miR-701 modulates the humoral immune response of Coptotermes formosanus against Metarhizium anisopliae

Weiwen Chen , Zhiqiang Li

Insect Science ›› 2025, Vol. 32 ›› Issue (6) : 1822 -1837.

PDF
Insect Science ›› 2025, Vol. 32 ›› Issue (6) :1822 -1837. DOI: 10.1111/1744-7917.70095
ORIGINAL ARTICLE
miR-701 modulates the humoral immune response of Coptotermes formosanus against Metarhizium anisopliae
Author information +
History +
PDF

Abstract

Termites are not only social insects but also significant global insect pests. Investigating the molecular mechanisms regulating immune defense response in termites is beneficial for developing novel approaches to termite management. Currently, research mainly focuses on coding RNAs in termite immunity, with limited exploration of non-coding RNAs. Here, we identified miR-701, a markedly downregulated microRNA (miRNA) in the globally significant termite pest Coptotermes formosanus after Metarhizium anisopliae infection, which targets the immune gene Toll4. Transcriptome analysis of termites injected with miR-701 agomir revealed that miR-701 affects the immune-related response, growth, and development of termites. Treatment with miR-701 agomir, either through injection or ingestion, resulted in a notably reduced survival rate of termites infected with M. anisopliae compared to the control group infected with M. anisopliae alone. Additionally, termites injected with miR-701 agomir exhibited a significant decrease in the expression of antimicrobial peptide genes termicin and lysozyme, alongside a notable increase in the colony-forming units of M. anisopliae in the infected termites. Subsequent investigations demonstrated that miR-701 suppressed the expression of the target gene Toll4, consequently inhibiting the Toll signaling pathway and diminishing the expression of antimicrobial peptides. These findings suggest that termites can combat M. anisopliae by downregulating miR-701 expression to activate the Toll signaling pathway and enhance antimicrobial peptides synthesis. This discovery improves our comprehension of the role of miRNAs in termites’ immune responses and the mechanism of termites managing miRNAs to boost their pathogen resistance. Additionally, it reveals a new molecular target for termite biological control.

Keywords

fungus / humoral immune / lethal effect / miRNA / termite

Cite this article

Download citation ▾
Weiwen Chen, Zhiqiang Li. miR-701 modulates the humoral immune response of Coptotermes formosanus against Metarhizium anisopliae. Insect Science, 2025, 32(6): 1822-1837 DOI:10.1111/1744-7917.70095

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Aggarwal, K. and Silverman, N. (2008) Positive and negative regulation of the Drosophila immune response. BMB Reports, 41, 267–277.

[2]

Ahmad, F., Fouad, H., Liang, S.Y., Hu, Y. and Mo, J.C. (2021) Termites and Chinese agricultural system: applications and advances in integrated termite management and chemical control. Insect Science, 28, 2–20.

[3]

Ambros, V. (2004) The functions of animal microRNAs. Nature, 431, 350–355.

[4]

Asgari, S. (2013) MicroRNA functions in insects. Insect Biochemistry and Molecular Biology, 43, 388e397.

[5]

Chao, T.L., Yang, L.X., Lou, D.L., Fan, Y.H., He, Y., Shan, X.Q., et al. (2022) Fluvalinate-induced changes in microRNA expression profile of Apis mellifera ligustica brain tissue. Frontiers in Genetic, 13, 855987.

[6]

Chen, W.W., Zeng, W.H., Shen, D.N., Feng, S.Y. and Li, Z.Q. (2023a) Genome-wide identification of Coptotermes formosanus immune genes and their potential roles in termite control. Gene, 877, 147569.

[7]

Chen, W.W., Zhang, H., Chen, Y., Zeng, W.H. and Li, Z.Q. (2023b) Combined use of lipopolysaccharide-binding protein dsRNA and Gram-negative bacteria for pest management of Coptotermes formosanus. Pest Management Science, 79, 2299–2310.

[8]

Chen, W.W. and Li, Z.Q. (2025) miR-571 manipulating termite immune response to fungus and showing potential for green management of Copotermes formosanus (Blattodea: Isoptera). Pesticide Biochemistry and Physiology, 208, 106274.

[9]

Chouvenc, T., Su, N.Y. and Kenneth, G.J. (2011) Fifty years of attempted biological control of termites–analysis of a failure. Biological Control, 59, 69–82.

[10]

Chouvenc, T., Su, N.Y. and Robert, A. (2009) Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. Journal of Invertebrate Pathology, 10, 130–136.

[11]

Collins, D.H., Mohorianu, I., Beckers, M., Moulton, V., Dalmay, T. and Bourke, A.F.G. (2017) MicroRNAs associated with caste determination and differentiation in a primitively eusocial insect. Scientific Reports, 7, 45674.

[12]

Feng, K., Jiang, D.B., Luo, J. and Tang, F. (2023) OfGNBP silencing enhances the toxicity of Serratia marcescens Bizio (SM1) to Odontotermes formosanus (Shiraki). Pesticide Biochemistry and Physiology, 189, 105306.

[13]

Masson, F., Brown, R.L., Vizueta, J., Irvine, T., Xiong, Z.J., Romiguier, J., et al. (2024) Pathogen-specific social immunity is associated with erosion of individual immune function in an ant. Nature Communications, 15, 9260.

[14]

Glastad, K.M., Gokhale, K., Liebig, J. and Goodisman, M.A.D. (2016) The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Scientific Reports, 6, 37110.

[15]

Hamilton, C. and Bulmer, M.S. (2012) Molecular antifungal defenses in subterranean termites: RNA interference reveals in vivo roles of termicins and GNBPs against a naturally encountered pathogen. Developmental and Comparative Immunology, 36, 372–377.

[16]

Hussain, A., Tian, M.Y., He, Y.R., Bland, J.M. and Gu, W.X. (2010) Behavioral and electrophysiological responses of Coptotermes formosanus Shiraki towards entomopathogenic fungal volatiles. Biological Control, 55, 166–173.

[17]

Ke, Y.L., Zhang, S.J. and Li, Z.Q. (2022) Phylogenetic relationships of Chinese Coptotermes (Blattodea: Isoptera: Rhinotermitidae) termites and a new synonym inferred from morphological data. Journal of Entomological Science, 57, 64–81.

[18]

Lax, A.R. and Osbrink, W.L. (2003) United States Department of Agriculture: agriculture research service research on targeted management of the Formosan subterranean termite Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae). Pest Management Science, 59, 788–800.

[19]

Li, L., Liu, F., Li, W.F., Li, Z.G., Pan, J., Yan, L.M., et al. (2012) Differences in microRNAs and their expressions between foraging and dancing honey bees, Apis mellifera L. Journal of Insect Physiology, 58, 1438–1443.

[20]

Liu, L., Li, G.H., Sun, P.D., Lei, C.L. and Huang, Q.Y. (2015) Experimental verification and molecular basis of active immunization against fungal pathogens in termites. Scientific Reports, 5, 15106.

[21]

Liu, L., Wang, W., Liu, Y.L., Sun, P.D., Lei, C.L. and Huang, Q.Y. (2019) The influence of allogrooming behavior on individual innate immunity in the subterranean termite Reticulitermes chinensis (Isoptera: Rhinotermitidae). Journal of Insect Science, 19, 6.

[22]

Liu, L., Wang, C.C., Zhao, X.Y., Guan, J.X., Lei, C.L. and Huang, Q.Y. (2020) Isocitrate dehydrogenase-mediated metabolic disorders disrupt active immunization against fungal pathogens in eusocial termites. Journal of Pest Science, 93, 291–301.

[23]

Liu, L., Wang, D.H., Zhao, C.C., Yan, F.M., Lei, C.L., Su, L.J., et al. (2023a) Transcriptomics reveals the killing mechanism by which entomopathogenic fungi manipulate the RNA expression profiles of termites and provides inspiration for green pest management. Journal of Agricultural and Food Chemistry, 71, 7152–7162.

[24]

Liu, L., Yan, F.M., Zhao, C.C., Su, L.J., Huang, Q.Y. and Tang, Q.B. (2023b) microRNAs shape social immunity: a potential target for biological control of the termite Reticulitermes chinensis. Journal of Pest Science, 96, 265–279.

[25]

Lu, X.Y., Wang, M.Y., Jiang, D.B. and Tang, F. (2024) The function of OforOrco in the allogrooming behavior of Odontotermes formosanus (Shiraki) induced by Serratia marcescens Bizio (SM1). Pesticide Biochemistry and Physiology, 204, 106004.

[26]

Lucas, K.J., Zhao, B., Liu, S. and Raikhel, A.S. (2015) Regulation of physiological processes by microRNAs in insects. Current Opinion in Insect Science, 11, 1–7.

[27]

Rosengaus, R.B., Jordan, C., Lefebvre, M.L. and Traniello, J.F.A. (1999) Pathogen alarm behaviour in a termite: a new form of communication in social insects. Die Naturwissenschaften, 86, 544–548.

[28]

Rust, M.K. and Su, N.Y. (2012) Managing social insects of urban importance. Annual Review of Entomology, 57, 355–375.

[29]

Seistrup, A., Choppin, M., Govind, S., Feldmeyer, B., Kever, M., Karaulanov, E., et al. (2023) Age- and caste-independent piRNAs in the germline and miRNA profiles linked to caste and fecundity in the ant Temnothorax rugatulus. Molecular Ecology, 32, 6027–6043.

[30]

Shi, T.F., Jiang, X.C., Cao, H.Q. and Yu, L.S. (2023) Exposure to sublethal concentrations of thiacloprid insecticide modulated the expression of microRNAs in honeybees (Apis mellifera L.). Ecotoxicology and Environmental Safety, 264, 115499.

[31]

Sun, Q., Haynes, K.F. and Zhou, X.G. (2016) Dynamic changes in death cues modulate risks and rewards of corpse management in a social insect. Functional Ecology, 31, 697–706.

[32]

Wang, Z.Q., Zhou, Y.J.Y., Li, X.G. and Tang, F. (2024a) Importance of core microRNA pathway genes and microRNAs associated with the defense of Odontotermes formosanus (Shiraki) against Serratia marcescens infection. Pesticide Biochemistry and Physiology, 201, 105864.

[33]

Wang, Z.Q., Zhou, Y.J.Y. and Tang, F. (2024b) RNAi-mediated silencing of transferrin promotes entomopathogens lethality in Odontotermes formosanus (Shiraki). Pesticide Biochemistry and Physiology, 205, 106149.

[34]

Wu, Y., Guo, Y.L., Fan, X.X., Zhao, H.D., Zhang, Y.Q., Guo, S.J., et al. (2023) ame-miR-34 modulates the larval body weight and immune response of Apis mellifera workers to Ascosphara apis invasion. International Journal of Molecular Sciences, 24, 1214.

[35]

Wu, P., Shang, Q., Dweteh, O.A., Huang, H.L., Zhang, S.L., Zhong, J.B., et al. (2019) Over expression of bmo-miR-2819 suppresses BmNPV replication by regulating the BmNPV ie-1 gene in Bomby mori. Molecular Immunology, 109, 134–139.

[36]

Yanagawa, A., Imai, T., Akino, T., Toh, Y. and Yoshimura, T. (2015) Olfactory cues from pathogenic fungus affect the direction of motion of termites, Coptotermes formosanus. Journal of Chemical Ecology, 41, 1118–1126.

[37]

Yu, J., Song, H.Y., Wang, H.F., Wang, Y., Liu, Z.G. and Xu, B.H. (2023) The microRNA Ame-Bantam-3p controls larval pupal development by targeting the multiple epidermal growth factor-like domains 8 gene (megf8) in the honeybee, Apis mellifera. International Journal of Molecular Sciences, 24, 5726.

[38]

Yu, S. X., Hassan, A., Mehmood, N., Zhou, W., Raza T. and Huang, Q.Y. (2024) Study on the role of RPL23 gene in active immunity of termite Reticulitermes chinensis against Metarhizium anisopliae. Journal of Invertebrate Pathology, 207,108226.

[39]

Zeng, W.H., Shen, D.N., Wu, W.J., Zhang, S.J., Li, Z.Q. and Zhang, D.D. (2024) Involvement of a catalase gene in lignin catalysis and immune defense against pathogenic fungus in Coptotermes formosanus: a potential new target for termite control. Pest Management Science, 80, 3258–3268.

[40]

Zhang, H., Li, Z.Q., Jia, F.L. and Chen, W.W. (2024) Impact of miR-120 on the immune response of Coptotermes formosanus against Metarhizium anisopliae. Journal of Environmental Entomology, 46, 948–957.

[41]

Zhao, X.Y., Liu, L., Zhou, W., Cai, Q. and Huang, Q.Y. (2020) Roles of selenoprotein T and transglutaminase in active immunization against entomopathogenic fungi in the termite Reticulitermes chinensis. Journal of Insect Physiology, 125, 104085.

[42]

Zhou, W., Huang, Q.Y., Zhao, X.Y., Liu, L. and Mehmood, N. (2021) Silencing of selenium-binding protein disrupted the active immunization of the termite Reticulitermes chinensis and improved the lethal effect of the entomopathogenic fungus Metarhizium anisopliae. Biological Control, 157, 104588.

[43]

Zondag, L., Dearden, P.K. and Wilson, M.J. (2012) Deep sequencing and expression of microRNAs from early honeybee (Apis mellifera) embryos reveals a role in regulating early embryonic patterning. BMC Ecology and Evolution, 12, 211.

RIGHTS & PERMISSIONS

2025 The Author(s). Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

PDF

1

Accesses

0

Citation

Detail

Sections
Recommended

/