumezopyrim and other frequently used insecticides in China. Insect Science28, 115–126.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods25, 402–408.

Long Y, Hu C, Shi B, Yang X, Hou M. 2012. Effects of temperature on mate location in the planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Environmental Entomology41, 1231–1238.

Lorenz M W, Kellner R, Hoffmann K H. 1995. A family of neuropeptides that inhibit juvenile hormone biosynthesis in the cricket, Gryllus bimaculatusJournal of Biological Chemistry270, 21103–21108.

Lorenz M W, Kellner R, Hoffmann K H, Gäde G. 2000. Identification of multiple peptides homologous to cockroach and cricket allatostatins in the stick insect Carausius morosusInsect Biochemistry and Molecular Biology30, 711–718.

Lujo S, Hartman E, Norton K, Pregmon E A, Rohde B B, Mankin R W. 2016. Disrupting mating behavior of Diaphorina citri (Liviidae). Journal of Economic Entomology109, 2373–2379.

Marder E, Thirumalai V. 2002. Cellular, synaptic and network effects of neuromodulation. Neural Networks15, 479–493.

Mazzoni V, Polajnar J, Baldini M, Rossi Stacconi M V, Anfora G, Guidetti R, Maistrello L. 2017. Use of substrate-borne vibrational signals to attract the brown marmorated stink bug, Halyomorpha halysJournal of Pest Science90, 1219–1229.

Mazzoni V, Presern J, Lucchi A, Virant-Doberlet M. 2009. Reproductive strategy of the nearctic leafhopper Scaphoideus titanus ball (Hemiptera: Cicadellidae). Bulletin of Entomological Research99, 401–413.

Min S, Chae H S, Jang Y H, Choi S, Lee S, Jeong Y T, Jones W D, Moon S J, Kim Y J, Chung J. 2016. Identification of a peptidergic pathway critical to satiety responses in DrosophilaCurrent Biology26, 814–820.

Monastirioti M. 2003. Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogasterDevelopmental Biology264, 38–49.

Nakazaki M, Crane A, Hu M, Seghers V, Ullrich S, Aguilar Bryan L, Bryan J. 2002. cAMP-activated protein kinase-independent potentiation of insulin secretion by cAMP is impaired in SUR1 null islets. Diabetes51, 3440–3449.

Oh Y, Yoon S E, Zhang Q, Chae H S, Daubnerová I, Shafer O T, Choe J, Kim Y J. 2014. A homeostatic sleep-stabilizing pathway in Drosophila composed of the sex peptide receptor and its ligand, the myoinhibitory peptide. PLoS Biology12, e1001974.

Paluzzi J P, Haddad A S, Sedra L, Orchard I, Lange A B. 2015. Functional characterization and expression analysis of the myoinhibiting peptide receptor in the Chagas disease vector, Rhodnius prolixusMolecular and Cellular Endocrinology399, 143–153.

Peymen K, Watteyne J, Borghgraef C, Van Sinay E, Beets I, Schoofs L. 2019. Myoinhibitory peptide signaling modulates aversive gustatory learning in Caenorhabditis elegansPLoS Genetics15, 1–21.

Poels J, Van Loy T, Vandersmissen H P, Van Hiel B, Van Soest S, Nachman R J, Vanden Broeck J. 2010. Myoinhibiting peptides are the ancestral ligands of the promiscuous Drosophila sex peptide receptor. Cellular and Molecular Life Sciences67, 3511–3522.

Polajnar J, Eriksson A, Lucchi A, Anfora G, Virant Doberlet M, Mazzoni V. 2015. Manipulating behaviour with substrate-borne vibrations - potential for insect pest control. Pest Management Science71, 15–23.

Polajnar J, Eriksson A, Virant-Doberlet M, Mazzoni V. 2016. Mating disruption of a grapevine pest using mechanical vibrations: from laboratory to the field. Journal of Pest Science89, 909–921.

Predel R, Rapus J, Eckert M. 2001. Myoinhibitory neuropeptides in the American cockroach. Peptides22, 199–208.

Reed H B. 1958. A study of dog carcass communities in Tennessee, with special reference to the insects. The American Midland Naturalist59, 213–245.

Rezával C, Nojima T, Neville M C, Lin A C, Goodwin S F. 2014. Sexually dimorphic octopaminergic neurons modulate female postmating behaviors in DrosophilaCurrent Biology24, 725–730.

Saxena K N, Kumar H. 1980. Interruption of acoustic communication and mating in a leafhopper and a planthopper by aerial sound vibrations picked up by plants. Experientia36, 933–936.

Schoofs L, Holman G M, Hayes T K, Nachman R J, De Loof A. 1991. Isolation, identification and synthesis of locustamyoinhibiting peptide (LOM-MIP), a novel biologically active neuropeptide from Locusta migratoriaRegulatory Peptides36, 111–119.

Shimoda M, Honda K I. 2013. Insect reactions to light and its applications to pest management. Applied Entomology and Zoology48, 413–421.

Shpak E, Leykam J F, Kieliszewski M J. 1999. Synthetic genes for glycoprotein design and the elucidation of hydroxyproline-O-glycosylation codes. Proceedings of the National Academy of Sciences of the United States of America96, 14736–14741.

Su Q, Lv J, Li W X, Sun J W, Li S H, Zhang W Q. 2021. Identification of putative abdominal vibration-related genes through transcriptome analyses in the brown planthopper (Nilaparvata lugens). Comparative Biochemistry and Physiology (Part D: Genomics and Proteomics), 39, 1–10.

Tanaka Y, Suetsugu Y, Yamamoto K, Noda H, Shinoda T. 2014. Transcriptome analysis of neuropeptides and G-protein coupled receptors (GPCRs) for neuropeptides in the brown planthopper Nilaparvata lugensPeptides53, 125–133.

Terhzaz S, Rosay P, Goodwin S F, Veenstra J A. 2007. The neuropeptide SIFamide modulates sexual behavior in DrosophilaBiochemical and Biophysical Research Communications352, 305–310.

Vandersmissen H P, Nachman R J, Vanden Broeck J. 2013. Sex peptides and MIPs can activate the same G protein-coupled receptor. General and Comparative Endocrinology188, 137–143.

Walker T J. 1988. Acoustic traps for agriculturally important insects. Florida Entomologist71, 484–492.

Wang S L, Wang W W, Ma Q, Shen Z F, Zhang M Q, Zhou N M, Zhang C X. 2019. Elevenin signaling modulates body color through the tyrosine-mediated cuticle melanism pathway. The FASEB Journal33, 9731–9741.

Williamson M, Lenz C, Winther A M, Nässel D R, Grimmelikhuijzen C J. 2001. Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin preprohormone from Drosophila melanogasterBiochemical and Biophysical Research Communications281, 544–550.

Wu S F, Zeng B, Zheng C, Mu X C, Zhang Y, Hu J, Zhang S, Gao C F, Shen J L. 2018. The evolution of insecticide resistance in the brown planthopper (Nilaparvata lugens Stål) of China in the period 2012–2016. Scientific Reports8, 4586.

Yamanaka N, Hua Y J, Roller L, Spalovská Valachová I, Mizoguchi A, Kataoka H, Tanaka Y. 2010. Bombyx prothoracicostatic peptides activate the sex peptide receptor to regulate ecdysteroid biosynthesis. Proceedings of the National Academy of Sciences of the United States of America107, 2060–2065.

Yanagisawa R, Suwa R, Takanashi T, Tatsuta H. 2021. Substrate-borne vibrations reduced the density of tobacco whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) infestations on tomato, Solanum lycopersicum: An experimental assessment. Applied Entomology and Zoology56, 157–163.

Yang C H, Rumpf S, Xiang Y, Gordon M D, Song W, Jan L Y, Jan Y N. 2009. Control of the postmating behavioral switch in Drosophila females by internal sensory neurons. Neuron61, 519–526.

Yapici N, Kim Y J, Ribeiro C, Dickson B J. 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature451, 33–37.

Yu B, Li D T, Lu J B, Zhang W X, Zhang C X. 2016. Seminal fluid protein genes of the brown planthopper, Nilaparvata lugensBMC Genomics17, 654.

Zeng Y, Zhou F H, Zhu D H. 2018. Fight outcome briefly affects the reproductive fitness of male crickets. Scientific Reports8, 9695.

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