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Journal of Integrative Agriculture  2024, Vol. 23 Issue (7): 2346-2361    DOI: 10.1016/j.jia.2023.11.030
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The biosynthesis of alarm pheromone in the wheat aphid Rhopalo-siphum padi is regulated by hormones via fatty acid metabolism
Chengxian Sun1*, Yaoguo Qin1, 2*, Julian Chen2#, Zhengxi Li1#
1 Department of Entomology/Ministry of Agriculture Key Laboratory for Monitoring and Environment-friendly Control of Crop Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China
2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
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摘要  在世界范围内严重危害农业和林业的蚜虫受到天敌攻击后会释放报警信息素以保护其种群。绝大多数蚜虫报警信息素的主要成分是一种倍半萜烯化合物——反式-β-法尼烯(EβF)。然而其生物合成和调控机制至今尚未阐释清楚。本研究以禾谷缢管蚜这一危害小麦的重要害虫为对象究EβF在蚜虫体内的生物合成机制。本研究发现禾谷缢管蚜仅在成熟胚胎和12龄蜕皮期合成EβF蚜虫腹末端充足的甘油三酯是EβF储存和释放的前提条件。通过转录组测序、RNA干扰、激素处理和定量检测等方法,后续研究发现禾谷缢管蚜利用脂肪酸降解途径产生的乙酰辅酶A为源头生物合成EβF。保幼激素抑制这此过程,而蜕皮激素通过调控脂肪酸代谢促进此过程。本研究首次系统地就蚜虫合成EβF的调控方式进行了探索,为后续研究蚜虫报警信息素生物合成的分子调控机制提供了新思路,也为制定蚜虫防治新策略提供了有价值的信息。

Abstract  

Aphids are major insect pests in agriculture and forestry worldwide. Following attacks by natural enemies, many aphids release an alarm pheromone to protect their population. In most aphids, the main component of the aphid alarm pheromone (AAP) is the sesquiterpene hydrocarbon (E)-β-farnesene (EβF). However, the mechanisms behind its biosynthesis and regulation remain poorly understood. In this study, we used the bird cherry–oat aphid Rhopalosiphum padi, which is an important wheat aphid, to investigate the regulatory mechanisms of EβF biosynthesis. Our results showed that EβF biosynthesis occurs during the mature embryo period and the molting period of the 1st- and 2nd-instar nymphs. Triglycerides provide the prerequisite material for EβF production and release. Based on transcriptome sequencing, RNAi analysis, hormone treatments, and quantitative measurements, we found that the biosynthesis of EβF utilizes acetyl coenzyme A produced from fatty acid degradation, which can be suppressed by juvenile hormone but it is promoted by 20-hydroxyecdysone through the modulation of fatty acid metabolism. This is the first systemic study on the modulation of EβF production in aphids. The results of our study provide insights into the molecular regulatory mechanisms of AAP biosynthesis, as well as valuable information for designing potential aphid control strategies.


Keywords:  (E)-β-farnesene       critical period for biosynthesis        fatty acid metabolism        juvenile hormone        20-hydroxyecdysone  
Received: 23 May 2023   Accepted: 16 October 2023
Fund: 
This work was supported by the National Natural Science Foundation of China (31972267 and 3227253) and the Chinese Universities Scientific Fund (2023TC109).
About author:  Chengxian Sun, Mobile: +86-18813117876, E-mail: wsyenan@163.com; Yaoguo Qin, E-mail: qinyaoguo@cau.edu.cn; #Correspondence Julian Chen, Tel: +86-10-62815934, E-mail: chenjulian@caas.cn; Zhengxi Li, Mobile: +86-13121868836, E-mail: zxli@cau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Chengxian Sun, Yaoguo Qin, Julian Chen, Zhengxi Li. 2024. The biosynthesis of alarm pheromone in the wheat aphid Rhopalo-siphum padi is regulated by hormones via fatty acid metabolism. Journal of Integrative Agriculture, 23(7): 2346-2361.

Arrese E L, Soulages, J L. 2010. Insect fat body: Energy, metabolism, and regulation. Annual Review of Entomology55, 207–225.

Athenstaedt K, Daum G. 2006. The life cycle of neutral lipids: Synthesis, storage and degradation. Cellular and Molecular Life Sciences63, 1355–1369.

Baumann A A, Benoit J B, Michalkova V, Mireji P, Attardo G M, Moulton, J K, Wilson T G, Aksoy S. 2013. Juvenile hormone and insulin suppress lipolysis between periods of lactation during tsetse fly pregnancy. Molecular and Cellular Endocrinology372, 30–41.

Bellés X, Martín D, Piulachs M D. 2005. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annual Review of Entomology50, 181–199.

Callow R K, Greenway A R, Griffiths D C. 1973. Chemistry of the secretion from the cornicles of various species of aphids. Journal of Insect Physiology19, 737e748.

Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant13, 1194–1202.

Chen N, Liu Y J, Fan Y L, Pei X J, Yang Y, Liao M T, Zhong J, Li N, Liu T X, Wang G, Pan Y, Schal C, Li S. 2022. A single gene integrates sex and hormone regulators into sexual attractiveness. Nature Ecology and Evolution6, 1180–1190.

Cheng Y J, Li Z X. 2019. Both farnesyl diphosphate synthase genes are involved in the production of alarm pheromone in the green peach aphid Myzus persicaeArchives of Insect Biochemistry and Physiology100, e21530.

Crock J, Wildung M, Croteau R. 1997. Isolation and bacterial expression of a sesquiterpene synthase cDNA clone from peppermint (Mentha×piperita, L.) that produces the aphid alarm pheromone (E)-β-farnesene. Proceedings of the National Academy of Sciences of the United States of America94, 12833–12838.

Dixon A F G. 1958. The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Ecological Entomology110, 319–334.

Du M F, Liu X M, Ma N N, Liu X G, Wei J Z, Yin X M, Zhou S T, Rafaeli A, Song Q S, An S H. 2017. Calcineurin-mediated dephosphorylation of acetyl-coA carboxylase is required for pheromone biosynthesis activating neuropeptide (PBAN)-induced sex pheromone biosynthesis in Helicoverpa armigeraMolecular and Cellular Proteomics16, 2138–2152.

van Emden H F, Dingley J, Dewhirst S Y, Pickett J A, Woodcock C M, Wadhams L J. 2014. The effect of artificial diet on the production of alarm pheromone by Myzus persicaePhysiological Entomology39, 285–291.

van Emden H F, Harrington R. 2017. Aphids as Crop Pests. Commonwealth Agricultural Bureaux International, UK. pp. 717.

Guo Z J, Kang S, Sun D, Gong L J, Zhou J L, Qin J Y, Guo L, Zhu L H, Bai Y, Ye F, Wu Q J, Wang S L, Crickmore N, Zhou X G, Zhang Y J. 2020. MAPK-dependent hormonal signaling plasticity contributes to overcoming Bacillus thuringiensis toxin action in an insect host. Nature Communications11, 3003.

Hossain M S, Liu Y, Zhou S, Li K, Tian L, Li S. 2013. 20-Hydroxyecdysone-induced transcriptional activity of FoxO upregulates brummer and acid lipase-1 and promotes lipolysis in Bombyx fat body. Insect Biochemistry and Molecular Biology43, 829–838.

Hull J J, Fónagy A. 2020. A sexy moth model–the molecular basis of sex pheromone biosynthesis in the silkmoth Bombyx mori. In: Ishikawa Y, ed., Insect Sex Pheromone Research and Beyond. Springer Publishers, Singapore. pp. 111–150.

Jayasinghe W H, Akhter M S, Nakahara K, Maruthi M N. 2022. Effect of aphid biology and morphology on plant virus transmission. Pest Management Science78, 416–427.

Jindra M, Palli S R, Riddiford L M. 2013. The juvenile hormone signaling pathway in insect development. Annual Review of Entomology58, 181–204.

Kang P, Chang K, Liu Y, Bouska M, Birnbaum A, Karashchuk G, Thakore R, Zheng W J, Post S, Brent C S, Li S, Tatar M, Bai H. 2017. Drosophila Kruppel homolog 1 represses lipolysis through interaction with dFOXO. Scientific Reports7, 16369.

Köllner T G, David A, Luck K, Beran F, Kunert G, Zhou J J, Caputi L, O’Connor S E. 2022. Biosynthesis of iridoid sex pheromones in aphids. Proceedings of the National Academy of Sciences of the United States of America119, e2211254119.

Li B, Dewey C N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics12, 323.

Li K, Jia Q Q, Li S. 2019. Juvenile hormone signaling - a mini review. Insect Science26, 600–606.

Liu J H, Zhao X J, Zhan Y D, Wang K, Francis F, Liu Y. 2021. New slow release mixture of (E)-β-farnesene with methyl salicylate to enhance aphid biocontrol efficacy in wheat ecosystem. Pest Management Science77, 3341–3348.

Maruyama T, Ito M, Kiuchi F, Honda G. 2001. Molecular cloning, functional expression and characterization of d-limonene synthase from Schizonepeta tenuifoliaBiological and Pharmaceutical Bulletin24, 373–377.

Michaud J P. 2022. The ecological significance of aphid cornicles and their secretions. Annual Review of Entomology67, 65–81.

Miller G L, Foottit R G. 2017. The Taxonomy of Crop PestsThe Aphids. In: Foottit R G, Adler P H, eds., Insect BiodiversityScience and Society. Wiley-Blackwell Publishing, UK. pp. 463–473.

Moayeri H R S, Mohandesi A R, Ashouri A. 2012. Fitness costs of cornicle secretions as a defense mechanism for cotton aphid, Aphis gossypii (Hem.: Aphididae). Journal of Entomological Society of Iran31, 51–61.

Mondor E B, Roitberg B D. 2003. Age-dependent fitness costs of alarm signaling in aphids. Canadian Journal of Zoology81, 757–762.

Oluwafemi S, Bruce T J, Pickett J A, Ton J, Birkett M A. 2011. Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. Journal of Chemical Ecology37, 40–48.

Pei X J, Fan Y L, Bai Y, Bai T T, Schal C, Zhang Z F, Chen N, Li S, Liu T X. 2021. Modulation of fatty acid elongation in cockroaches sustains sexually dimorphic hydrocarbons and female attractiveness. PLoS Biology19, e3001330.

Riddiford L M A. 2020. Life’s journey through insect metamorphosis. Annual Review of Entomology65, 1–16.

Robinson M D, McCarthy D J, Smyth G K. 2010. edgeR: A Bioconductor package for diferential expression analysis of digital gene expression data. Bioinformatics26, 139–140.

Schwartzberg E G, Kunert G, Stephan C. 2008. Real-time analysis of alarm pheromone emission by the pea aphid (Acyrthosiphon Pisum) under predation. Journal of Chemical Ecology34, 76–81.

Simon J C, Peccoud J. 2018, Rapid evolution of aphid pests in agricultural environments. Current Opinion in Insect Science26, 17–24.

Sun Z J, Li Z X. 2017. Host plants and obligate endosymbionts are not the sources for biosynthesis of the aphid alarm pheromone. Scientific Reports7, 6041.

Sun Z J, Li Z X. 2018. The terpenoid backbone biosynthesis pathway directly affects the biosynthesis of alarm pheromone in the aphid. Insect Molecular Biology27, 824–834.

Sun C X, Li Z X. 2019. Production of alarm pheromone starts at embryo stage and is modulated by rearing conditions and farnesyl diphosphate synthase genes in the bird cherry-oat aphid Rhopalosiphum padiBulletin of Entomological Research109, 821–830.

Sun C X, Li Z X. 2021. Biosynthesis of aphid alarm pheromone is modulated in response to starvation stress under regulation by the insulin, glycolysis and isoprenoid pathways. Journal of Insect Physiology128, 104174.

Tang Q Y, Zhang C X. 2013. Data processing system (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Science20, 254–260.

Tillman J A, Seybold S J, Jurenka R A, Blomquist G J. 1999. Insect pheromones - an overview of biosynthesis and endocrine regulation. Insect Biochemistry and Molecular Biology29, 481–514.

Turlings T C, Tumlinson J H, Heath R R, Proveaux A T, Doolittle R E. 1991. Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. Journal of Chemical Ecology17, 2235–2251.

Vandermoten S, Mescher M C, Francis F, Haubruge E, Verheggen F J. 2012. Aphid alarm pheromone: An overview of current knowledge on biosynthesis and functions. Insect Biochemistry and Molecular Biology42, 155–163.

Verheggen F J, Haubruge E, De Moraes C M, Mescher M C. 2009. Social enviroment influences aphid production of alarm pheromone. Behavioral Ecology20, 283–288.

Wang B, Dong W Y, Li H M, D’Onofrio C, Bai P H, Chen R P, Yang L L, Wu J N, Wang X Q, Wang B, Ai D, Knoll W, Pelosi P, Wang G R. 2022. Molecular basis of (E)-β-farnesene-mediated aphid location in the predator Eupeodes corollaeCurrent Biology32, 951–962.e7.

Wang S, Liu S M, Liu H H, Wang J W, Zhou S, Jiang R J, Bendena W G, Li S. 2010. 20-Hydroxyecdysone reduces insect food consumption resulting in fat body lipolysis during molting and pupation. Journal of Molecular Cell Biology2, 128–138.

Wang X L, Hou Y, Saha T T, Pei G G, Raikhel A S, Zou Z. 2017. Hormone and receptor interplay in the regulation of mosquito lipid metabolism. Proceedings of the National Academy of Sciences of the United States of America114, E2709–E2718.

Wang Y L, Yang H, Geerts C, Furtos A, Waters P, Cyr D, Wang S P, Mitchell G A. 2022. The multiple facets of acetyl-CoA metabolism: Energetics, biosynthesis, regulation, acylation and inborn errors. Molecular Genetics and Metabolism138, 106966.

Yan S, Qian J, Cai C, Ma Z Z, Li J H, Yin M Z, Ren B Y, Shen J. 2020. Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycinesJournal of Pest Science93, 449–459.

Zhang R B, Wang B, Grossi G, Falabella P, Liu Y, Yan S C, Lu J, Xi J H, Wang G R. 2016. Molecular basis of alarm pheromone detection in aphids. Current Biology27, 55–61.

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