1932

Abstract

Epigenetic inheritance is fundamentally important to cellular differentiation and developmental plasticity. In this review, we provide an introduction to the field of molecular epigenetics in insects. Epigenetic information is passed across cell divisions through the methylation of DNA, the modification of histone proteins, and the activity of noncoding RNAs. Much of our knowledge of insect epigenetics has been gleaned from a few model species. However, more studies of epigenetic information in traditionally nonmodel taxa will help advance our understanding of the developmental and evolutionary significance of epigenetic inheritance in insects. To this end, we also provide a brief overview of techniques for profiling and perturbing individual facets of the epigenome. Doing so in diverse cellular, developmental, and taxonomic contexts will collectively help shed new light on how genome regulation results in the generation of diversity in insect form and function.

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2019-01-07
2024-06-18
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Literature Cited

  1. 1.  Ahmad K, Henikoff S 2002. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9:1191–200
    [Google Scholar]
  2. 2.  Alabert C, Barth TK, Reverón-Gómez N, Sidoli S, Schmidt A et al. 2015. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev 29:585–90
    [Google Scholar]
  3. 3.  Alabert C, Groth A 2012. Chromatin replication and epigenome maintenance. Nat. Rev. Mol. Cell Biol. 13:153–67
    [Google Scholar]
  4. 4.  Arensburger P, Hice RH, Wright JA, Craig NL, Atkinson PW 2011. The mosquito Aedes aegypti has a large genome size and high transposable element load but contains a low proportion of transposon-specific piRNAs. BMC Genom 12:606
    [Google Scholar]
  5. 5.  Asgari S 2013. MicroRNA functions in insects. Insect Biochem. Mol. Biol. 43:388–97
    [Google Scholar]
  6. 6.  Badeaux AI, Shi Y 2013. Emerging roles for chromatin as a signal integration and storage platform. Nat. Rev. Mol. Cell Biol. 14:211–24
    [Google Scholar]
  7. 7.  Baldi S, Becker P 2013. The variant histone H2A.V of Drosophila—three roles, two guises. Chromosoma 122:245–58
    [Google Scholar]
  8. 8.  Bannister AJ, Kouzarides T 2011. Regulation of chromatin by histone modifications. Cell Res 21:381–95
    [Google Scholar]
  9. 9.  Bartlett DW, Davis ME 2006. Insights into the kinetics of siRNA-mediated gene silencing from live-cell and live-animal bioluminescent imaging. Nucleic Acids Res 34:322–33
    [Google Scholar]
  10. 10.  Bassett AR, Tibbit C, Ponting CP, Liu J-L 2013. Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4:220–28
    [Google Scholar]
  11. 11.  Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L et al. 2015. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520:243–47
    [Google Scholar]
  12. 12.  Bell O, Tiwari VK, Thoma NH, Schubeler D 2011. Determinants and dynamics of genome accessibility. Nat. Rev. Genet. 12:554–64
    [Google Scholar]
  13. 13.  Belles X 2017. MicroRNAs and the evolution of insect metamorphosis. Annu. Rev. Entomol. 62:111–25
    [Google Scholar]
  14. 14.  Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ 2017. Evolution of DNA methylation across insects. Mol. Biol. Evol. 34:654–65
    [Google Scholar]
  15. 15.  Blythe SA, Wieschaus EF 2016. Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis. eLife 5:e20148
    [Google Scholar]
  16. 16.  Bonasio R 2012. Emerging topics in epigenetics: ants, brains, and noncoding RNAs. Ann. N. Y. Acad. Sci. 1260:14–23
    [Google Scholar]
  17. 17.  Bonasio R, Li QY, Lian JM, Mutti NS, Jin LJ et al. 2012. Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr. Biol 22:1755–64
    [Google Scholar]
  18. 18.  Bonasio R, Shiekhattar R 2014. Regulation of transcription by long noncoding RNAs. Annu. Rev. Genet. 48:433–55
    [Google Scholar]
  19. 19.  Bonasio R, Tu SJ, Reinberg D 2010. Molecular signals of epigenetic states. Science 330:612–16
    [Google Scholar]
  20. 20.  Bose P, Dai Y, Grant S 2014. Histone deacetylase inhibitor (HDACI) mechanisms of action: emerging insights. Pharmacol. Ther. 143:323–36
    [Google Scholar]
  21. 21.  Brind'Amour J, Liu S, Hudson M, Chen C, Karimi MM, Lorincz MC 2015. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat. Comm. 6:6033
    [Google Scholar]
  22. 22.  Brookes E, Pombo A 2009. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep 10:1213–19
    [Google Scholar]
  23. 23.  Buchwald M, Krämer OH, Heinzel T 2009. HDACi—targets beyond chromatin. Cancer Lett 280:160–67
    [Google Scholar]
  24. 24.  Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Meth. 10:1213–18
    [Google Scholar]
  25. 25.  Carthew RW, Sontheimer EJ 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–55
    [Google Scholar]
  26. 26.  Castel SE, Martienssen RA 2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14:100–12
    [Google Scholar]
  27. 27.  Cech TR, Steitz JA 2014. The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157:77–94
    [Google Scholar]
  28. 28.  Chambeyron S, Seitz H 2014. Insect small non-coding RNA involved in epigenetic regulations. Curr. Opin. Insect Sci. 1:1–9
    [Google Scholar]
  29. 29.  Cheng JC, Matsen CB, Gonzales FA, Ye W, Greer S et al. 2003. Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J. Natl. Cancer Inst. 95:399–409
    [Google Scholar]
  30. 30.  Conrad T, Akhtar A 2012. Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nat. Rev. Genet. 13:123–34
    [Google Scholar]
  31. 31.  Corces MR, Trevino AE, Hamilton EG, Greenside PG, Sinnott-Armstrong NA et al. 2017. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Meth. 14:959–62
    [Google Scholar]
  32. 32.  Cunningham CB, Ji LX, Wiberg RAW, Shelton J, McKinney EC et al. 2015. The genome and methylome of a beetle with complex social behavior, Nicrophorus vespilloides (Coleoptera: Silphidae). Genome Biol. Evol. 7:3383–96
    [Google Scholar]
  33. 33.  Czech B, Hannon GJ 2016. One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem. Sci. 41:324–37
    [Google Scholar]
  34. 34.  Dahlin JL, Nelson KM, Strasser JM, Barsyte-Lovejoy D, Szewczyk MM et al. 2017. Assay interference and off-target liabilities of reported histone acetyltransferase inhibitors. Nat. Comm. 8:1527
    [Google Scholar]
  35. 35.  Davie K, Jacobs J, Atkins M, Potier D, Christiaens V et al. 2015. Discovery of transcription factors and regulatory regions driving in vivo tumor development by ATAC-seq and FAIRE-seq open chromatin profiling. PLOS Genet 11:e1004994
    [Google Scholar]
  36. 36.  de Ruijter AJM, van Gennip AH, Caron HN, Kemp S, van Kuilenburg ABP 2003. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 370:737–49
    [Google Scholar]
  37. 37.  Dowling D, Pauli T, Donath A, Meusemann K, Podsiadlowski L et al. 2016. Phylogenetic origin and diversification of RNAi pathway genes in insects. Genome Biol. Evol. 8:3784–93
    [Google Scholar]
  38. 38.  Fatica A, Bozzoni I 2014. Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 15:7–21
    [Google Scholar]
  39. 39.  Ferguson-Smith AC 2011. Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12:565–75
    [Google Scholar]
  40. 40.  Foret S, Kucharski R, Pellegrini M, Feng SH, Jacobsen SE et al. 2012. DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. PNAS 109:4968–73
    [Google Scholar]
  41. 41.  Foret S, Kucharski R, Pittelkow Y, Lockett GA, Maleszka R 2009. Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genom 10:472
    [Google Scholar]
  42. 42.  Galbraith DA, Kocher SD, Glenn T, Albert I, Hunt GJ et al. 2016. Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera). PNAS 113:1020–25
    [Google Scholar]
  43. 43.  Gardini A, Shiekhattar R 2015. The many faces of long noncoding RNAs. FEBS J 282:1647–57
    [Google Scholar]
  44. 44.  Giles KE, Woolnough JL, Atwood B 2016. ncRNA function in chromatin organization. Epigenetic Gene Expression and Regulation S Huang, MD Litt, CA Blakey 117–48 London: Academic Press
    [Google Scholar]
  45. 45.  Glastad KM, Arsenault SV, Vertacnik KL, Geib SM, Kay S et al. 2017. Variation in DNA methylation is not consistently reflected by sociality in Hymenoptera. Genome Biol. Evol. 9:1687–98
    [Google Scholar]
  46. 46.  Glastad KM, Chau LM, Goodisman MAD 2015. Epigenetics in social insects. Advances in Insect Physiology: Genomics, Physiology and Behavior of Social Insects A Zayed, CF Kent 48227–69 Oxford: Academic
    [Google Scholar]
  47. 47.  Glastad KM, Gokhale K, Liebig J, Goodisman MAD 2016. The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Sci. Rep 6:37110
    [Google Scholar]
  48. 48.  Glastad KM, Hunt BG, Yi SV, Goodisman MAD 2014. Epigenetic inheritance and genome regulation: Is DNA methylation linked to ploidy in haplodiploid insects?. Proc. Biol. Sci. 281:20140411
    [Google Scholar]
  49. 49.  Glastad KM, Hunt BG, Goodisman MAD 2015. DNA Methylation and chromatin organization in insects: insights from the ant Camponotus floridanus. . Genome Biol. Evol 7:931–42
    [Google Scholar]
  50. 50.  Greer EL, Shi Y 2012. Histone methylation: a dynamic mark in health, disease and inheritance. Nat. Rev. Genet. 13:343–57
    [Google Scholar]
  51. 51.  Gu LQ, Knipple DC 2013. Recent advances in RNA interference research in insects: implications for future insect pest management strategies. Crop Prot 45:36–40
    [Google Scholar]
  52. 52.  Ha M, Kim VN 2014. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15:509–24
    [Google Scholar]
  53. 53.  Han P, Chang CP 2015. Long non-coding RNA and chromatin remodeling. RNA Biol 12:1094–98
    [Google Scholar]
  54. 54.  Heard E, Martienssen RA 2014. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157:95–109
    [Google Scholar]
  55. 55.  Henikoff S 2008. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 9:15–26
    [Google Scholar]
  56. 56.  Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B et al. 2012. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15:1371–73
    [Google Scholar]
  57. 57.  Hirakata S, Siomi MC 2016. piRNA biogenesis in the germline: from transcription of piRNA genomic sources to piRNA maturation. Biochim. Biophys. Acta 1859:82–92
    [Google Scholar]
  58. 58.  Holoch D, Moazed D 2015. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16:71–84
    [Google Scholar]
  59. 59.  Housman G, Ulitsky I 2016. Methods for distinguishing between protein-coding and long noncoding RNAs and the elusive biological purpose of translation of long noncoding RNAs. Biochim. Biophys. Acta 1859:31–40
    [Google Scholar]
  60. 60.  Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin HF 2013. A major epigenetic programming mechanism guided by piRNAs. Dev. Cell 24:502–16
    [Google Scholar]
  61. 61.  Hublitz P, Albert M, Peters AHFM 2009. Mechanisms of transcriptional repression by histone lysine methylation. Int. J. Dev. Biol. 53:335–54
    [Google Scholar]
  62. 62.  Hunt BG, Glastad KM, Yi SV, Goodisman MAD 2013. The function of intragenic DNA methylation: insights from insect epigenomes. Integr. Comp. Biol. 53:319–28
    [Google Scholar]
  63. 63.  Jayakodi M, Jung JW, Park D, Ahn YJ, Lee SC et al. 2015. Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera. BMC Genom 16:680
    [Google Scholar]
  64. 64.  Jones PA 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13:484–92
    [Google Scholar]
  65. 65.  Jones PA, Taylor SM 1980. Cellular-differentiation, cytidine analogs and DNA methylation. Cell 20:85–93
    [Google Scholar]
  66. 66.  Kasinathan S, Orsi GA, Zentner GE, Ahmad K, Henikoff S 2014. High-resolution mapping of transcription factor binding sites on native chromatin. Nat. Meth. 11:203–9
    [Google Scholar]
  67. 67.  Kelleher ES 2016. Reexamining the P-element invasion of Drosophila melanogaster through the lens of piRNA silencing. Genetics 203:1513–31
    [Google Scholar]
  68. 68.  Kharchenko PV, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC et al. 2011. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471:480–85
    [Google Scholar]
  69. 69.  Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H et al. 2014. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 509:633–36
    [Google Scholar]
  70. 70.  Kohler C, Wolff P, Spillane C 2012. Epigenetic mechanisms underlying genomic imprinting in plants. Annu. Rev. Plant Biol. 63:331–52
    [Google Scholar]
  71. 71.  Kucharski R, Maleszka J, Foret S, Maleszka R 2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–30
    [Google Scholar]
  72. 72.  Kulaeva OI, Hsieh FK, Studitsky VM 2010. RNA polymerase complexes cooperate to relieve the nucleosomal barrier and evict histones. PNAS 107:11325–30
    [Google Scholar]
  73. 73.  Kung JTY, Colognori D, Lee JT 2013. Long noncoding RNAs: past, present, and future. Genetics 193:651–69
    [Google Scholar]
  74. 74.  Kuroda MI, Hilfiker A, Lucchesi JC 2016. Dosage compensation in Drosophila—a model for the coordinate regulation of transcription. Genetics 204:435–50
    [Google Scholar]
  75. 75.  Lakhotia SC 2015. Divergent actions of long noncoding RNAs on X-chromosome remodelling in mammals and Drosophila achieve the same end result: dosage compensation. J. Genet. 94:575–84
    [Google Scholar]
  76. 76.  Lewis JJ, van der Burg KRL, Mazo-Vargas A, Reed RD 2016. ChIP-seq-annotated Heliconiuserato genome highlights patterns of cis-regulatory evolution in Lepidoptera. Cell Rep 16:2855–63
    [Google Scholar]
  77. 77.  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
    [Google Scholar]
  78. 78.  Li YF, Sasaki H 2011. Genomic imprinting in mammals: its life cycle, molecular mechanisms and reprogramming. Cell Res 21:466–73
    [Google Scholar]
  79. 79.  Libbrecht R, Oxley PR, Keller L, Kronauer DJC 2016. Robust DNA methylation in the clonal raider ant brain. Curr. Biol. 26:391–95
    [Google Scholar]
  80. 80.  Lim JP, Brunet A 2013. Bridging the transgenerational gap with epigenetic memory. Trends Genet 29:176–86
    [Google Scholar]
  81. 81.  Liu YJ, Zhang JY, Li AM, Liu ZW, Zhang YY, Sun XH 2016. Detection of Piwi-interacting RNAs based on sequence features. Genet. Mol. Res. 15:gmr8638
    [Google Scholar]
  82. 82.  Lopez-Ezquerra A, Harrison MC, Bornberg-Bauer E 2017. Comparative analysis of lincRNA in insect species. BMC Evol. Biol. 17:155
    [Google Scholar]
  83. 83.  Löser E, Latreille D, Iovino N 2016. Chromatin preparation and chromatin immuno-precipitation from Drosophila embryos. Polycomb Group Proteins: Methods and Protocols C Lanzuolo, B Bodega 23–36 New York: Springer Sci. Bus.
    [Google Scholar]
  84. 84.  Lucas KJ, Zhao B, Liu SP, Raikhel AS 2015. Regulation of physiological processes by microRNAs in insects. Curr. Opin. Insect Sci. 11:1–7
    [Google Scholar]
  85. 85.  Luteijn MJ, Ketting RF 2013. PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat. Rev. Genet. 14:523–34
    [Google Scholar]
  86. 86.  Lyko F 2018. The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat. Rev. Genet. 19:81–92
    [Google Scholar]
  87. 87.  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
    [Google Scholar]
  88. 88.  Maleszka R 2016. Epigenetic code and insect behavioural plasticity. Curr. Opin. Insect Sci. 15:45–52
    [Google Scholar]
  89. 89.  Malik HS, Henikoff S 2003. Phylogenomics of the nucleosome. Nat. Struct. Mol. Biol. 10:882–91
    [Google Scholar]
  90. 90.  Marco A 2012. Regulatory RNAs in the light of Drosophila genomics. Brief. Funct. Genom. 11:356–65
    [Google Scholar]
  91. 91.  Margueron R, Reinberg D 2010. Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 11:285–96
    [Google Scholar]
  92. 92.  Maumus F, Fiston-Lavier AS, Quesneville H 2015. Impact of transposable elements on insect genomes and biology. Curr. Opin. Insect Sci. 7:30–36
    [Google Scholar]
  93. 93.  Mayer W, Niveleau A, Walter J, Fundele R, Haaf T 2000. Embryogenesis: demethylation of the zygotic paternal genome. Nature 403:501–2
    [Google Scholar]
  94. 94.  Mazo-Vargas A, Concha C, Livraghi L, Massardo D, Wallbank RW et al. 2017. Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity. PNAS 114:10701–706
    [Google Scholar]
  95. 95.  Meller VH, Joshi SS, Deshpande N 2015. Modulation of chromatin by noncoding RNA. Annu. Rev. Genet. 49:673–95
    [Google Scholar]
  96. 96.  Mercer TR, Mattick JS 2013. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20:300–7
    [Google Scholar]
  97. 97.  Mito Y, Henikoff JG, Henikoff S 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37:1090–97
    [Google Scholar]
  98. 98.  Mitsudome T, Mon H, Xu J, Li Z, Lee JM et al. 2015. Biochemical characterization of maintenance DNA methyltransferase DNMT-1 from silkworm. Bombyx mori. Insect Biochem. Mol. Biol. 58:55–65
    [Google Scholar]
  99. 99.  Mukherjee K, Twyman RM, Vilcinskas A 2015. Insects as models to study the epigenetic basis of disease. Prog. Biophys. Mol. Biol. 118:69–78
    [Google Scholar]
  100. 100.  Nazer E, Lei EP 2014. Modulation of chromatin modifying complexes by noncoding RNAs in trans. Curr. Opin. Genet. Dev 25:68–73
    [Google Scholar]
  101. 101.  Nejepinska J, Flemr M, Svoboda P 2012. The canonical RNA interference pathway in animals. Regulatory RNAs B Mallick 111–49 Heidelberg, Ger: Springer
    [Google Scholar]
  102. 102.  Neri F, Rapelli S, Krepelova A, Incarnato D, Parlato C et al. 2017. Intragenic DNA methylation prevents spurious transcription initiation. Nature 543:72–77
    [Google Scholar]
  103. 103.  O'Neill LP, Turner BM 2003. Immunoprecipitation of native chromatin: NChIP. Methods 31:76–82
    [Google Scholar]
  104. 104.  Park PJ 2009. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10:669–80
    [Google Scholar]
  105. 105.  Paroo Z, Corey DR 2004. Challenges for RNAi in vivo. Trends Biotechnol 22:390–94
    [Google Scholar]
  106. 106.  Perrimon N, Ni J-Q, Perkins L 2010. In vivo RNAi: today and tomorrow. Cold Spring Harbor. Perspect. Biol. 2:a003640
    [Google Scholar]
  107. 107.  Peterson CL, Laniel M-A 2004. Histones and histone modifications. Curr. Biol 14:R546–51
    [Google Scholar]
  108. 108.  Picao-Osorio J, Lago-Baldaia I, Patraquim P, Alonso CR 2017. Pervasive behavioral effects of microRNA regulation in Drosophila. Genetics 206:1535–48
    [Google Scholar]
  109. 109.  Plongthongkum N, Diep DH, Zhang K 2014. Advances in the profiling of DNA modifications: cytosine methylation and beyond. Nat. Rev. Genet. 15:647
    [Google Scholar]
  110. 110.  Queller DC 2003. Theory of genomic imprinting conflict in social insects. BMC Evol. Biol. 3:15
    [Google Scholar]
  111. 111.  Quinn JJ, Zhang QFC, Georgiev P, Ilik IA, Akhtar A, Change HY 2016. Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Genes Dev 30:191–207
    [Google Scholar]
  112. 112.  Rechavi O, Lev I 2017. Principles of transgenerational small RNA inheritance in Caenorhabditis elegans. Curr. Biol 27:R720–30
    [Google Scholar]
  113. 113.  Remnant EJ, Ashe A, Young PE, Buchmann G, Beekman M et al. 2016. Parent-of-origin effects on genome-wide DNA methylation in the Cape honey bee (Apis mellifera capensis) may be confounded by allele-specific methylation. BMC Genom 17:226
    [Google Scholar]
  114. 114.  Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J et al. 2003. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12:1591–98
    [Google Scholar]
  115. 115.  Rozhkov NV, Hammell M, Hannon GJ 2013. Multiple roles for Piwi in silencing Drosophila transposons. Genes Dev 27:400–412
    [Google Scholar]
  116. 116.  Sarkar A, Volff JN, Vaury C 2017. piRNAs and their diverse roles: a transposable element-driven tactic for gene regulation?. FASEB J 31:436–46
    [Google Scholar]
  117. 117.  Schaefer KA, Wu W-H, Colgan DF, Tsang SH, Bassuk AG, Mahajan VB 2017. Unexpected mutations after CRISPR-Cas9 editing in vivo. Nat. Meth. 14:547–48
    [Google Scholar]
  118. 118.  Schmidl C, Rendeiro AF, Sheffield NC, Bock C 2015. ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors. Nat. Meth. 12:963–65
    [Google Scholar]
  119. 119.  Scott JG, Michel K, Bartholomay LC, Siegfried BD, Hunter WB et al. 2013. Towards the elements of successful insect RNAi. J. Insect Physiol. 59:1212–21
    [Google Scholar]
  120. 120.  Shalem O, Sanjana NE, Zhang F 2015. High-throughput functional genomics using CRISPR-Cas9. Nat. Rev. Genet. 16:299–311
    [Google Scholar]
  121. 121.  Shpigler HY, Saul MC, Murdoch EE, Cash-Ahmed AC, Seward CH et al. 2017. Behavioral, transcriptomic and epigenetic responses to social challenge in honey bees. Genes Brain Behav 16:579–91
    [Google Scholar]
  122. 122.  Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B et al. 2011. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479:74–79
    [Google Scholar]
  123. 123.  Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C et al. 2016. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351aac6633
  124. 124.  Simola DF, Ye CY, Mutti NS, Dolezal K, Bonasio R et al. 2013. A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res 23:486–96
    [Google Scholar]
  125. 125.  Singh BN, Zhang G, Hwa YL, Li J, Dowdy SC, Jiang S-W 2010. Nonhistone protein acetylation as cancer therapy targets. Expert Rev. Anticancer Ther 10:935–54
    [Google Scholar]
  126. 126.  Spannhoff A, Kim YY, Raynal NJM, Gharibyan V, Su M-B et al. 2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep 12:238–43
    [Google Scholar]
  127. 127.  Su J, Wang F, Cai Y, Jin J 2016. The functional analysis of histone acetyltransferase MOF in tumorigenesis. Int. J. Mol. Sci. 17:99
    [Google Scholar]
  128. 128.  Suganuma T, Workman JL 2011. Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 80:473–99
    [Google Scholar]
  129. 129.  Sun D, Guo ZJ, Liu Y, Zhang YJ 2017. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Front. Physiol. 8:608
    [Google Scholar]
  130. 130.  Sundaram AY, Hughes T, Biondi S, Bolduc N, Bowman SK et al. 2016. A comparative study of ChIP-seq sequencing library preparation methods. BMC Genom 17:816
    [Google Scholar]
  131. 131.  Suzuki MM, Bird A 2008. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9:465–76
    [Google Scholar]
  132. 132.  Talbert PB, Henikoff S 2010. Histone variants—ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11:264–75
    [Google Scholar]
  133. 133.  Thinnes CC, England KS, Kawamura A, Chowdhury R, Schofield CJ, Hopkinson RJ 2014. Targeting histone lysine demethylases—progress, challenges, and the future. Biochim. Biophys. Acta Gene Reg. Mech. 1839:1416–32
    [Google Scholar]
  134. 134.  Trible W, Olivos-Cisneros L, McKenzie SK, Saragosti J, Chang N-C et al. 2017. orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–35e710
    [Google Scholar]
  135. 135.  Ulitsky I 2016. Evolution to the rescue: using comparative genomics to understand long non-coding RNAs. Nat. Rev. Genet. 17:601–14
    [Google Scholar]
  136. 136.  Verlinden H 2017. Insect Epigenetics 53 London: Academic
    [Google Scholar]
  137. 137.  Vodovar N, Bronkhorst AW, van Cleef KWR, Miesen P, Blanc H et al. 2012. Arbovirus-derived piRNAs exhibit a ping-pong signature in mosquito cells. PLOS ONE 7:e30861
    [Google Scholar]
  138. 138.  Waddington CH 1942. The epigenotype. Endeavour 1:18–20
    [Google Scholar]
  139. 139.  Wang X, Werren JH, Clark AG 2016. Allele-specific transcriptome and methylome analysis reveals stable inheritance and cis-regulation of DNA methylation in Nasonia. PLOS Biol 14:e1002500
    [Google Scholar]
  140. 140.  Wang XH, Fang XD, Yang PC, Jiang XT, Jiang F et al. 2014. The locust genome provides insight into swarm formation and long-distance flight. Nat. Comm. 5:1–9
    [Google Scholar]
  141. 141.  Wang Y, Jorda M, Jones PL, Maleszka R, Ling X et al. 2006. Functional CpG methylation system in a social insect. Science 314:645–47
    [Google Scholar]
  142. 142.  Wu YQ, Cheng TC, Liu C, Liu DL, Zhang Q et al. 2016. Systematic identification and characterization of long non-coding RNAs in the silkworm. Bombyx mori. PLOS ONE 11:e0147147
    [Google Scholar]
  143. 143.  Xiang H, Zhu JD, Chen QA, Dai FY, Li X et al. 2010. Single base–resolution methylome of the silkworm reveals a sparse epigenomic map. Nat. Biotechnol. 28:756–56
    [Google Scholar]
  144. 144.  Xiong Y, Dowdy SC, Podratz KC, Jin F, Attewell JR et al. 2005. Histone deacetylase inhibitors decrease DNA methyltransferase-3B messenger RNA stability and down-regulate de novo DNA methyltransferase activity in human endometrial cells. Cancer Res 65:2684–89
    [Google Scholar]
  145. 145.  Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M et al. 2017. An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170:736–47e739
    [Google Scholar]
  146. 146.  Yan H, Simola DF, Bonasio R, Liebig J, Berger SL, Reinberg D 2014. Eusocial insects as emerging models for behavioural epigenetics. Nat. Rev. Genet. 15:677–88
    [Google Scholar]
  147. 147.  Yin Y, Morgunova E, Jolma A, Kaasinen E, Sahu B et al. 2017. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science 356:eaaj2239
    [Google Scholar]
  148. 148.  Yu N, Christiaens O, Liu JS, Niu JZ, Cappelle K et al. 2013. Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci 20:4–14
    [Google Scholar]
  149. 149.  Zemach A, McDaniel IE, Silva P, Zilberman D 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916–19
    [Google Scholar]
  150. 150.  Zentner GE, Henikoff S 2013. Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 20:259–66
    [Google Scholar]
  151. 151.  Zhou VW, Goren A, Bernstein BE 2011. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12:7–18
    [Google Scholar]
/content/journals/10.1146/annurev-ento-011118-111914
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