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A potential genetic control by suppression of the wing developmental gene wingless in a global invasive pest Bactrocera dorsalis

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Abstract

The adverse effects of invasive pests on ecosystems have gradually intensified, and the prevention of invasive pests is a long-standing research focus. Genetic control strategies are effective, sustainable and environmentally friendly methods for controlling pests and have received substantial attention worldwide. However, there is a lack of researches on the genetic control of Bactrocera dorsalis Hendel, a global invasive pest with strong flight ability. The wing of B. dorsalis as an important flight organ may be a main reason for its widespread occurrence. Here, we first analysed the wing structure of B. dorsalis and found that its wing has the typical characteristic of Diptera insect wing. The spatiotemporal expressions of the wing development genes were examined by quantitative real-time PCR, antibody staining and RNA in situ hybridization. The results indicated that the wing development genes were significantly upregulated in the pupal stage, and the regional expression of each gene was clarified. Wingless (wg), a key gene that significantly affects wing development, was selected from nine genes through RNA interference and used to simulate the field control of B. dorsalis. The offspring population and the fruit-borer rate decreased significantly after the simulated control. This study provides preliminary support for the application of genetic pest control by regulating the wing development gene and proposes a novel idea for solving the problem of the extensive spread of B. dorsalis.

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References

  • Aketarawong N, Chinvinijkul S, Orankanok W, Guglielmino CR, Franz G, Malacrida AR, Thanaphum S (2011) The utility of microsatellite DNA markers for the evaluation of area-wide integrated pest management using SIT for the fruit fly, Bactrocera dorsalis (Hendel), control programs in Thailand. Genetica 139:129–140

    PubMed  Google Scholar 

  • Blair SS, Brower DL, Thomas JB, Zavortink M (1994) The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120:1805

    CAS  PubMed  Google Scholar 

  • Brisson JA, Ishikawa A, Miura T (2010) Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs. Insect Mol Biol 192:63–73

    Google Scholar 

  • Bruno Wilke AB, Marrelli MT (2012) Genetic control of mosquitoes: population suppression strategies. Rev Inst Med Trop Sao Paulo 54:287–292

    Google Scholar 

  • Chen C, Huang H, Ward CM, Su JT, Schaeffer LV, Guo M, Hay BA (2007) A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila. Science 316:597–600

    CAS  PubMed  Google Scholar 

  • Clarke AR, Armstrong KF, Carmichael AE, Milne JR, Raghu S, Roderick GK, Yeates DK (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu Rev Entomol 50:293–319

    CAS  PubMed  Google Scholar 

  • Clarke AR, Li ZH, Qin YJ, Zhao ZH, Liu LJ, Schutze MK (2019) Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is not invasive through Asia: it’s been there all along. J Appl Entomol 143(8):797–801

    Google Scholar 

  • Ekesi S, De Meyer M, Mohamed SA, Virgilio M, Borgemeister C (2016) Taxonomy, ecology, and management of native and exotic fruit fly species in Africa. Annu Rev Entomol 61:219–238

    CAS  PubMed  Google Scholar 

  • Fabricius JC (1794) Entomologia systematica emendata et aucta, vol 4. Impensis Christ. Gottl. Proft., Copenhagen

    Google Scholar 

  • Fraimout A et al (2018) Phenotypic plasticity of Drosophila suzukii wing to developmental temperature: implications for flight. J Exp Biol 221:jeb166868

    Google Scholar 

  • Grimaldi DA, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Grimm S, Pflugfelder GO (1996) Control of the gene optomotor-blind in Drosophila wing development by decapentaplegic and wingless. Science 271:1601–1604

    CAS  PubMed  Google Scholar 

  • Guo S, Zhao Z, Liu L, Li Z, Shen J (2018) Comparative transcriptome analyses uncover key candidate genes mediating flight capacity in Bactrocera dorsalis (Hendel) and Bactrocera correcta (Bezzi) (Diptera: Tephritidae). Int J Mol Sci 19:396

    PubMed Central  Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Google Scholar 

  • Hu J, Chen B, Li Z (2014) Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. J Insect Physiol 67:105–113

    CAS  PubMed  Google Scholar 

  • James AA (2005) Gene drive systems in mosquitoes: rules of the road. Trends Parasitol 21:64–67

    CAS  PubMed  Google Scholar 

  • Li J, Qian J, Xu Y, Yan S, Shen J, Yin M (2019) A facile-synthesized star polycation constructed as a highly efficient gene vector in pest management. ACS Sustain Chem Eng 7:6316–6322

    CAS  Google Scholar 

  • Liu X, Jin Y, Ye H (2013) Recent spread and climatic ecological niche of the invasive guava fruit fly, Bactrocera correcta, in mainland China. J Pest Sci 86:449–458

    Google Scholar 

  • Liu G, Wu Q, Li J, Zhang G, Wan F (2015) RNAi-mediated knock-down of transformer and transformer 2 to generate male-only progeny in the oriental fruit fly, Bactrocera dorsalis (Hendel). PLoS ONE 10:e0128892

    PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    CAS  Google Scholar 

  • Medved V, Marden JH, Fescemyer HW, Der JP, Liu J, Mahfooz N, Popadic A (2015) Origin and diversification of wings: insights from a neopteran insect. Proc Natl Acad Sci USA 112:15946–15951

    CAS  PubMed  Google Scholar 

  • Nugnes F, Russo E, Viggiani G, Bernardo U (2018) First record of an invasive fruit fly belonging to Bactrocera dorsalis complex (Diptera: Tephritidae) in Europe. Insects 9:182

    PubMed Central  Google Scholar 

  • Permpoon R, Aketarawong N, Thanaphum S (2011) Isolation and characterization of Doublesex homologues in the Bactrocera species: B. dorsalis (Hendel) and B. correcta (Bezzi) and their putative promoter regulatory regions. Genetica 139:113–127

    CAS  PubMed  Google Scholar 

  • Qin Y et al (2018) Population structure of a global agricultural invasive pest, Bactrocera dorsalis (Diptera: Tephritidae). Evol Appl 11:1990–2003

    PubMed  PubMed Central  Google Scholar 

  • Qin Y, Wang C, Zhao Z, Pan X, Li Z (2019) Climate change impacts on the global potential geographical distribution of the agricultural invasive pest, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Clim Change 155:145–156

    Google Scholar 

  • Ray RP, Nakata T, Henningsson P, Bomphrey RJ (2016) Enhanced flight performance by genetic manipulation of wing shape in Drosophila. Nat Commun 7:10851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez DD, Felix JT, Diaz-Benjumea FJ (2004) The role of the T-box gene optomotor-blind in patterning the Drosophila wing. Dev Biol 268:481–492

    Google Scholar 

  • Schliekelman P, Ellner S, Gould F (2005) Pest control by genetic manipulation of sex ratio. J Econ Entomol 98:18–34

    PubMed  Google Scholar 

  • Shen Z (2009) Insect ecology and ecological principles of IPM. China Agricultural University Press, Beijing

    Google Scholar 

  • Shen D (2014) Systemically interfering with immune response by a fluorescent cationic dendrimer delivered gene suppression. J Mater Chem B 2:4653–4659

    CAS  PubMed  Google Scholar 

  • Shen J, Dahmann C, Pflugfelder GO (2010) Spatial discontinuity of Optomotor-blind expression in the Drosophila wing imaginal disc disrupts epithelial architecture and promotes cell sorting. BMC Dev Biol 10:23

    PubMed  PubMed Central  Google Scholar 

  • Shi Y et al (2019) The ecdysis triggering hormone system, via ETH/ETHR-B, is essential for successful reproduction of a major pest insect, Bactrocera dorsalis (Hendel). Front Physiol 10:151

    PubMed  PubMed Central  Google Scholar 

  • Stephens AEA, Kriticos DJ, Leriche A (2007) The current and future potential geographical distribution of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Bull Entomol Res 97:369–378

    CAS  PubMed  Google Scholar 

  • Tomoyasu Y, Wheeler SR, Denell RE (2005) Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433:643–647

    CAS  PubMed  Google Scholar 

  • Wan X, Nardi F, Zhang B, Liu Y (2011) The oriental fruit fly, Bactrocera dorsalis, in China: origin and gradual inland range expansion associated with population growth. PLoS ONE 6:e2523810

    Google Scholar 

  • Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12:1474–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. Environ Entomol 22:1408

    Google Scholar 

  • Wimmer EA (2005) Eco-friendly insect management. Nat Biotechnol 23:432–433

    CAS  PubMed  Google Scholar 

  • Yuan S, Kong Q, Xiao C, Yang S, Sun W, Zhang J, Li Z (2006) Introduction to two kinds of artificial diets for mass rearing of adult Bactrocera dorsalis (Hendel). J Huazhong Agric Univ 25:371–374

    Google Scholar 

  • Zecca M, Struhl G (2007) Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation. Development 134:3001–3010

    CAS  PubMed  Google Scholar 

  • Zeng Y et al (2019) Global distribution and invasion pattern of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). J Appl Entomol 143:165–176

    Google Scholar 

  • Zhang X, Luo D, Pflugfelder GO, Shen J (2013) Dpp signaling inhibits proliferation in the Drosophila wing by Omb-dependent regional control of bantam. Development 140:2917–2922

    CAS  PubMed  Google Scholar 

  • Zhang J et al (2019) Identification of COP9 signalosome subunit genes in Bactrocera dorsalis and functional analysis of csn3 in female fecundity. Front Physiol 10:162

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Professor Yin Meizhen from Beijing University of Chemical Technology for providing the nanocarriers. This research was financially supported by Natural Science Foundation of Beijing Municipality [6172021, 6182020] and the National Natural Science Foundation of China [31872295].

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Authors and Affiliations

  1. Department of Entomology, MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing, 100193, China

    Shaokun Guo, Xiaoyu Guo, Linyu Zheng, Zihua Zhao, Lijun Liu, Jie Shen & Zhihong Li

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  1. Shaokun Guo
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  2. Xiaoyu Guo
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  3. Linyu Zheng
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  4. Zihua Zhao
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  5. Lijun Liu
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  6. Jie Shen
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  7. Zhihong Li
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Correspondence to Jie Shen or Zhihong Li.

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Guo, S., Guo, X., Zheng, L. et al. A potential genetic control by suppression of the wing developmental gene wingless in a global invasive pest Bactrocera dorsalis. J Pest Sci 94, 517–529 (2021). https://doi.org/10.1007/s10340-020-01263-1

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  • DOI: https://doi.org/10.1007/s10340-020-01263-1

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