Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-26T06:21:44.766Z Has data issue: false hasContentIssue false
  • English
  • Français

Mechanistic effects of microwave radiation on pupal emergence in the leafminer fly, Liriomyza trifolii

Published online by Cambridge University Press:  12 December 2022

Ya-Wen Chang Open the ORCID record for Ya-Wen Chang [Opens in a new window] ,
Yue Zhang ,
Yu-Qing Yan ,
Yu-Cheng Wang ,
Cheng-Dong Wu ,
Jie Hu  and
Yu-Zhou Du Open the ORCID record for Yu-Zhou Du [Opens in a new window]
Ya-Wen Chang
Affiliation:
School of Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, China
Yue Zhang
Affiliation:
School of Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, China
Yu-Qing Yan
Affiliation:
School of Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, China
Yu-Cheng Wang
Affiliation:
School of Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, China
Cheng-Dong Wu
Affiliation:
Pukou Agricultural Technology Extension Center of Nanjing City, Pukou, China
Jie Hu
Affiliation:
Plant Protection and Quarantine Station of Jiangsu Province, Nanjing, China
Yu-Zhou Du*
Affiliation:
School of Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou, China Joint International Research Laboratory of Agriculture and Agri-Product Safety, the Ministry of Education, Yangzhou University, Yangzhou, China
*
Author for correspondence: Yu-Zhou Du, Email: yzdu@yzu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Liriomyza trifolii is a significant pest of vegetable and ornamental crops across the globe. Microwave radiation has been used for controlling pests in stored products; however, there are few reports on the use of microwaves for eradicating agricultural pests such as L. trifolii, and its effects on pests at the molecular level is unclear. In this study, we show that microwave radiation inhibited the emergence of L. trifolii pupae. Transcriptomic studies of L. trifolii indicated significant enrichment of differentially expressed genes (DEGs) in ‘post-translational modification, protein turnover, chaperones’, ‘sensory perception of pain/transcription repressor complex/zinc ion binding’ and ‘insulin signaling pathway’ when analyzed with the Clusters of Orthologous Groups, Gene Ontology and the Kyoto Encyclopedia of Genes and Genomes databases, respectively. The top DEGs were related to reproduction, immunity and development and were significantly expressed after microwave radiation. Interestingly, there was no significant difference in the expression of genes encoding heat shock proteins or antioxidant enzymes in L. trifolii treated with microwave radiation as compared to the untreated control. The expression of DEGs encoding cuticular protein and protein takeout were silenced by RNA interference, and the results showed that knockdown of these two DEGs reduced the survival of L. trifolii exposed to microwave radiation. The results of this study help elucidate the molecular response of L. trifolii exposed to microwave radiation and provide novel ideas for control.

Keywords

Differentially expressed genesLiriomyza trifoliimicrowave radiationRNAitranscriptome analysis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 2 , April 2023 , pp. 282 - 291
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamo, SA (2012) The effects of the stress response on immune function in invertebrates: an evolutionary perspective on an ancient connection. Hormones and Behavior 62, 324–330.CrossRefGoogle Scholar
Adamo, SA (2017) Stress responses sculpt the insect immune system, optimizing defense in an ever-changing world. Developmental and Comparative Immunology 66, 24–32.CrossRefGoogle Scholar
Anders, S and Huber, W (2010) Differential expression analysis for sequence count data. Genome Biology 11, R106.CrossRefGoogle ScholarPubMed
Barbosa, DRE, Fontes, LD, Silva, PRR, Neves, JA, de Melo, AF and Esteves, AB (2017) Microwave radiation to control Callosobruchus maculatus (Coleoptera: Chrysomelidae) larvae in cowpea cultivars. Austral Entomology 56, 70–74.CrossRefGoogle Scholar
Baum, JA and Roberts, JK (2014) Progress towards RNAi-mediated insect pest management. Advances in Insect Physiology 47, 249–295.CrossRefGoogle Scholar
Bedi, SS and Singh, M (1992) Microwaves for control of stored grain insects. National Academy Science Letters 15, 195–197.Google Scholar
Burand, JP and Hunter, WB (2013) RNAi: future in insect management. Journal of Invertebrate Pathology 112, S68–S74.CrossRefGoogle ScholarPubMed
Calabrò, E, Condello, S, Currò, M, Ferlazzo, N, Caccamo, D, Magazù, S and Ientile, R (2012) Modulation of heat shock protein response in SH-SY5Y by mobile phone microwaves. World Journal of Biological Chemistry 3, 34–40.CrossRefGoogle ScholarPubMed
Chang, YW, Chen, JY, Lu, MX, Gao, Y, Tian, ZH, Gong, WR, Zhu, W and Du, YZ (2017) Selection and validation of reference genes for quantitative real time PCR analysis under different experimental conditions in the leafminer Liriomyza trifolii (Diptera: Agromyzidae). PLoS One 12, e0181862.CrossRefGoogle ScholarPubMed
Chang, YW, Wang, YC, Zhang, XX, Iqbal, J, Lu, MX, Gong, HX and Du, YZ (2020 a) Comparative transcriptome analysis of three invasive leafminer flies provides insights into interspecific competition. International Journal of Biological Macromolecules 165, 1664–1674.CrossRefGoogle ScholarPubMed
Chang, YW, Zhang, XX, Lu, MX, Gong, WR and Du, YZ (2020 b) Transcriptome analysis of Liriomyza trifolii (Diptera: Agromyzidae) in response to temperature stress. Comparative Biochemistry and Physiology – Part D: Genomics and Proteomics 34, 100677.Google ScholarPubMed
Charles, JP (2010) The regulation of expression of insect cuticle protein genes. Insect Biochemistry and Molecular Biology 40, 205–213.CrossRefGoogle ScholarPubMed
Chen, B and Kang, L (2002) Cold hardiness and supercooling capacity in the pea leafminer Liriomyza huidobrensis. Cryo Letters 23, 173–182.Google ScholarPubMed
Chen, LL, Lin, CJ, Lai, ZL, Shi, F, Weng, and Cai, JL (2018) Insecticidal efficacy of microwave on Empoasca onukii (Hemiptera, Cicadellidae). Fujian Journal of Agricultural Science 33, 1301–1306.Google Scholar
Cui, J, Zhu, SY, Gao, Y, Bi, R, Xu, Z and Shi, SS (2018) Comparative transcriptome analysis of Megacopta cribraria (Hemiptera: Plataspidae) in response to high-temperature stress. Journal of Economic Entomology 112, 407–415.CrossRefGoogle Scholar
Cui, HY, Zeng, YY, Reddy, GVP, Gao, F, Li, ZH and Zhao, ZH (2021) UV radiation increases mortality and decreases the antioxidant activity in a tephritid fly. Food and Energy Security 10, e297.CrossRefGoogle Scholar
Dubrovsky, EB (2005) Hormonal cross talk in insect development. Trends in Endocrinology and Metabolism 16, 6–11.CrossRefGoogle ScholarPubMed
Gao, YL, Reitz, SR, Wei, QB, Yu, WY and Lei, ZR (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS One 7, e36622.CrossRefGoogle ScholarPubMed
Gao, YL, Reitz, SR, Xing, ZL, Ferguson, S and Lei, ZR (2017) A decade of a leafminer invasion in China: lessons learned. Pest Management Science 73, 1775–1779.CrossRefGoogle ScholarPubMed
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, di Palma, F, Birren, BW, Nusbaum, C, Lindblad-Toh, K, Friedman, N and Regev, A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652.CrossRefGoogle ScholarPubMed
Hoz, ADL, Díaz-Ortiza, A and Morenoa, A (2005) Microwaves in organic synthesis. Thermal and non-thermal microwave effects. Chemical Society Reviews 34, 164–178.CrossRefGoogle ScholarPubMed
Joga, MR, Zotti, MJ, Smagghe, G and Christiaens, O (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Frontiers in Physiology 7, 553.CrossRefGoogle ScholarPubMed
Johnson, MW, Welter, SC, Toscano, NC, Tingi, P and Trumble, JT (1983) Reduction of tomato leaflet photosynthesis rates by mining activity of Liriomyza sativae (Diptera: Agromyzidae). Journal of Economic Entomology 76, 1061–1063.CrossRefGoogle Scholar
Kang, FF, Cheng, Y, Huang, QL, Wei, YD, Zhang, RF and Yang, F (2009) Advances in application of microwave technology to pest quarantine. Plant Protection 35, 36–39.Google Scholar
Knipling, EF (1959) The sterile male method of population control. Science 130, 902–904.CrossRefGoogle ScholarPubMed
Liu, F, Meng, JY, Yang, CL and Zhang, CY (2020) Cloning and expression profile of vitellogenin gene and its response to UV-A stress in Ostrinia furnacalis (Guenée). Acta Entomologica Sinica 63, 255–265.Google Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408.CrossRefGoogle ScholarPubMed
Lu, HH, Zhou, JC, Xiong, SB and Zhao, SM (2010) Effects of low-intensity microwave radiation on Tribolium castaneum physiological and biochemical characteristics and survival. Journal of Insect Physiology 56, 1356–1361.CrossRefGoogle ScholarPubMed
Pang, XF and Zhang, AY (2001) Study on the mechanism and characteristics of biological thermal effect of microwave. Chinese Journal of Atomic and Molecular Physics 18, 421–425.Google Scholar
Parrella, MP (1987) Biology of Liriomyza. Annual Review of Entomology 32, 201–224.CrossRefGoogle Scholar
Parrella, MP, Jones, VP, Youngman, RR and Lebeck, LM (1985) Effect of leaf mining and leaf stippling of Liriomyza spp. on photosynthetic rates of chrysanthemum. Annals of the Entomological Society of America 78, 90–93.CrossRefGoogle Scholar
Purohit, P, Jayas, DS, Yadav, BK, Chelladurai, V, Fields, PG and White, NDG (2013) Microwaves to control Callosobruchus maculatus in stored mung bean (Vigna radiata). Journal of Stored Products Research 53, 19–22.CrossRefGoogle Scholar
Reitz, SR, Kund, GS, Carson, WG, Phillips, PA and Trumble, JT (1999) Economics of reducing insecticide use on celery through low-input pest management strategies. Agriculture, Ecosystems and Environment 73, 185–197.CrossRefGoogle Scholar
Reitz, SR, Gao, YL and Lei, ZR (2013) Insecticide use and the ecology of invasive Liriomyza leafminer management. In Trdan, S (ed.), Insecticides – Development of Safer and More Effective Technologies. Rijeka: InTech, pp. 235–255.Google Scholar
Riddiford, LM, Cherbas, P and Truman, JW (2000) Ecdysone receptors and their biological actions. Vitamins and Hormones 60, 1–73.CrossRefGoogle ScholarPubMed
Robinson, AS (2005) Genetic basis of the sterile insect technique. In Dyck, VA, Hendrichs, J and Robinson, AS (eds), Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands: Springer, pp. 95–114.CrossRefGoogle Scholar
Roy, S, Saha, TT, Zou, Z and Raikhel, AS (2018) Regulatory pathways controlling insect reproduction. Annual Review of Entomology 63, 1.CrossRefGoogle ScholarPubMed
Sang, W, Ma, WH, Qiu, L, Zhu, ZH and Lei, CL (2012) The involvement of heat shock protein and cytochrome P450 genes in response to UV-A exposure in the beetle Tribolium castaneum. Journal of Insect Physiology 58, 830–836.CrossRefGoogle ScholarPubMed
Sang, W, Gao, Q, Zhang, CY, Huang, QY, Lei, CL and Wang, XP (2022) Research and application of physical control of agricultural insect pests in China. Journal of Plant Protection 49, 173–183.Google Scholar
Shallom, JM, Di Carlo, AL, Ko, D, Penafiel, LM, Nakai, A and Litovitz, TA (2002) Microwave exposure induces Hsp70 and confers protection against hypoxia in chick embryos. Journal of Cellular Biochemistry 86, 490–496.CrossRefGoogle ScholarPubMed
Shang, F, Ding, BY, Ye, C, Yang, L, Chang, TY, Xie, J, Tang, LD, Niu, JZ and Wang, JJ (2020) Evaluation of a cuticle protein gene as a potential RNAi target in aphids. Pest Management Science 76, 134–140.CrossRefGoogle ScholarPubMed
Spencer, KA (1973) Series Entomologica. In Göttingen, ES (ed.), Agromyzidae (Diptera) of Economic Importance, Edition 1, Vol. 9. Bath: The Hague Publishers, pp. 19–28.CrossRefGoogle Scholar
Su, L, Yang, CL, Meng, JY, Zhou, L and Zhang, CY (2021) Comparative transcriptome and metabolome analysis of Ostrinia furnacalis female adults under UV-A exposure. Scientific Reports 11, 6797.CrossRefGoogle ScholarPubMed
Tabara, H, Grishok, A and Mello, CC (1998) RNAi in C. elegans: soaking in the genome sequence. Science 282, 430–431.CrossRefGoogle Scholar
Tungjitwitayakul, J, Tatun, N, Vajarasathira, B and Sakurai, S (2016) Effects of ultraviolet-C and microwave irradiation on the expression of heat shock protein genes in the maize weevil (Coleoptera: Curculionidae). European Journal of Entomology 113, 135–142.CrossRefGoogle Scholar
Varet, H, Brilletguéguen, L, Coppée, JY and Dillies, MA (2016) SAR tools: a DESeq2- and EdgeR-based R pipeline for comprehensive differential analysis of RNA-Seq data. PLoS One 11, e0157022.CrossRefGoogle Scholar
Yang, CL, Meng, JY, Yao, MS and Zhang, CY (2021) Transcriptome analysis of Myzus persicae to UV-B stress. Journal of Insect Science 21, 1–9.CrossRefGoogle ScholarPubMed
Zhang, MZ, Jin, WL, Wang, JZ, Sun, SL, Qin, XC and Zhang, ZY (2007) Insecticidal efficacy of microwave treatment against Callosobruchus chinensis (L.) (Coleoptera: Bruchidae) and its effects on the germination rate of adzuki beans. Acta Entomologica Sinica 50, 967–974.Google Scholar
Zhang, H, Li, H, Guan, R and Miao, X (2015) Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying dsRNA on larvae. Entomologia Experimentalis et Applicata 155, 218–228.Google Scholar
Zhang, X, Yi, P, Chu, PF, Yuan, XQ, Zhan, EL, Leng, CM, Li, Y, Hu, D and Li, YP (2020) Effects of microwave irradiation on the growth, development and reproduction of the green peach aphid, Myzus persicae (Hemiptera: Aphididae). Acta Entomologica Sinica 63, 1215–1222.Google Scholar
Supplementary material: File

Chang et al. supplementary material

Figure S1

Download Chang et al. supplementary material(File)
File 69.4 KB