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Annual Review of Entomology

Volume 70, 2025

Epigenetic Regulation in Insect–Microbe Interactions

  • Yiling Lai1,2 and Sibao Wang1,2
  • 1New Cornerstone Science Laboratory, CAS Key Laboratory of Insect Developmental and Evolutionary Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences (CAS), Shanghai, China; email: [email protected] 2CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China
  • Vol. 70:293-311 (Volume publication date January 2025)
  • First published as a Review in Advance on October 07, 2024
  • Copyright © 2025 by the author(s).
    This work is licensed under a Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See credit lines of images or other third-party material in this article for license information.

Abstract

Insects have evolved diverse interactions with a variety of microbes, such as pathogenic fungi, bacteria, and viruses. The immune responses of insect hosts, along with the dynamic infection process of microbes in response to the changing host environment and defenses, require rapid and fine-tuned regulation of gene expression programs. Epigenetic mechanisms, including DNA methylation, histone modifications, and noncoding RNA regulation, play important roles in regulating the expression of genes involved in insect immunity and microbial pathogenicity. This review highlights recent discoveries and insights into epigenetic regulatory mechanisms that modulate insect–microbe interactions. A deeper understanding of these regulatory mechanisms underlying insect–microbe interactions holds promise for the development of novel strategies for biological control of insect pests and mitigation of vector-borne diseases.

Keyword(s): DNA methylation, histone modifications, insect immunity, insect–microbe interactions, microbial pathogenicity, small RNAs
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Literature Cited

  1. 1.
    Abbas MN, Kausar S, Asma B, Ran WH, Li JG, et al. 2023.. MicroRNAs reshape the immunity of insects in response to bacterial infection. . Front. Immunol. 14::1176966
     [Crossref] [Google Scholar]
  2. 2.
    Amarante AD, da Silva ICD, Carneiro VC, Vicentino ARR, Pinto MD, et al. 2022.. Zika virus infection drives epigenetic modulation of immunity by the histone acetyltransferase CBP of Aedes aegypti. . PLOS Negl. Trop. Dis. 16::e0010559
     [Crossref] [Google Scholar]
  3. 3.
    Arsala D, Wu X, Yi SV, Lynch JA. 2022.. Dnmt1a is essential for gene body methylation and the regulation of the zygotic genome in a wasp. . PLOS Genet. 18::e1010181
     [Crossref] [Google Scholar]
  4. 4.
    Asgari S. 2011.. Role of microRNAs in insect host–microorganism interactions. . Front. Physiol. 2::48
     [Crossref] [Google Scholar]
  5. 5.
    Asgari S. 2023.. Cross-kingdom RNAi to enhance the efficacy of insect pathogens. . Trends Parasitol. 39::4–6
     [Crossref] [Google Scholar]
  6. 6.
    Baradaran E, Moharramipour S, Asgari S, Mehrabadi M. 2019.. Induction of DNA methyltransferase genes in Helicoverpa armigera following injection of pathogenic bacteria modulates expression of antimicrobial peptides and affects bacterial proliferation. . J. Insect Physiol. 118::103939
     [Crossref] [Google Scholar]
  7. 7.
    Berenguer J, Lagerweij T, Zhao XW, Dusoswa S, van der Stoop P, et al. 2018.. Glycosylated extracellular vesicles released by glioblastoma cells are decorated by CCL18 allowing for cellular uptake via chemokine receptor CCR8. . J. Extracell. Vesicles 7::1446660
     [Crossref] [Google Scholar]
  8. 8.
    Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ. 2017.. Evolution of DNA methylation across insects. . Mol. Biol. Evol. 34::654–65
     [Google Scholar]
  9. 9.
    Bonning BC, Saleh MC. 2021.. The interplay between viruses and RNAi pathways in insects. . Annu. Rev. Entomol. 66::61–79
     [Crossref] [Google Scholar]
  10. 10.
    Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, et al. 2014.. Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. . Nat. Commun. 5::5488
     [Crossref] [Google Scholar]
  11. 11.
    Burggren WW. 2017.. Epigenetics in insects: mechanisms, phenotypes and ecological and evolutionary implications. . Adv. Insect Physiol. 53::1–30
     [Crossref] [Google Scholar]
  12. 12.
    Cai J, Wu GZ, Jose PA, Zeng CY. 2016.. Functional transferred DNA within extracellular vesicles. . Exp. Cell Res. 349::179–83
     [Crossref] [Google Scholar]
  13. 13.
    Cai Q, Qiao LL, Wang M, He BY, Lin FM, et al. 2018.. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. . Science 360::1126–29
     [Crossref] [Google Scholar]
  14. 14.
    Colombo M, Raposo G, Théry C. 2014.. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. . Annu. Rev. Cell Dev. Biol. 30::255–89
     [Crossref] [Google Scholar]
  15. 15.
    Cristino AS, Barchuk AR, Freitas FCP, Narayanan RK, Biergans SD, et al. 2014.. Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee. . Nat. Commun. 5::5529
     [Crossref] [Google Scholar]
  16. 16.
    Cui CL, Wang Y, Li YF, Sun PL, Jiang JY, et al. 2022.. Expression of mosquito miRNAs in entomopathogenic fungus induces pathogen-mediated host RNA interference and increases fungal efficacy. . Cell Rep. 41::111527
     [Crossref] [Google Scholar]
  17. 17.
    Cui CL, Wang Y, Liu JN, Zhao J, Sun PL, Wang SB. 2019.. A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection. . Nat. Commun. 10::4298
     [Crossref] [Google Scholar]
  18. 18.
    du Preez PH, Breeds K, Burger NFV, Swiegers HW, Truter JC, Botha A-M. 2020.. DNA methylation and demethylation are regulated by functional DNA methyltransferases and DnTET enzymes in Diuraphis noxia. . Front. Genet. 11::452
     [Crossref] [Google Scholar]
  19. 19.
    Dubey SK, Shrinet J, Sunil S. 2019.. Aedes aegypti microRNA, miR-2944b-5p interacts with 3′UTR of chikungunya virus and cellular target vps-13 to regulate viral replication. . PLOS Negl. Trop. Dis. 13::e0007429
     [Crossref] [Google Scholar]
  20. 20.
    Etebari K, Asgari S. 2013.. Conserved microRNA miR-8 blocks activation of the Toll pathway by upregulating Serpin 27 transcripts. . RNA Biol. 10::1356–64
     [Crossref] [Google Scholar]
  21. 21.
    Field LM. 2000.. Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). . Biochem. J. 349::863–68
     [Crossref] [Google Scholar]
  22. 22.
    Galbraith DA, Yang XY, Niño EL, Yi S, Grozinger C. 2015.. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). . PLOS Pathog. 11::e1004713
     [Crossref] [Google Scholar]
  23. 23.
    Gao H, Cui CL, Wang LL, Jacobs-Lorena M, Wang SB. 2020.. Mosquito microbiota and implications for disease control. . Trends Parasitol. 36::98–111
     [Crossref] [Google Scholar]
  24. 24.
    Garbuzov A, Tatar M. 2010.. Hormonal regulation of Drosophila microRNA let-7 and miR-125 that target innate immunity. . Fly 4::306–11
     [Crossref] [Google Scholar]
  25. 25.
    Ginibre N, Legrand L, Bientz V, Ogier JC, Lanois A, et al. 2022.. Diverse roles for a conserved DNA-methyltransferase in the entomopathogenic bacterium Xenorhabdus. . Int. J. Mol. Sci. 23::11981
     [Crossref] [Google Scholar]
  26. 26.
    Glastad KM, Hunt BG, Goodisman MAD. 2014.. Evolutionary insights into DNA methylation in insects. . Curr. Opin. Insect Sci. 1::25–30
     [Crossref] [Google Scholar]
  27. 27.
    Glastad KM, Hunt BG, Yi SV, Goodisman MAD. 2011.. DNA methylation in insects: on the brink of the epigenomic era. . Insect Mol. Biol. 20::553–65
     [Crossref] [Google Scholar]
  28. 28.
    Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, et al. 2006.. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. . Science 311::395–98
     [Crossref] [Google Scholar]
  29. 29.
    Gomes FM, Silva M, Molina-Cruz A, Barillas-Mury C. 2022.. Molecular mechanisms of insect immune memory and pathogen transmission. . PLOS Pathog. 18::e1010939
     [Crossref] [Google Scholar]
  30. 30.
    Gomes FM, Tyner MDW, Barletta ABF, Saha B, Yenkoidiok-Douti L, et al. 2021.. Double peroxidase and histone acetyltransferase AgTip60 maintain innate immune memory in primed mosquitoes. . PNAS 118::e2114242118
     [Crossref] [Google Scholar]
  31. 31.
    Gómez-Díaz E, Jordà M, Peinado MA, Rivero A. 2012.. Epigenetics of host-pathogen interactions: the road ahead and the road behind. . PLOS Pathog. 8::e1003007
     [Crossref] [Google Scholar]
  32. 32.
    Gómez-Díaz E, Rivero A, Chandre F, Corces VG. 2014.. Insights into the epigenomic landscape of the human malaria vector Anopheles gambiae. . Front. Genet. 5::277
     [Google Scholar]
  33. 33.
    Harris CJ, Scheibe M, Wongpalee SP, Liu WL, Cornett EM, et al. 2018.. A DNA methylation reader complex that enhances gene transcription. . Science 362::1182–86
     [Crossref] [Google Scholar]
  34. 34.
    He C, Zhang ZQ, Li BQ, Tian SP. 2020.. The pattern and function of DNA methylation in fungal plant pathogens. . Microorganisms 8::227
     [Crossref] [Google Scholar]
  35. 35.
    He J, Chen QQ, Wei YY, Jiang F, Yang ML, et al. 2016.. MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts. . PNAS 113::584–89
     [Crossref] [Google Scholar]
  36. 36.
    Heitmueller M, Billion A, Dobrindt U, Vilcinskas A, Mukherjee K. 2017.. Epigenetic mechanisms regulate innate immunity against uropathogenic and commensal-like Escherichia coli in the surrogate insect model Galleria mellonella. . Infect. Immun. 85::e00336-17
     [Crossref] [Google Scholar]
  37. 37.
    Hu Y-T, Wu T-C, Yang E-C, Wu P-C, Lin P-T, Wu Y-L. 2017.. Regulation of genes related to immune signaling and detoxification in Apis mellifera by an inhibitor of histone deacetylation. . Sci. Rep. 7::41255
     [Crossref] [Google Scholar]
  38. 38.
    Huang HL, Wu P, Zhang SL, Shang Q, Yin HT, et al. 2019.. DNA methylomes and transcriptomes analysis reveal implication of host DNA methylation machinery in BmNPV proliferation in Bombyx mori. . BMC Genom. 20::736
     [Crossref] [Google Scholar]
  39. 39.
    Hussain M, Asgari S. 2010.. Functional analysis of a cellular microRNA in insect host-ascovirus interaction. . J. Virol. 84::612–20
     [Crossref] [Google Scholar]
  40. 40.
    Hussain M, Asgari S. 2014.. MicroRNA-like viral small RNA from dengue virus 2 autoregulates its replication in mosquito cells. . PNAS 111::2746–51
     [Crossref] [Google Scholar]
  41. 41.
    Hussain M, Asgari S. 2014.. MicroRNAs as mediators of insect host-pathogen interactions and immunity. . J. Insect Physiol. 70::151–58
     [Crossref] [Google Scholar]
  42. 42.
    Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S. 2011.. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. . PNAS 108::9250–55
     [Crossref] [Google Scholar]
  43. 43.
    Hussain M, O'Neill SL, Asgari S. 2013.. Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs. . RNA Biol. 10::1868–75
     [Crossref] [Google Scholar]
  44. 44.
    Hussain M, Torres S, Schnettler E, Funk A, Grundhoff A, et al. 2012.. West Nile virus encodes a microRNA-like small RNA in the 3′ untranslated region which up-regulates GATA4 mRNA and facilitates virus replication in mosquito cells. . Nucleic Acids Res. 40::2210–23
     [Crossref] [Google Scholar]
  45. 45.
    Hussain M, Walker T, O'Neill SL, Asgari S. 2013.. Blood meal induced microRNA regulates development and immune associated genes in the dengue mosquito vector, Aedes aegypti. . Insect Biochem. Mol. Biol. 43::146–52
     [Crossref] [Google Scholar]
  46. 46.
    Ivasyk I, Olivos-Cisneros L, Valdés-Rodríguez S, Droual M, Jang H, et al. 2023.. DNMT1 mutant ants develop normally but have disrupted oogenesis. . Nat. Commun. 14::2201
     [Crossref] [Google Scholar]
  47. 47.
    Jia QJ, Fu YJ. 2022.. microRNA-34-5p encoded by Spodoptera frugiperda regulates the replication and infection of Autographa californica multiple nucleopolyhedrovirus by targeting odv-e66, ac78 and ie2. . Pest Manag. Sci. 78::5379–89
     [Crossref] [Google Scholar]
  48. 48.
    Kang LQ, Wang ML, Cao XL, Tang SM, Xia DG, et al. 2018.. Inhibition of expression of BmNPV cg30 by bmo-miRNA-390 is a host response to baculovirus invasion. . Arch. Virol. 163::2719–25
     [Crossref] [Google Scholar]
  49. 49.
    Kausar S, Abbas MN, Gul I, Liu RC, Li QQ, et al. 2022.. Molecular identification of two DNA methyltransferase genes and their functional characterization in the anti-bacterial immunity of Antheraea pernyi. . Front. Immunol. 13::855888
     [Crossref] [Google Scholar]
  50. 50.
    Kim LK, Choi UY, Cho HS, Lee JS, Lee WB, et al. 2007.. Down-regulation of NF-κB target genes by the AP-1 and STAT complex during the innate immune response in Drosophila. . PLOS Biol. 5::2064–76
     [Crossref] [Google Scholar]
  51. 51.
    Kim T, Yoon J, Cho HS, Lee WB, Kim J, et al. 2005.. Downregulation of lipopolysaccharide response in Drosophila by negative crosstalk between the AP1 and NF-κB signaling modules. . Nat. Immunol. 6::211–18
     [Crossref] [Google Scholar]
  52. 52.
    Lai YL, Cao X, Chen JJ, Wang LL, Wei G, Wang SB. 2020.. Coordinated regulation of infection-related morphogenesis by the KMT2-Cre1-Hyd4 regulatory pathway to facilitate fungal infection. . Sci. Adv. 6::eaaz1659
     [Crossref] [Google Scholar]
  53. 53.
    Lai YL, Wang LL, Zheng WL, Wang SB. 2022.. Regulatory roles of histone modifications in filamentous fungal pathogens. . J. Fungi 8::565
     [Crossref] [Google Scholar]
  54. 54.
    Law JA, Jacobsen SE. 2010.. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. . Nat. Rev. Genet. 11::204–20
     [Crossref] [Google Scholar]
  55. 55.
    Lee GJ, Hyun S. 2014.. Multiple targets of the microRNA miR-8 contribute to immune homeostasis in Drosophila. . Dev. Comp. Immunol. 45::245–51
     [Crossref] [Google Scholar]
  56. 56.
    Lewis SH, Ross L, Bain SA, Pahita E, Smith SA, et al. 2020.. Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods. . PLOS Genet. 16::e1008864
     [Crossref] [Google Scholar]
  57. 57.
    Li RM, Huang Y, Zhang Q, Zhou HJ, Jin P, Ma F. 2019.. The miR-317 functions as a negative regulator of Toll immune response and influences Drosophila survival. . Dev. Comp. Immunol. 95::19–27
     [Crossref] [Google Scholar]
  58. 58.
    Li RM, Yao XL, Zhou HJ, Jin P, Ma F. 2021.. The Drosophila miR-959–962 cluster members repress Toll signaling to regulate antibacterial defense during bacterial infection. . Int. J. Mol. Sci. 22::886
     [Crossref] [Google Scholar]
  59. 59.
    Li RM, Zhou HJ, Jia CL, Jin P, Ma F. 2020.. Drosophila Myc restores immune homeostasis of Imd pathway via activating miR-277 to inhibit imd/Tab2. . PLOS Genet. 16::e1008989
     [Crossref] [Google Scholar]
  60. 60.
    Li SJ, Li Y, Shen L, Jin P, Chen LM, Ma F. 2017.. miR-958 inhibits Toll signaling and Drosomycin expression via direct targeting of Toll and Dif in Drosophila melanogaster. . Am. J. Physiol. Cell Physiol. 312::C103–10
     [Crossref] [Google Scholar]
  61. 61.
    Li SJ, Shen L, Sun LJ, Xu J, Jin P, et al. 2017.. Small RNA-Seq analysis reveals microRNA-regulation of the Imd pathway during Escherichia coli infection in Drosophila. . Dev. Comp. Immunol. 70::80–87
     [Crossref] [Google Scholar]
  62. 62.
    Li SJ, Xu J, Sun LJ, Li RM, Jin P, Ma F. 2017.. Drosophila miR-964 modulates Toll signaling pathway in response to bacterial infection. . Dev. Comp. Immunol. 77::252–58
     [Crossref] [Google Scholar]
  63. 63.
    Li SZ, Xu XX, Zheng ZH, Zheng JL, Shakeel M, Jin FL. 2019.. MicroRNA expression profiling of Plutella xylostella after challenge with B. thuringiensis. . Dev. Comp. Immunol. 93::115–24
     [Crossref] [Google Scholar]
  64. 64.
    Li WZ, Wang YL, Zhu JY, Wang ZX, Tang GL, Huang B. 2017.. Differential DNA methylation may contribute to temporal and spatial regulation of gene expression and the development of mycelia and conidia in entomopathogenic fungus Metarhizium robertsii. . Fungal Biol. 121::293–303
     [Crossref] [Google Scholar]
  65. 65.
    Li Y, Li SJ, Li RM, Xu J, Jin P, et al. 2017.. Genome-wide miRNA screening reveals miR-310 family members negatively regulate the immune response in Drosophila melanogaster via co-targeting Drosomycin. . Dev. Comp. Immunol. 68::34–45
     [Crossref] [Google Scholar]
  66. 66.
    Li-Byarlay H, Li Y, Stroud H, Feng SH, Newman TC, et al. 2013.. RNA interference knockdown of DNA methyltransferase 3 affects gene alternative splicing in the honey bee. . PNAS 110::12750–55
     [Crossref] [Google Scholar]
  67. 67.
    Lin S, Wang YS, Zhao Z, Wu WM, Su Y, et al. 2021.. Two putative cypovirus-encoded miRNAs co-regulate the host gene of GTP-binding nuclear protein Ran and facilitate virus replication. . Front. Physiol. 12::663482
     [Crossref] [Google Scholar]
  68. 68.
    Ling L, Kokoza VA, Zhang CY, Aksoy E, Raikhel AS. 2017.. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. . PNAS 114::E8017–24
     [Crossref] [Google Scholar]
  69. 69.
    Liu ZL, Ling L, Xu J, Zeng BS, Huang YP, et al. 2018.. MicroRNA-14 regulates larval development time in Bombyx mori. . Insect Biochem. Mol. Biol. 93::57–65
     [Crossref] [Google Scholar]
  70. 70.
    Lovett B, Bilgo E, Millogo SA, Ouattarra AK, Sare I, et al. 2019.. Transgenic Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso. . Science 364::894–97
     [Crossref] [Google Scholar]
  71. 71.
    Lyko F. 2018.. The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. . Nat. Rev. Genet. 19::81–92
     [Crossref] [Google Scholar]
  72. 72.
    Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 2010.. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. . PLOS Biol. 8::e1000506
     [Crossref] [Google Scholar]
  73. 73.
    Ma F, Liu XG, Li D, Wang P, Li N, et al. 2010.. MicroRNA-466l upregulates IL-10 expression in TLR-triggered macrophages by antagonizing RNA-binding protein tristetraprolin-mediated IL-10 mRNA degradation. . J. Immunol. 184::6053–59
     [Crossref] [Google Scholar]
  74. 74.
    Ma L, Liu L, Zhao YJ, Yang L, Chen CH, et al. 2020.. JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184. . PLOS Pathog. 16::e1008627
     [Crossref] [Google Scholar]
  75. 75.
    Merkling SH, Bronkhorst AW, Kramer JM, Overheul GJ, Schenck A, Van Rij RP. 2015.. The epigenetic regulator G9a mediates tolerance to RNA virus infection in Drosophila. . PLOS Pathog. 11::e1004692
     [Crossref] [Google Scholar]
  76. 76.
    Morris O, Liu X, Domingues C, Runchel C, Chai A, et al. 2016.. Signal integration by the IκB protein pickle shapes Drosophila innate host defense. . Cell Host Microbe 20::283–95
     [Crossref] [Google Scholar]
  77. 77.
    Mukherjee K, Dobrindt U. 2022.. The emerging role of epigenetic mechanisms in insect defense against pathogens. . Curr. Opin. Insect Sci. 49::8–14
     [Crossref] [Google Scholar]
  78. 78.
    Mukherjee K, Dubovskiy I, Grizanova E, Lehmann R, Vilcinskas A. 2019.. Epigenetic mechanisms mediate the experimental evolution of resistance against parasitic fungi in the greater wax moth Galleria mellonella. . Sci. Rep. 9::1626
     [Crossref] [Google Scholar]
  79. 79.
    Mukherjee K, Fischer R, Vilcinskas A. 2012.. Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. . Front. Zool. 9::25
     [Crossref] [Google Scholar]
  80. 80.
    Mukherjee K, Grizanova E, Chertkova E, Lehmann R, Dubovskiy I, Vilcinskas A. 2017.. Experimental evolution of resistance against Bacillus thuringiensis in the insect model host Galleria mellonella results in epigenetic modifications. . Virulence 8::1618–30
     [Crossref] [Google Scholar]
  81. 81.
    Nai YS, Huang YC, Yen MR, Chen PY. 2021.. Diversity of fungal DNA methyltransferases and their association with DNA methylation patterns. . Front. Microbiol. 11::616922
     [Crossref] [Google Scholar]
  82. 82.
    Neri F, Rapelli S, Krepelova A, Incarnato D, Parlato C, et al. 2017.. Intragenic DNA methylation prevents spurious transcription initiation. . Nature 543::72–77
     [Crossref] [Google Scholar]
  83. 83.
    Payelleville A, Lanois A, Gislard M, Dubois E, Roche D, et al. 2017.. DNA adenine methyltransferase (Dam) overexpression impairs Photorhabdus luminescens motility and virulence. . Front. Microbiol. 8::1671
     [Crossref] [Google Scholar]
  84. 84.
    Payelleville A, Legrand L, Ogier JC, Roques C, Roulet A, et al. 2018.. The complete methylome of an entomopathogenic bacterium reveals the existence of loci with unmethylated adenines. . Sci. Rep. 8::12091
     [Crossref] [Google Scholar]
  85. 85.
    Provataris P, Meusemann K, Niehuis O, Grath S, Misof B. 2018.. Signatures of DNA methylation across insects suggest reduced DNA methylation levels in Holometabola. . Genome Biol. Evol. 10::1185–97
     [Crossref] [Google Scholar]
  86. 86.
    Qu S, Wang SB. 2018.. Interaction of entomopathogenic fungi with the host immune system. . Dev. Comp. Immunol. 83::96–103
     [Crossref] [Google Scholar]
  87. 87.
    Ren K, Mou Y-N, Tong S-M, Ying S-H, Feng M-G. 2021.. DIM5/KMT1 controls fungal insect pathogenicity and genome stability by methylation of histone H3K4, H3K9 and H3K36. . Virulence 12::1306–22
     [Crossref] [Google Scholar]
  88. 88.
    Ren K, Mou Y-N, Tong S–M, Ying S-H, Feng M-G. 2021.. SET1/KMT2-governed histone H3K4 methylation coordinates the lifecycle in vivo and in vitro of the fungal insect pathogen Beauveria bassiana. . Environ. Microbiol. 23::5541–54
     [Crossref] [Google Scholar]
  89. 89.
    Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C. 2010.. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. . Science 329::1353–55
     [Crossref] [Google Scholar]
  90. 90.
    Rountree MR, Selker EU. 2010.. DNA methylation and the formation of heterochromatin in Neurospora crassa. . Heredity 105::38–44
     [Crossref] [Google Scholar]
  91. 91.
    Ruiz JL, Yerbanga RS, Lefèvre T, Ouedraogo JB, Corces VG, Gómez-Díaz E. 2019.. Chromatin changes in Anopheles gambiae induced by Plasmodium falciparum infection. . Epigenet. Chromatin 12::5
     [Crossref] [Google Scholar]
  92. 92.
    Sarda S, Zeng J, Hunt BG, Yi SV. 2012.. The evolution of invertebrate gene body methylation. . Mol. Biol. Evol. 29::1907–16
     [Crossref] [Google Scholar]
  93. 93.
    Sbaraini N, Bellini R, Penteriche AB, Guedes RLM, Garcia AWA, et al. 2019.. Genome-wide DNA methylation analysis of Metarhizium anisopliae during tick mimicked infection condition. . BMC Genom. 20::836
     [Crossref] [Google Scholar]
  94. 94.
    Schuster S, Miesen P, van Rij RP. 2019.. Antiviral RNAi in insects and mammals: parallels and differences. . Viruses 11::448
     [Crossref] [Google Scholar]
  95. 95.
    Singh CP, Singh J, Nagaraju J. 2012.. A baculovirus-encoded microRNA (miRNA) suppresses its host miRNA biogenesis by regulating the exportin-5 cofactor Ran. . J. Virol. 86::7867–79
     [Crossref] [Google Scholar]
  96. 96.
    Singh CP, Singh J, Nagaraju J. 2014.. bmnpv-miR-3 facilitates BmNPV infection by modulating the expression of viral P6.9 and other late genes in Bombyx mori. . Insect Biochem. Mol. Biol. 49::59–69
     [Crossref] [Google Scholar]
  97. 97.
    Sun X, Liu BQ, Li CQ, Chen ZB, Xu XR, Luan JB. 2022.. A novel microRNA regulates cooperation between symbiont and a laterally acquired gene in the regulation of pantothenate biosynthesis within Bemisia tabaci whiteflies. . Mol. Ecol. 31::2611–24
     [Crossref] [Google Scholar]
  98. 98.
    Vasudevan S, Tong YC, Steitz JA. 2007.. Switching from repression to activation: MicroRNAs can up-regulate translation. . Science 318::1931–34
     [Crossref] [Google Scholar]
  99. 99.
    Ventós-Alfonso A, Ylla G, Montañes J-C, Belles X. 2020.. DNMT1 promotes genome methylation and early embryo development in cockroaches. . iScience 23::101778
     [Crossref] [Google Scholar]
  100. 100.
    Vickers KC, Remaley AT. 2012.. Lipid-based carriers of microRNAs and intercellular communication. . Curr. Opin. Lipidol. 23::91–97
     [Crossref] [Google Scholar]
  101. 101.
    Vilcinskas A. 2016.. The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. . Zoology 119::273–80
     [Crossref] [Google Scholar]
  102. 102.
    Vogel E, Santos D, Mingels L, Verdonckt TW, Vanden Broeck J. 2019.. RNA interference in insects: protecting beneficials and controlling pests. . Front. Physiol. 9::1912
     [Crossref] [Google Scholar]
  103. 103.
    Wang C, Wang S. 2017.. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. . Annu. Rev. Entomol. 62::73–90
     [Crossref] [Google Scholar]
  104. 104.
    Wang LL, Lai YL, Chen JJ, Cao X, Zheng WL, et al. 2023.. The ASH1-PEX16 regulatory pathway controls peroxisome biogenesis for appressorium-mediated insect infection by a fungal pathogen. . PNAS 120::e2217145120
     [Crossref] [Google Scholar]
  105. 105.
    Wang M, Weiberg A, Jin HL. 2015.. Pathogen small RNAs: a new class of effectors for pathogen attacks. . Mol. Plant Pathol. 16::219–23
     [Crossref] [Google Scholar]
  106. 106.
    Wang M, Weiberg A, Lin FM, Thomma BPHJ, Huang HD, Jin HL. 2016.. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. . Nat. Plants 2::16151
     [Crossref] [Google Scholar]
  107. 107.
    Wang Y, Cui CL, Wang GD, Li YF, Wang SB. 2021.. Insects defend against fungal infection by employing microRNAs to silence virulence-related genes. . PNAS 118::e2023802118
     [Crossref] [Google Scholar]
  108. 108.
    Wang YL, Wang TT, Qiao LT, Zhu JY, Fan JR, et al. 2017.. DNA methyltransferases contribute to the fungal development, stress tolerance and virulence of the entomopathogenic fungus Metarhizium robertsii. . Appl. Microbiol. Biotechnol. 101::4215–26
     [Crossref] [Google Scholar]
  109. 109.
    Wang YL, Wang ZX, Liu C, Wang SB, Huang B. 2015.. Genome-wide analysis of DNA methylation in the sexual stage of the insect pathogenic fungus Cordyceps militaris. . Fungal Biol. 119::1246–54
     [Crossref] [Google Scholar]
  110. 110.
    Wang ZZ, Ye XQ, Hang JH, Chen XX. 2022.. Virus and endogenous viral element-derived small non-coding RNAs and their roles in insect-virus interaction. . Curr. Opin. Insect Sci. 49::85–92
     [Crossref] [Google Scholar]
  111. 111.
    Weiberg A, Wang M, Bellinger M, Jin HL. 2014.. Small RNAs: a new paradigm in plant-microbe interactions. . Annu. Rev. Phytopathol. 52::495–516
     [Crossref] [Google Scholar]
  112. 112.
    Weiberg A, Wang M, Lin FM, Zhao HW, Zhang ZH, et al. 2013.. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. . Science 342::118–23
     [Crossref] [Google Scholar]
  113. 113.
    Wu P, Jiang XX, Sang Q, Annan E, Cheng T, Guo XJ. 2017.. Inhibition of miR-274-3p increases BmCPV replication by regulating the expression of BmCPV NS5 gene in Bombyx mori. . Virus Genes 53::643–49
     [Crossref] [Google Scholar]
  114. 114.
    Wu P, Jie W, Shang Q, Annan E, Jiang X, et al. 2017.. DNA methylation in silkworm genome may provide insights into epigenetic regulation of response to Bombyx mori cypovirus infection. . Sci. Rep. 7::16013
     [Crossref] [Google Scholar]
  115. 115.
    Wu P, Qin GX, Qian HY, Chen T, Guo XJ. 2016.. Roles of miR-278-3p in IBP2 regulation and Bombyx mori cytoplasmic polyhedrosis virus replication. . Gene 575:(2 Part 1):264–69
     [Crossref] [Google Scholar]
  116. 116.
    Wu P, Shang Q, Dweteh OA, Huang HL, Zhang SL, et al. 2019.. Over expression of bmo-miR-2819 suppresses BmNPV replication by regulating the BmNPV ie-1 gene in Bombyx mori. . Mol. Immunol. 109::134–39
     [Crossref] [Google Scholar]
  117. 117.
    Wu X, Bhatia N, Grozinger CM, Yi SV. 2022.. Comparative studies of genomic and epigenetic factors influencing transcriptional variation in two insect species. . Genes Genom. Genet. 12::jkac230
     [Crossref] [Google Scholar]
  118. 118.
    Xiong XP, Kurthkoti K, Chang KY, Li JL, Ren XJ, et al. 2016.. miR-34 modulates innate immunity and ecdysone signaling in Drosophila. . PLOS Pathog. 12::e1006034
     [Crossref] [Google Scholar]
  119. 119.
    Xu LN, Ling YH, Wang YQ, Wang ZY, Hu BJ, et al. 2015.. Identification of differentially expressed microRNAs between Bacillus thuringiensis Cry1Ab-resistant and -susceptible strains of Ostrinia furnacalis. . Sci. Rep. 5::15461
     [Crossref] [Google Scholar]
  120. 120.
    Yan H, Bonasio R, Simola DF, Liebig J, Berger SL, Reinberg D. 2015.. DNA methylation in social insects: how epigenetics can control behavior and longevity. . Annu. Rev. Entomol. 60::435–52
     [Crossref] [Google Scholar]
  121. 121.
    Yao YL, Ma XY, Wang TY, Yan JY, Chen NF, et al. 2023.. A bacteriocyte symbiont determines whitefly sex ratio by regulating mitochondrial function. . Cell Rep. 42::112102
     [Crossref] [Google Scholar]
  122. 122.
    Zhang GM, Hussain M, Asgari S. 2014.. Regulation of arginine methyltransferase 3 by a Wolbachia-induced microRNA in Aedes aegypti and its effect on Wolbachia and dengue virus replication. . Insect Biochem. Mol. Biol. 53::81–88
     [Crossref] [Google Scholar]
  123. 123.
    Zhang GM, Hussain M, O'Neill SL, Asgari S. 2013.. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. . PNAS 110::10276–81
     [Crossref] [Google Scholar]
  124. 124.
    Zhang JH, Dong Y, Wang M, Wang HT, Yi DS, et al. 2021.. MicroRNA-315-5p promotes rice black-streaked dwarf virus infection by targeting a melatonin receptor in the small brown planthopper. . Pest Manag. Sci. 77::3561–70
     [Crossref] [Google Scholar]
  125. 125.
    Zhang SD, An SH, Hoover K, Li Z, Li XR, et al. 2018.. Host miRNAs are involved in hormonal regulation of HaSNPV-triggered climbing behaviour in Helicoverpa armigera. . Mol. Ecol. 27::459–75
     [Crossref] [Google Scholar]
  126. 126.
    Zhang X, Meng Y, Huang Y, Zhang D, Fang W. 2021.. A novel cascade allows Metarhizium robertsii to distinguish cuticle and hemocoel microenvironments during infection of insects. . PLOS Biol. 19::e3001360
     [Crossref] [Google Scholar]
  127. 127.
    Zhao Z, Li L, Zeng R, Lin L, Yuan D, et al. 2023.. 5mC modification orchestrates choriogenesis and fertilization by preventing prolonged ftz-f1 expression. . Nat. Commun. 14::8234
     [Crossref] [Google Scholar]
  128. 128.
    Zhou HJ, Wu SS, Liu L, Liu XQ, Lan SY, et al. 2022.. Drosophila Relish-mediated miR-317 expression facilitates immune homeostasis restoration via inhibiting PGRP-LC. . Eur. J. Immunol. 52::1934–45
     [Crossref] [Google Scholar]
  129. 129.
    Zhou Q, Wang ZX, Zhang J, Meng HM, Huang B. 2012.. Genome-wide identification and profiling of microRNA-like RNAs from Metarhizium anisopliae during development. . Fungal Biol. 116::1156–62
     [Crossref] [Google Scholar]
  130. 130.
    Lai YL, Zheng WL, Zheng YT, Lu HQ, Qu S, et al. 2024.. Unveiling a novel entry gate: insect foregut as an alternative infection route for fungal entomopathogens. . Innovation 5::100644
     [Google Scholar]
/content/journals/10.1146/annurev-ento-022724-010640
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Epigenetic Regulation in Insect–Microbe Interactions
Annual Review of Entomology 70, 293 (2025); https://doi.org/10.1146/annurev-ento-022724-010640
/content/journals/10.1146/annurev-ento-022724-010640
/content/journals/10.1146/annurev-ento-022724-010640
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