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Downregulation of chitin synthase A gene by diallyl trisulfide, an active substance from garlic essential oil, inhibits oviposition and alters the morphology of adult Sitotroga cerealella

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Abstract

The Angoumois grain moth, Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae), is the most serious and destructive pest of stored commodities around the globe, particularly on wheat, rice and maize. Previously, we confirmed that diallyl trisulfide (DAT), an active substance from garlic essential oil, reduced oviposition of females after a fumigation at the sublethal concentration (LC20 = 0.015 µL/L); meanwhile, through transcriptome sequencing, we found that DAT significantly downregulates the expression of chitin synthase A (CHSA) gene. To gain a broader insight, we assessed effects of DAT and dsRNA of CHSA gene of S. cerealella (dsScerCHSA) on the morphology, physiology and oviposition of adult S. cerealella, and we found that ScerCHSA was expressed in the adult stage and observed higher in the cuticle. Furthermore, results indicated that DAT fumigation significantly downregulated the mRNA expression of ScerCHSA and inhibited moth oviposition at the sublethal concentration. Downregulation of ScerCHSA resulted in chitin reduction, epidermal disruption, morphological and physiological alterations. Meanwhile, silencing of ScerCHSA resulted in the oviposition reduction of the moth; moreover, the morphological and physiological alterations were similar to the group treated with DAT. Therefore, we conclude that DAT could regulate the expression of ScerCHSA at the transcriptional level, cause histological and morphological alteration and finally inhibit the moth oviposition, which proves DAT possesses the great potential for being used in pest control as a friendly biopesticide.

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References

  • Acheuk F, Cusson M, Doumandji-Mitiche B (2012) Effects of a methanolic extract of the plant Haplophyllum tuberculatum and of teflubenzuron on female reproduction in the migratory locust, Locusta migratoria (Orthoptera: Oedipodinae). J Insect Physiol 58:335–341

    Article  CAS  PubMed  Google Scholar 

  • Alenton RRR, Kondo H, Hirono I, Maningas MBB (2016) Gene silencing of VP9 gene impairs WSSV infectivity on Macrobrachium rosenbergii. Virus Res 214:65–70

    Article  CAS  PubMed  Google Scholar 

  • Ampasala DR, Zheng S, Zhang D, Ladd T, Doucet D, Krell PJ, Retnakaran A, Feng Q (2011) An epidermis-specific chitin synthase CDNA in Choristoneura fumiferana: cloning, characterization, developmental and hormonal-regulated expression. Arch Insect Biochem Physiol 76:83–96

    Article  CAS  PubMed  Google Scholar 

  • Ankri S, Mirelman D (1999) Antimicrobial properties of allicin from garlic. Micro Infect 1:125–129

    Article  CAS  Google Scholar 

  • Arakane Y, Muthkrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, Lorenzen MD, Kanost M, Beeman RW (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14:453–463

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Specht CA, Kramer KJ, Muthukrishnan S, Beeman RW (2008) Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 38:959–962

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Baguinon MC, Jasrapuria S, Chaudhari S, Doyungan A, Kramer KJ, Muthkrishnan S, Beeman RW (2011) Both UDP N-acetylglucosamine pyrophosphorylases of Tribolium castaneum are critical for molting, survival and fecundity. Insect Biochem Mol Biol 41:42–50

    Article  CAS  PubMed  Google Scholar 

  • Attia S, Grissa KL, Lognay G, Bitume E, Hance T, Mailleux AC (2013) A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides. J Pest Sci 86:361–386. https://doi.org/10.1007/s10340-013-0503-0

    Article  Google Scholar 

  • Belinato TA, Martins AJ, Lima JBP, Lima-Camara TNd, Peixoto AA, Valle D (2009) Effect of the chitin synthesis inhibitor triflumuron on the development, viability and reproduction of Aedes aegypti. Mem do Inst Oswal Cruz 104:43–47

    Article  CAS  Google Scholar 

  • Boshra SA (2007) Effect of high-temperature pre-irradiation on reproduction and mating competitiveness of male Sitotroga cerealella (Olivier) and their F1 progeny. J Stor Prod Res 43:73–78

    Article  Google Scholar 

  • Chang MM, Shah S, Wu M-Y, Zhang SS, Wu G, Yang FL (2020) Effect of diallyl trisulfide on the reproductive behavior of the grain moth, sitotroga cerealella (Lepidoptera: Gelechiidae). Insects 11:21

    Article  Google Scholar 

  • Farnesi LC, Brito JM, Linss JG, Pelajo MM, Valle D, Rezende G (2012) Physiological and morphological aspects of Aedes aegypti developing larvae: effects of the chitin synthesis inhibitor novaluron. PLoS ONE 7:e30363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fouad HA, Faroni L, Souza TW, Ribeir RC, Sousa FS, Zanuncio J (2014) Botanical extracts of plants from the Brazilian Cerrado for the integrated management of Sitotroga cerealella (Lepidoptera: Gelechiidae) in stored grain. J Stor Prod Res 57:6–11

    Article  Google Scholar 

  • Hogenkamp DG, Arakane Y, Zimoch L, Merzendorfer H, Kramer KJ, Beeman RW, Kanost MR, Specht CA, Muthukrishnan S (2005) Chitin synthase genes in Manduca sexta: characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochem Mol Biol 35:529–540

    Article  CAS  PubMed  Google Scholar 

  • Ioriatti C, Pasqualini E, Pasquier D, Tomasi C (2006) Efficacy baselines of seven insecticides against larvae of Pandemis heparana (Lepidoptera: Tortricidae). J Pest Sci 79:163

    Article  Google Scholar 

  • Iqbal J, Jilani G, Aslam M (2010) Growth inhibiting effects of plant extracts against the grain moth, Sitotroga cerealella (Oliv.) (Gelechiidae: Lepidoptera). Pak J Zool 1:42–45

    Google Scholar 

  • Kato N, Mueller CR, Fuchs JF, Wessely V, Lan Q, Christensen BM (2006) Regulatory mechanisms of chitin biosynthesis and roles of chitin in peritrophic matrix formation in the midgut of adult Aedes aegypti. Insect Biochem Mol Biol 36:1–9

    Article  CAS  PubMed  Google Scholar 

  • Kramer KJ, Koga D (1986) Insect chitin: physical state, synthesis, degradation and metabolic regulation. Insect Biochem 16:851–877

    Article  CAS  Google Scholar 

  • Kupferschmidt K (2013) A lethal dose of RNA. Am Assoc Adv Sci 341:732–733

    CAS  Google Scholar 

  • Lee YL, Cesario T, Wang Y, Shanbrom E, Thrupp L (2003) Antibacterial activity of vegetables and juices. Nutrition 19:994–996

    Article  CAS  PubMed  Google Scholar 

  • López JD, Latheef MA, Hoffmann WC (2011) Effect of hexaflumuron on feeding response and reproduction of bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) 1. Southwestern Entomol 36:247–260

    Article  Google Scholar 

  • Ma M, Chang MM, Lei CL, Yang FL (2016) A garlic substance disrupts odorant-binding protein recognition of insect pheromones released from adults of the angoumois grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Mol Biol 25:530–540

    Article  CAS  PubMed  Google Scholar 

  • Ma M, Ying YY, He ZY, Lu Y, Li XG, Lei CL, Yang FL (2017) Comparative transcriptome analysis reveals potential gene targets for ovipositional inhibition by diallyl trisulfide against female Sitotroga cerealella Agri. Gene 5:12–18

    Google Scholar 

  • Macedo L, Junior JD, Coelho R, Fonseca F, Firmino A, Silva M, Fragoso R, Albuquerque E, Silva MS, Engler J, Terra W, Grossi M (2017) Knocking down chitin synthase 2 by RNAi is lethal to the cotton boll weevil. Biotech Res Inn 1:72–86

    Article  Google Scholar 

  • Matsumura F (2010) Studies on the action mechanism of benzoylurea insecticides to inhibit the process of chitin synthesis in insects: a review on the status of research activities in the past, the present and the future prospects. Pest Biochem Physio 97:133–139

    Article  CAS  Google Scholar 

  • Merzendorfer H (2006) Insect chitin synthases: a review. J Com Physio B 176:1–15

    Article  CAS  Google Scholar 

  • Miron T, Mironchik M, Mirelman D, Wilchek M, Rabinkov A (2003) Inhibition of tumor growth by a novel approach: in situ allicin generation using targeted alliinase delivery. Mol Cancer Therap 2:1295–1301

    CAS  Google Scholar 

  • Mohammed AM, Diab MR, Abdelsattar M, Sayed M (2017) Characterization and RNAi-mediated knockdown of Chitin Synthase A in the potato tuber moth, Phthorimaea operculella. Sci Rep 7:1–12

    Article  CAS  Google Scholar 

  • Moreira MF, Santos AS, Marotta H, Mansur JF, Ramos IB, Machado E, Souza G, Eberlin M, Kaiser C, Kramer KJ, Muthukrishnan S, Vasconcellos AM (2007) A chitin-like component in Aedes aegypti eggshells, eggs and ovaries. Insect Biochem Mol Biol 37:1249–1261

    Article  CAS  PubMed  Google Scholar 

  • Nunes FMF, Simões ZLP (2009) A non-invasive method for silencing gene transcription in honeybees maintained under natural conditions. Insect Biochem Mol Biol 39:157–160

    Article  CAS  PubMed  Google Scholar 

  • Nunes FM, Aleixo AC, Barchuk AR, Bomtorin AD, Grozinger CM, Simões ZL (2013) Non-target effects of green fluorescent protein (GFP)-derived double-stranded RNA (dsRNA-GFP) used in honey bee RNA interference (RNAi) assays. Insects 4:90–103

    Article  PubMed  PubMed Central  Google Scholar 

  • Ostrowski S, Dierick HA, Bejsovec AJG (2002) Genetic control of cuticle formation during embryonic development of Drosophila melanogaster. Genetics 161:171–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rezende GL, Martins AJ, Gentile C, Farnesi LC, Pelajo MM, Peixoto AA, Valle D (2008) Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Develop Biol 8:82

    Article  CAS  Google Scholar 

  • Shah FM, Razaq M, Ali Q, Shad SA, Aslam M, Hardy IC (2019) Field evaluation of synthetic and neem-derived alternative insecticides in developing action thresholds against cauliflower pests. Sci Rep 9:7684

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sohail S, Tariq K, Zheng W, Ali MW, Peng W, Raza MF, Zhang H (2019) RNAi-mediated knockdown of Tssk1 and Tektin1 genes impair male fertility in bactrocera dorsalis. Insects 10:164

    Article  PubMed Central  Google Scholar 

  • Tang B, Chen X, Liu Y, Tian H, Liu J, Hu J, Xu W, Zhang W (2008) Characterization and expression patterns of a membrane-bound trehalase from Spodoptera exigua. BMC Mol Biol 9:51

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tatun N, Singtripop T, Tungjitwitayakul J, Sakurai S (2008) Regulation of soluble and membrane-bound trehalase activity and expression of the enzyme in the larval midgut of the bamboo borer Omphisa fuscidentalis. Insect Biochem Mol Biol 38:788–795

    Article  CAS  PubMed  Google Scholar 

  • Tavares WS, Costa MA, Cruz I, Silveira RD, Serrao JE, Zanuncio JC (2010) Selective effects of natural and synthetic insecticides on mortality of Spodoptera frugiperda (Lepidoptera: Noctuidae) and its predator Eriopis connexa (Coleoptera: Coccinellidae). J Environ Sci Health Part B 45:557–561

    Article  CAS  Google Scholar 

  • Terenius TO, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, Kanginakudru S, Albrechtsen M, An C, Aymeric JL, Barthel AB (2011) RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57:231–245

    Article  CAS  PubMed  Google Scholar 

  • Trematerra P (2015) Adult dispersal of Sitotroga cerealella in a conventional small-farm in Southern Italy. Bull Insecto 68:111–118

    Google Scholar 

  • Yan S, Qian J, Cai C, Ma Z, Li J, Yin M, Shen J (2020) Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycines. J Pest Sci 93:449–459. https://doi.org/10.1007/s10340-019-01157-x

    Article  Google Scholar 

  • Yang FL, Zhu F, Lei CL (2010) Garlic essential oil and its major component as fumigants for controlling Tribolium castaneum (Herbst) in chambers filled with stored grain. J Pest Sci 83:311–317

    Article  Google Scholar 

  • Yang FL, Zhu F, Lei CL (2012) Insecticidal activities of garlic substances against adults of grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Sci 19:205–212

    Article  Google Scholar 

  • Yang WJ, Xu KK, Cong L, Wang JJ (2013) Identification, mRNA expression, and functional analysis of chitin synthase 1 gene and its two alternative splicing variants in oriental fruit fly, Bactrocera dorsalis. Int J Biol Sci 9:331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yao Q, Zhang D, Tang B, Chen J, Chen J, Lu L, Zhang W (2010) Identification of 20-hydroxyecdysone late-response genes in the chitin biosynthesis pathway. PLoS ONE 5:e14058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoza KI, Imamura T, Kramer KJ, Morgan TD, Nakamura S, Akiyama K, Ohtsubo KI (2005) Avidin expressed in transgenic rice confers resistance to the stored-product insect pests Tribolium confusum and Sitotroga cerealella. Biosci Biotech Biochem 69:966–971

    Article  CAS  Google Scholar 

  • Yu N, Christiaens O, Liu J, Niu J, Cappelle K, Caccia S, Huvenne H, Smagghe G (2013) Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci 20:4–14

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Liu X, Zhang J, Li D, Sun Y, Guo Y, Ma E, Zhu KY (2010) Silencing of two alternative splicing-derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect Biochem Mol Biol 40:824–833

    Article  CAS  PubMed  Google Scholar 

  • Zhuo W, Fang Y, Kong L, Li X, Sima Y, Xu S (2014) Chitin synthase A: a novel epidermal development regulation gene in the larvae of Bombyx mori. Mol Biol Rep 41:4177–4186

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Abbas for kind help in microscopy. This work was supported by the National Natural Science Foundation of China (31871955), the National Key Research and Development Program of China (2018YFD0201009), the National Genetically Modified Organisms Breeding Major Project (2016ZX08012-005), Hubei Provincial Natural Science Foundation of China (2017CFB541), Fundamental Research Funds for the Central Universities (No.2662017JC032) and the China Scholarship Council (CSC) to Sakhawat shah.

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Shah, S., Hafeez, M., Wu, MY. et al. Downregulation of chitin synthase A gene by diallyl trisulfide, an active substance from garlic essential oil, inhibits oviposition and alters the morphology of adult Sitotroga cerealella. J Pest Sci 93, 1097–1106 (2020). https://doi.org/10.1007/s10340-020-01226-6

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