The emerging role of epigenetic mechanisms in insect defense against pathogens

Palli, 2021, Epigenetic regulation of post-embryonic development, Curr Opin Insect Sci, 43, 63, 10.1016/j.cois.2020.09.011 Glastad, 2019, Epigenetics in insects: genome regulation and the generation of phenotypic diversity, Annu Rev Entomol, 64, 185, 10.1146/annurev-ento-011118-111914 Zhang, 2019, Epigenetic regulation of the innate immune response to infection, Nat Rev Immunol, 19, 417, 10.1038/s41577-019-0151-6 Sommer, 2020, Phenotypic plasticity: from theory and genetics to current and future challenges, Genetics, 215, 1, 10.1534/genetics.120.303163 Ferro, 2019, Experimental evolution of immunological specificity, Proc Natl Acad Sci U S A, 116, 20598, 10.1073/pnas.1904828116 Mukherjee, 2020, Seasonal phenotype-specific expression of microRNAs during metamorphosis in the European map butterfly Araschnia levana, Arch Insect Biochem Physiol, 104, 10.1002/arch.21657 Gegner, 2021, Complete metamorphosis in Manduca sexta involves specific changes in DNA methylation patterns, Front Ecol Evol, 9, 10.3389/fevo.2021.646281 Greenwood, 2016, Current analysis of host-parasite interactions with a focus on next generation sequencing data, Zoology (Jena), 119, 298, 10.1016/j.zool.2016.06.010 Mukherjee, 2017, Experimental evolution of resistance against Bacillus thuringiensis in the insect model host Galleria mellonella results in epigenetic modifications, Virulence, 8, 1618, 10.1080/21505594.2017.1325975 Mukherjee, 2019, Epigenetic mechanisms mediate the experimental evolution of resistance against parasitic fungi in the greater wax moth Galleria mellonella, Sci Rep, 9, 10.1038/s41598-018-36829-8 Vilcinskas, 2016, The role of epigenetics in host-parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum, Zoology (Jena), 119, 273, 10.1016/j.zool.2016.05.004 Richard, 2019, Epigenetics and insect polyphenism: mechanisms and climate change impacts, Curr Opin Insect Sci, 35, 138, 10.1016/j.cois.2019.06.013 Srinivasan, 2012, Aphids: a model for polyphenism and epigenetics, Genet Res Int, 2012 Oldroyd, 2021, The role of epigenetics, particularly DNA methylation, in the evolution of caste in insect societies, Philos Trans R Soc Lond B Biol Sci, 376, 10.1098/rstb.2020.0115 Gerardo, 2010, Immunity and other defenses in pea aphids, Acyrthosiphon pisum, Genome Biol, 11, 10.1186/gb-2010-11-2-r21 Heitmueller, 2017, Epigenetic mechanisms regulate innate immunity against uropathogenic and commensal-like Escherichia coli in the surrogate insect model Galleria mellonella, Infect Immun, 85, 10.1128/IAI.00336-17 Maleszka, 2016, Epigenetic code and insect behavioural plasticity, Curr Opin Insect Sci, 15, 45, 10.1016/j.cois.2016.03.003 Lyko, 2018, The DNA methyltransferase family: a versatile toolkit for epigenetic regulation, Nat Rev Genet, 19, 81, 10.1038/nrg.2017.80 Bewick, 2017, Evolution of DNA methylation across insects, Mol Biol Evol, 34, 654 Huang, 2019, DNA methylomes and transcriptomes analysis reveal implication of host DNA methylation machinery in BmNPV proliferation in Bombyx mori, BMC Genomics, 20, 10.1186/s12864-019-6146-7 Mitsudome, 2015, Biochemical characterization of maintenance DNA methyltransferase DNMT-1 from silkworm, Bombyx mori, Insect Biochem Mol Biol, 58, 55, 10.1016/j.ibmb.2015.01.008 Schulz, 2018, Dnmt1 has an essential function despite the absence of CpG DNA methylation in the red flour beetle Tribolium castaneum, Sci Rep, 8, 10.1038/s41598-018-34701-3 Bewick, 2019, Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus, Epigenetics Chromatin, 12, 10.1186/s13072-018-0246-5 Goll, 2005, Eukaryotic cytosine methyltransferases, Annu Rev Biochem, 74, 481, 10.1146/annurev.biochem.74.010904.153721 Mallon, 2016, Acute and chronic gregarisation are associated with distinct DNA methylation fingerprints in desert locusts, Sci Rep, 6, 10.1038/srep35608 Bewick, 2016, Evolution of DNA methylation across insects, Mol Biol Evol, 34, 654 Kausar, 2021, A review on the DNA methyltransferase family of insects: aspect and prospects, Int J Biol Macromol, 186, 289, 10.1016/j.ijbiomac.2021.06.205 Abhyankar, 2018, Drosophila DNA/RNA methyltransferase contributes to robust host defense in aging animals by regulating sphingolipid metabolism, J Exp Biol, 221 Baradaran, 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, 10.1016/j.jinsphys.2019.103939 Özbek, 2020, Reprograming of epigenetic mechanisms controlling host insect immunity and development in response to egglaying by a parasitoid wasp, Proc Biol Sci, 287 Claudio-Piedras, 2020, DNA methylation in Anopheles albimanus modulates the midgut immune response against Plasmodium berghei, Front Immunol, 10, 10.3389/fimmu.2019.03025 Hunt, 2010, Functional conservation of DNA methylation in the pea aphid and the honeybee, Genome Biol Evol, 2, 719, 10.1093/gbe/evq057 Hunt, 2013, Patterning and regulatory associations of DNA methylation are mirrored by histone modifications in insects, Genome Biol Evol, 5, 591, 10.1093/gbe/evt030 Strichman-Almashanu, 2002, A genome-wide screen for normally methylated human CpG islands that can identify novel imprinted genes, Genome Res, 12, 543, 10.1101/gr.224102 Glastad, 2011, DNA methylation in insects: on the brink of the epigenomic era, Insect Mol Biol, 20, 553, 10.1111/j.1365-2583.2011.01092.x Cingolani, 2013, Intronic non-CG DNA hydroxymethylation and alternative mRNA splicing in honey bees, BMC Genomics, 14, 10.1186/1471-2164-14-666 Xiang, 2013, Comparative methylomics between domesticated and wild silkworms implies possible epigenetic influences on silkworm domestication, BMC Genomics, 14, 10.1186/1471-2164-14-646 Beeler, 2014, Whole-genome DNA methylation profile of the jewel wasp (Nasonia vitripennis), G3 (Bethesda), 4, 383, 10.1534/g3.113.008953 Provataris, 2018, Signatures of DNA methylation across insects suggest reduced DNA methylation levels in holometabola, Genome Biol Evol, 10, 1185, 10.1093/gbe/evy066 Song, 2017, Genome-wide DNA methylomes from discrete developmental stages reveal the predominance of non-CpG methylation in Tribolium castaneum, DNA Res, 24, 445, 10.1093/dnares/dsx016 Bain, 2021, Sex-specific expression and DNA methylation in a species with extreme sexual dimorphism and paternal genome elimination, Mol Ecol, 00, 1 Rider, 2010, Chromatin-remodelling proteins of the pea aphid, Acyrthosiphon pisum (Harris), Insect Mol Biol, 19, 201, 10.1111/j.1365-2583.2009.00972.x Mukherjee, 2012, Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection, Front Zool, 9, 10.1186/1742-9994-9-25 George, 2020, Histone deacetylase 11 knockdown blocks larval development and metamorphosis in the red flour beetle, Tribolium castaneum, Front Genet, 11, 10.3389/fgene.2020.00683 George, 2019, Histone deacetylase 1 suppresses Kruppel homolog 1 gene expression and influences juvenile hormone action in Tribolium castaneum, Proc Natl Acad Sci U S A, 116, 17759, 10.1073/pnas.1909554116 Roy, 2018, Epigenetic modifications acetylation and deacetylation play important roles in juvenile hormone action, BMC Genomics, 19, 10.1186/s12864-018-5323-4 Kirfel, 2020, Inhibition of histone acetylation and deacetylation enzymes affects longevity, development, and fecundity in the pea aphid (Acyrthosiphon pisum), Arch Insect Biochem Physiol, 103, 10.1002/arch.21614 Ambros, 2004, The functions of animal microRNAs, Nature, 431, 350, 10.1038/nature02871 Bartel, 2004, MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 116, 281, 10.1016/S0092-8674(04)00045-5 Lu, 2009, MicroRNA in the immune system, microRNA as an immune system, Immunology, 127, 291, 10.1111/j.1365-2567.2009.03092.x Macfarlane, 2010, MicroRNA: biogenesis, function and role in cancer, Curr Genomics, 11, 537, 10.2174/138920210793175895 Winter, 2007, Anopheles gambiae miRNAs as actors of defence reaction against Plasmodium invasion, Nucleic Acids Res, 35, 6953, 10.1093/nar/gkm686 Mukherjee, 2020, MicroRNAs regulate innate immunity against uropathogenic and commensal-like Escherichia coli infections in the surrogate insect model Galleria mellonella, Sci Rep, 10, 10.1038/s41598-020-59407-3 Mukherjee, 2014, Development and immunity-related microRNAs of the lepidopteran model host Galleria mellonella, BMC Genomics, 15, 10.1186/1471-2164-15-705 Freitak, 2012, Gender- and stressor-specific microRNA expression in Tribolium castaneum, Biol Lett, 8, 860, 10.1098/rsbl.2012.0273 Kurtz, 2016, Host-parasite coevolution-rapid reciprocal adaptation and its genetic basis, Zoology (Jena), 119, 241, 10.1016/j.zool.2016.06.011 Gegner, 2019, Epigenetic mechanisms are involved in sex-specific trans-generational immune priming in the lepidopteran model host Manduca sexta, Front Physiol, 10, 10.3389/fphys.2019.00137 Schulz, 2018, Paternal knockdown of Dnmt2 increases offspring susceptibility to bacterial infection, bioRxiv [Preprint] Habig, 2021, Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus, Nat Commun, 12, 10.1038/s41467-021-26108-y Dubovskiy, 2013, Can insects develop resistance to insect pathogenic fungi?, PLoS One, 8, 10.1371/journal.pone.0060248 Dubovskiy, 2013, More than a colour change: insect melanism, disease resistance and fecundity, Proc Biol Sci, 280 Dubovskiy, 2016, Immuno-physiological adaptations confer wax moth Galleria mellonella resistance to Bacillus thuringiensis, Virulence, 7, 860, 10.1080/21505594.2016.1164367 Etebari, 2015, Genome wide discovery of long intergenic non-coding RNAs in Diamondback moth (Plutella xylostella) and their expression in insecticide resistant strains, Sci Rep, 5, 10.1038/srep14642 Ali, 2020, Re-thinking adaptive immunity in the beetles: evolutionary and functional trajectories of lncRNAs, Genomics, 112, 1425, 10.1016/j.ygeno.2019.08.012 Mei-zhen, 2019, Progress and prospects of noncoding RNAs in insects, J Integr Agric, 18, 729, 10.1016/S2095-3119(18)61976-8 Satyavathi, 2017, Long non-coding RNAs regulating immunity in insects, Noncoding RNA, 3 Oppold, 2015, Epigenetic alterations and decreasing insecticide sensitivity of the Asian tiger mosquito Aedes albopictus, Ecotoxicol Environ Saf, 122, 45, 10.1016/j.ecoenv.2015.06.036 Brevik, 2020, Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata, Evol Appl, 14, 746, 10.1111/eva.13153 Zenk, 2017, Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition, Science, 357, 212, 10.1126/science.aam5339 Samata, 2020, Intergenerationally maintained histone H4 lysine 16 acetylation is instructive for future gene activation, Cell, 182, 127, 10.1016/j.cell.2020.05.026