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Antimicrobial peptide cecropin B functions in pathogen resistance of Mythimna separata

Published online by Cambridge University Press:  11 April 2024

Yi-Xiao Wang
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Hong-Jia Yang
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Wei-Jia Zhang
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Xiao-Hui Zhao
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Meng-Yao Cui
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Jin-Bo Zhang
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Xin-xin Zhang*
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
Dong Fan*
Affiliation:
College of Plant Protection, Northeast Agricultural University, Harbin, China
*
Corresponding authors: Xin-xin Zhang; Email: xinxinz@neau.edu.cn, Dong Fan; Email: dnfd@163.com
Corresponding authors: Xin-xin Zhang; Email: xinxinz@neau.edu.cn, Dong Fan; Email: dnfd@163.com

Abstract

Mythimna separata (Lepidoptera: Noctuidae) is an omnivorous pest that poses a great threat to food security. Insect antimicrobial peptides (AMPs) are small peptides that are important effector molecules of innate immunity. Here, we investigated the role of the AMP cecropin B in the growth, development, and immunity of M. separata. The gene encoding M. separata cecropin B (MscecropinB) was cloned. The expression of MscecropinB was determined in different developmental stages and tissues of M. separata. It was highest in the prepupal stage, followed by the pupal stage. Among larval stages, the highest expression was observed in the fourth instar. Tissue expression analysis of fourth instar larvae showed that MscecropinB was highly expressed in the fat body and haemolymph. An increase in population density led to upregulation of MscecropinB expression. MscecropinB expression was also upregulated by the infection of third and fourth instar M. separata with Beauveria bassiana or Bacillus thuringiensis (Bt). RNA interference (RNAi) targeting MscecropinB inhibited the emergence rate and fecundity of M. separata, and resulted in an increased sensitivity to B. bassiana and Bt. The mortality of M. separata larvae was significantly higher in pathogen plus RNAi-treated M. separata than in controls treated with pathogens only. Our findings indicate that MscecropinB functions in the eclosion and fecundity of M. separata and plays an important role in resistance to infection by B. bassiana and Bt.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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References

Aronson, AI and Shai, Y (2001) Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action. FEMS Microbiology Letters 195, 18.CrossRefGoogle ScholarPubMed
Boman, HG (2003) Antibacterial peptides: basic facts and emerging concepts. Journal of Internal Medicine 254, 197215.CrossRefGoogle ScholarPubMed
Brogden, KA, De Lucca, AJ, Bland, J and Elliott, S (1996) Isolation of an ovine pulmonary surfactant-associated anionic peptide bactericidal for Pasteurella haemolytica. Proceedings of the National Academy of Sciences 93, 412416.CrossRefGoogle ScholarPubMed
Cao, Q and Ni, C (2014) Advances on the safety of biological control with Bacillus thuringiensis. Hubei Agricultural Sciences 53, 24852489.Google Scholar
Chen, L, Pan, Q, Waqas, MS and Liu, T (2020) Morphological traits for sex identification of the oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae). Journal of Integrative Agriculture 19, 14581463.CrossRefGoogle Scholar
Chu, X (2022) Gene identification, yeast expression and functional studies of antimicrobial peptides from Monochamus alternatus Hope. Fujian Agriculture and Forestry University. https://doi.org/10.27018/d.cnki.gfjnu.2022.000567Google Scholar
Cui, Z, Huang, N, He, P, Xu, W, Hu, J and Cui, S (2023) Application progress of Bacillus thuringiensis in the field of pest control. Modern Flour Industry 37, 1318.Google Scholar
De Lucca, AJ, Bland, JM, Jacks, TJ, Grimm, C and Walsh, TJ (1998) Fungicidal and binding properties of the natural peptides cecropin B and dermaseptin. Medical Mycology 36, 291298.CrossRefGoogle ScholarPubMed
Dong, S (2021) Cloning, expression and antifungal activity analysis of CPAlo 13768 antimicrobial peptide gene from Conogethes punctiferalis. Henan Agricultural University. https://doi.org/10.27117/d.cnki.ghenu.2021.000450Google Scholar
Dong, J, Liu, X, Yue, J, Qiao, Y, Chu, Y, Wang, P and Zhang, Q (2014) Resistance of armyworms to five insecticides in Beijing. Chinese Journal of Pesticide Science 16, 687692.Google Scholar
Duan, X, Jia, Z, Xu, Y, Long, T, Wang, Y, Li, W and Zhao, J (2023) Current status of enzyme production characteristics and application research of Beauveria bassiana. Hubei Plant Protection, 1318.Google Scholar
Feng, L, Tan, Z and Tan, B (2019) Physiological function and mechanism of antimicrobial peptides and its application in weaned piglet. Chinese Journal of Animal Science 58, 1319.Google Scholar
Ferreira, JM and de Freitas Soares, FE (2023) Entomopathogenic fungi hydrolytic enzymes: a new approach to biocontrol? Journal of Natural Pesticide Research 3, 100020. https://doi.org/10.1016/j.napere.2023.100020CrossRefGoogle Scholar
Hajek, AE and Leger, RJS (1994) Interactions between fungal pathogens and insect hosts. Annual Review of Entomology 39, 293322.CrossRefGoogle Scholar
Holdbrook, DA, Singh, S, Choong, YK, Petrlova, J, Malmsten, M, Bond, PJ, Verma, NK, Schmidtchen, A and Saravanan, R (2018) Influence of pH on the activity of thrombin-derived antimicrobial peptides. Biochimica et Biophysica Acta (BBA)-Biomembranes 1860, 23742384.CrossRefGoogle ScholarPubMed
Hu, H, Wang, C, Guo, X, Li, W, Wang, Y and He, Q (2013) Broad activity against porcine bacterial pathogens displayed by two insect antimicrobial peptides moricin and cecropin B. Molecules and Cells 35, 106114.CrossRefGoogle ScholarPubMed
Hwang, JS, Lee, J, Kim, YJ, Bang, H, Yun, E and Kim, S (2009) Isolation and characterization of a defensin-like peptide (coprisin) from the dung beetle, Copris tripartitus. International Journal of Peptides. https://doi.org/10.1155/2009/136284CrossRefGoogle ScholarPubMed
Jing, W (2021) Effects of bursicon on the antimicrobial peptide gene expression and disease resistance in crowded Mythimna separata larvae. Yangzhou University. https://doi.org/10.27441/d.cnki.gyzdu.2021.000998Google Scholar
Kang, Y, Meng, J, Wang, Y and Zhang, S (2021) Research progress on functional characteristics and mechanism of antimicrobial peptides. Food Science and Technology 46, 265270.Google Scholar
Li, C and Zhang, S (2005) A review of study on virulence of Beauveria bassiana against pests. Journal of Tangshan Normal University, 4043.Google Scholar
Li, X, Ma, Y, Li, X, Yu, H and Zhang, J (2012) Research progress in parasporal crystal from Bacillus thuringiensis. Journal of Anhui Agricultural Science 40, 59205924.Google Scholar
Li, Y, Yao, Q, Ren, M, Yang, F, Zou, M, Zhang, Y and Lin, Q (2019) Progress on action mechanisms of antimicrobial peptides. Advances in Veterinary Medicine 40, 98103.Google Scholar
Li, X, Liu, J and Bao, M (2020) Occurrence rule and comprehensive control technology of corn slime worms. Shanxi Agricultural Economics, 108+114. https://doi.org/10.16675/j.cnki.cn14-1065/f.2020.06.056Google Scholar
Li, Y, Sun, H, Yasoob, H, Tian, Z and Zhang, Y (2021) Biogenetic cantharidin is a promising leading compound to manage insecticide resistance of Mythimna separata (Lepidoptera: Noctuidae). Pesticide Biochemistry and Physiology 172, 104769.CrossRefGoogle ScholarPubMed
Liu, F, Sun, L, Tang, T and Wang, L (2011) Cloning, sequence analysis and induced expression of attacin-2 gene in housefly (Musca domestica). Journal of Insects 54, 2733. https://doi.org/10.16380/j.kcxb.2011.01.004Google Scholar
Liu, W, Liu, Y, Xin, Q, Liu, S and Feng, K (2022) Occurrence characteristics and monitoring forecast of armyworm migration in Tianjin area. Tianjin Agriculture and Forestry Science and Technology, 1517+35. https://doi.org/10.16013/j.cnki.1002-0659.2022.0080Google Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.CrossRefGoogle Scholar
Ma, H, Abbas, MN, Zhang, K, Hu, X, Xu, M, Lang, H, Kausar, S, Yang, L and Cui, H (2019a) 20-Hydroxyecdysone regulates the transcription of the lysozyme via broad-complex Z2 gene in silkworm, Bombyx mori. Developmental & Comparative Immunology 94, 6672.CrossRefGoogle ScholarPubMed
Ma, L, Sha, Y, Zhang, X and Wang, B (2019b) Occurrence characteristics and prevention and control measures of armyworm on maize in Hongsibu district. Ningxia Agriculture and Forestry Science and Technology 60, 3335.Google Scholar
Ma, S, Ma, T, Ren, M and Ma, Z (2021) Insecticidal action of the botanical insecticide wilforine on Mythimna separata (Walker) related with the changes of ryanodine receptor expression. Ecotoxicology and Environmental Safety 213, 112025.CrossRefGoogle ScholarPubMed
Roh, JY, Choi, JY, Li, MS, Jin, BR and Je, YH (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. Journal of Microbiology and Biotechnology 17, 547.Google ScholarPubMed
Schittek, B, Hipfel, R, Sauer, B, Bauer, J, Kalbacher, H, Stevanovic, S, Schirle, M, Schroeder, K, Blin, N and Meier, F (2001) Dermcidin: a novel human antibiotic peptide secreted by sweat glands. Nature Immunology 2, 11331137.CrossRefGoogle ScholarPubMed
Schnepf, E, Crickmore, N, Van Rie, J, Lereclus, D, Baum, J, Feitelson, J, Zeigler, DR and Dean, DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiology and Molecular Biology Reviews 62, 775806.CrossRefGoogle ScholarPubMed
Scholte, EJ, Knols, BG, Samson, RA and Takken, W (2004) Entomopathogenic fungi for mosquito control: a review. Journal of Insect Science 4, 19.CrossRefGoogle ScholarPubMed
Singh, S, Papareddy, P, Kalle, M, Schmidtchen, A and Malmsten, M (2014) Effects of linear amphiphilicity on membrane interactions of C-terminal thrombin peptides. RSC Advances 4, 3758237591.CrossRefGoogle Scholar
Song, J, Yang, Q and Zhao, M (2005) Recent advances in Bt toxic protein gene. Journal of Northeast Forestry University, 6667. https://doi.org/10.3969/j.issn.1000-5382.2005.01.025Google Scholar
Uvell, H and Engstrom, Y (2007) A multilayered defense against infection: combinatorial control of insect immune genes. Trends in Genetics 23, 342349.CrossRefGoogle ScholarPubMed
Wang, G (2020) The antimicrobial peptide database provides a platform for decoding the design principles of naturally occurring antimicrobial peptides. Protein Science 29, 818.CrossRefGoogle ScholarPubMed
Wang, Z (2023) Role and effect of antimicrobial peptides in pig breeding. Swine Science 40, 9496.Google Scholar
Wang, D, Zeng, M, Li, H, Wang, Q and Wu, G (2012) Effects of inoculation method on toxicity of Beauveria bassiana against 5th instar lavae of Homona coffearia. Journal of Fujian Agricultural Sciences 27, 10971101.Google Scholar
Wei, Q (2012) Discussion on biological features and control technology of armyworm. Journal of Guangxi Agricultural 27, 2628.Google Scholar
Wu, S (2017) Discussion on agricultural pest resistance and comprehensive management. Private Science and Technology, 196.Google Scholar
Xu, H (2021) Harm of myxworms and coarse shrinkage disease in summer maize seedling stage. New Agriculture, 1415.Google Scholar
Xue, F, Feng, S and Li, J (2023) Application and prospect of artificial intelligence in antimicrobial peptides screening. Journal of China Pharmaceutical University 54, 314322.Google Scholar
Yang, C, Mu, Y, Wang, J and Chen, X (2021) Research progress on biological control of Mythimna separata (Walker). Anhui Agricultural Sciences 49, 1015.Google Scholar
Yu, H, Ren, Z, Wang, Z and Pei, H (2023) Study on the pathogenicity of Bacillus thuringiensis to Chilo suppressalis (Walker) and its synergistic effect with adjuvants. Journal of Northeast Agricultural University 54, 1220+44.Google Scholar
Yuan, L (2022) The mechanism of CREB regulating the resistance and immunity of Mythimna separata larvae at different densities. Yangzhou University. https://doi.org/10.27441/d.cnki.gyzdu.2022.002631Google Scholar
Zasloff, M (2002) Antimicrobial peptides of multicellular organisms. Nature 415, 389395.CrossRefGoogle ScholarPubMed
Zhang, L and Hua, S (2023) Application of antimicrobial peptides as new antibiotic substitutes in livestock and poultry breeding. Journal of Animal Husbandry and Veterinary Medicine 42, 120122.Google Scholar
Zhang, K, Yu, Z, Jiang, S, Sun, D, Hui, J, Zheng, Y, Li, X, Wang, X and Wu, J (2018) Association of host plant growth and weed occurrence with armyworm (Mythimna separata) damage in corn fields. Journal of Integrative Agriculture 17, 15381544.CrossRefGoogle Scholar
Zhao, Y, Su, L, Li, S, Li, Y, Xu, X, Cheng, W, Wang, Y and Wu, J (2018) Insecticide resistance of the field populations of oriental armyworm, Mythimna separata (Walker) in Shaanxi and Shanxi provinces of China. Journal of Integrative Agriculture 17, 15561562.CrossRefGoogle Scholar
Zhao, Z, Zhang, A, Pan, C and Jiang, N (2019) Insect antimicrobial peptides and their bioactive mechanism. Chinese Journal of Animal Nutrition 33, 66416647.Google Scholar
Zhuang, B, Zhao, W, Pei, H, Sun, L, Wang, Y, Chen, J and Yu, H (2019) Isolation, culture and pathogenicity of Beauveria bassiana strains against four important pests. Chinese Journal of Applied Entomology 57, 14171426.Google Scholar
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