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The Maize Methylome

  • Jaclyn M. Noshay
  • Peter A. Crisp
  • Nathan M. SpringerEmail author
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

DNA methylation is a chromatin modification that has generally been associated with gene silencing or heterochromatin. Plants have mechanisms to allow for the stable inheritance of DNA methylation through mitosis or meiosis. This creates the potential for DNA methylation to provide epigenetic inheritance for traits in maize and other crops. Epigenetics refers to heritable transmission of information that is not solely attributable to DNA sequence. Several examples of epigenetic inheritance were first described in maize including paramutation, imprinting, and transposable element inactivation. There is evidence that DNA methylation is associated with each of these epigenetic phenomena. In addition, natural variation for epigenetic states may contribute substantially to variation among maize inbreds and could be an important source of variation for crop improvement. Advances in our understanding of the molecular mechanisms controlling DNA methylation in Arabidopsis have provided clues to the genes and pathways likely to be important in maize. Recent technological developments have provided the opportunity to characterize the genome-wide distribution of DNA methylation in the maize genome. This has provided insights into the patterns of DNA methylation in plant species with large, complex genomes and has led to the identification of potential cryptic genomic information that is silenced by DNA methylation. We will summarize current understanding of the mechanisms that regulate methylation and factors that influence variation and stability of the maize methylome.

References

  1. Alleman M et al (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442(7100):295–298PubMedCrossRefPubMedCentralGoogle Scholar
  2. Anderson SN et al (2018) Subtle perturbations of the maize methylome reveal genes and transposons silenced by chromomethylase or RNA-directed DNA methylation pathwaysGoogle Scholar
  3. Barber WT et al (2012) Repeat associated small RNAs vary among parents and following hybridization in maize. Proc Natl Acad Sci USA 109(26):10444–10449PubMedCrossRefPubMedCentralGoogle Scholar
  4. Baucom RS et al (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5(11):e1000732PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bauer MJ, Fischer RL (2011) Genome demethylation and imprinting in the endosperm. Curr Opin Plant Biol 14(2):162–167PubMedPubMedCentralCrossRefGoogle Scholar
  6. Becker C et al (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480(7376):245–249PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bewick AJ et al (2016) On the origin and evolutionary consequences of gene body DNA methylation. Proc Natl Acad Sci USA 113(32):9111–9116PubMedCrossRefPubMedCentralGoogle Scholar
  8. Brink RA (1956) A genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41(6):872–889PubMedPubMedCentralGoogle Scholar
  9. Chandler VL (2007) Paramutation: from maize to mice. Cell 128(4):641–645PubMedCrossRefPubMedCentralGoogle Scholar
  10. Coe EH (1959) A regular and continuing conversion-type phenomenon at the B locus in maize. Proc Natl Acad Sci USA 45(6):828–832PubMedCrossRefPubMedCentralGoogle Scholar
  11. Coe EH (2001) The origins of maize genetics. Nat Rev Genet 2(11):898–905PubMedCrossRefPubMedCentralGoogle Scholar
  12. Crisp PA et al (2016) Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2(2):e1501340PubMedPubMedCentralCrossRefGoogle Scholar
  13. Du J et al (2014) Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol Cell 55(3):495–504PubMedPubMedCentralCrossRefGoogle Scholar
  14. Du J et al (2015) DNA methylation pathways and their crosstalk with histone methylation. 33(4):395–401Google Scholar
  15. Du J et al (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151(1):167–180PubMedPubMedCentralCrossRefGoogle Scholar
  16. Eggleston WB, Alleman M, Kermicle JL (1995) Molecular organization and germinal instability of R-stippled maize. Genetics 141(1):347–360PubMedPubMedCentralGoogle Scholar
  17. Eichten SR et al (2011) Heritable epigenetic variation among maize inbreds. PLoS Genet 7(11)PubMedPubMedCentralCrossRefGoogle Scholar
  18. Eichten SR et al (2013) Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25(8):2783–2797PubMedPubMedCentralCrossRefGoogle Scholar
  19. Eichten SR et al (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8(12)PubMedPubMedCentralCrossRefGoogle Scholar
  20. Eichten SR, Springer NM (2015) Minimal evidence for consistent changes in maize DNA methylation patterns following environmental stress. Front Plant Sci 6:308PubMedPubMedCentralCrossRefGoogle Scholar
  21. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330(6004):622–627PubMedPubMedCentralCrossRefGoogle Scholar
  22. Forestan C, Farinati S, Aiese Cigliano R, Lunardon A, Sanseverino W, Varotto S (2017) Maize RNA PolIV affects the expression of genes with nearby TE insertions and has a genome-wide repressive impact on transcription. BMC Plant Biol 17:161PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gehring M (2013) Genomic imprinting: insights from plants. Annu Rev Genet 47:187–208PubMedCrossRefPubMedCentralGoogle Scholar
  24. Gehring M, Missirian V, Henikoff S (2011) Genomic analysis of parent-of-origin allelic expression in arabidopsis thaliana seeds. PLoS ONE 6(8):e23687PubMedPubMedCentralCrossRefGoogle Scholar
  25. Gehring M, Bubb KL, Henikoff S (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324(5933):1447–1451PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gent JI et al (2013) CHH islands: De novo DNA methylation in near-gene chromatin regulation in maize. Genome Res 23(4):628–637PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gouil Q, Baulcombe DC (2016) DNA methylation signatures of the plant chromomethyltransferases. PLoS Genet 12(12):e1006526PubMedPubMedCentralCrossRefGoogle Scholar
  28. Greenberg MVC et al (2013) Interplay between active chromatin marks and RNA-directed DNA methylation in arabidopsis thaliana. PLoS Genet 9(11)PubMedPubMedCentralCrossRefGoogle Scholar
  29. Haag JR et al (2014) Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits. 9(1), 378–390Google Scholar
  30. Hale CJ et al (2007) A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize. PLoS Biol 5(10):2156–2165CrossRefGoogle Scholar
  31. Haring M et al (2010) The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation. Plant J Cell Mol Biol 63(3):366–378CrossRefGoogle Scholar
  32. Haun WJ et al (2007) Genomic imprinting, methylation and molecular evolution of maize enhancer of zeste (Mez) homologs. Plant J Cell Mol Biol 49(2):325–337CrossRefGoogle Scholar
  33. Haun WJ, Springer NM (2008) Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J Cell Mol BiolGoogle Scholar
  34. Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157(1):95–109PubMedPubMedCentralCrossRefGoogle Scholar
  35. Henderson IR et al (2010) The De novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in arabidopsis thaliana. PLoS Genet 6(10):1–11CrossRefGoogle Scholar
  36. Hermon P et al (2007) Activation of the imprinted Polycomb Group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64(4):387–395PubMedCrossRefGoogle Scholar
  37. Hollick JB (2017) Paramutation and related phenomena in diverse species. Nat Rev Genet 18(1):5–23PubMedCrossRefGoogle Scholar
  38. Hsieh T-F et al (2009) Genome-wide demethylation of arabidopsis endosperm. Science 324(5933):1451–1454PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jia Y et al (2009) Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet 5(11):e1000737PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jiao Y et al (2017) Improved maize reference genome with single-molecule technologies. Nature 546(7659):524–527PubMedGoogle Scholar
  41. Johannes F et al (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5(6):e1000530PubMedPubMedCentralCrossRefGoogle Scholar
  42. Johnson LM et al (2014) SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507(7490):124–128PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jullien PE et al (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol CB 22(19):1825–1830PubMedCrossRefPubMedCentralGoogle Scholar
  44. Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci USA 90(19):8773–8776PubMedCrossRefPubMedCentralGoogle Scholar
  45. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43(2–3):179–188PubMedCrossRefPubMedCentralGoogle Scholar
  46. Kawakatsu T et al (2016) Unique cell-type-specific patterns of DNA methylation in the root meristem. Nat Plants 2:16058PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kermicle JL (1970) Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66(1):69–85PubMedPubMedCentralGoogle Scholar
  48. Lauria M et al (2004) Extensive maternal DNA hypomethylation in the endosperm of Zea mays. Plant Cell 16(2):510–522PubMedPubMedCentralCrossRefGoogle Scholar
  49. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220PubMedPubMedCentralCrossRefGoogle Scholar
  50. Law JA et al (2013) Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498(7454):385–389PubMedPubMedCentralCrossRefGoogle Scholar
  51. Li Q et al (2014a) Genetic perturbation of the maize methylome. Plant Cell 26(12):4602–4616PubMedPubMedCentralCrossRefGoogle Scholar
  52. Li Q et al (2014b) Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. Genetics 196(3):667–676PubMedCrossRefPubMedCentralGoogle Scholar
  53. Li Q et al (2015a) RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. In: Proceedings of the National Academy of Sciences of the United States of America, p 1514680112Google Scholar
  54. Li Q et al (2015b) Examining the causes and consequences of context-specific differential DNA methylation in maize. Plant Physiol 168(4):1262–1274PubMedPubMedCentralCrossRefGoogle Scholar
  55. Li Q et al (2015c) Post-conversion targeted capture of modified cytosines in mammalian and plant genomes. Nucleic Acids Res 43(12):1–16PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lisch D et al (2002) A mutation that prevents paramutation in maize also reverses mutator transposon methylation and silencing. Proc Natl Acad Sci USA 99(9):6130–6135PubMedCrossRefPubMedCentralGoogle Scholar
  57. Lister R et al (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133(3):523–536PubMedPubMedCentralCrossRefGoogle Scholar
  58. Liu R et al (2015) A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc Natl Acad Sci USA 112(34):10804–10809PubMedCrossRefPubMedCentralGoogle Scholar
  59. Loenen WAM, Raleigh EA (2014) The other face of restriction: modification-dependent enzymes. Nucleic Acids Res 42(1):56–69PubMedCrossRefPubMedCentralGoogle Scholar
  60. Lu Y, Rong T, Cao M (2008) Analysis of DNA methylation in different maize tissues. J Genet Genomics 35(1):41–48PubMedCrossRefPubMedCentralGoogle Scholar
  61. Makarevitch I et al (2013) Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell 25(3):780–793PubMedPubMedCentralCrossRefGoogle Scholar
  62. Makarevitch I et al (2007) Natural variation for alleles under epigenetic control by the maize chromomethylase Zmet2. Genetics 177(2):749–760PubMedPubMedCentralCrossRefGoogle Scholar
  63. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation : an epigenetic pathway of increasing complexityGoogle Scholar
  64. McClintock B (1956) Controlling elements and the gene. Cold Spring Harb Symp Quant Biol 21:197–216PubMedCrossRefPubMedCentralGoogle Scholar
  65. McClintock B (1964) Aspects of gene regulation in maize. Carnegie Inst Wash Year Book 63:592–602Google Scholar
  66. McCue AD et al (2014) ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J 34(1):20–35PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mei W et al (2017) A comprehensive analysis of alternative splicing in paleopolyploid maize. Front Plant Sci 8:1–19Google Scholar
  68. Melquist S, Luff B, Bender J (1999) Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153(1):401–413PubMedPubMedCentralGoogle Scholar
  69. Niederhuth CE et al (2016) Widespread natural variation of DNA methylation within angiosperms. bioRxiv 1–19Google Scholar
  70. Palmer LE (2003) Maize genome sequencing by methylation filtration. Science 302(5653):2115–2117PubMedCrossRefPubMedCentralGoogle Scholar
  71. Panda K, Slotkin RK (2013) Proposed mechanism for the initiation of transposable element silencing by the RDR6-directed DNA methylation pathway. Plant Signal Behav 8(8):8–10CrossRefGoogle Scholar
  72. Papa CM (2001) Maize chromomethylase zea methyltransferase2 is required for CpNpG methylation. Plant Cell Online 13(8):1919–1928CrossRefGoogle Scholar
  73. Park M, Keung AJ, Khalil AS (2016) The epigenome: the next substrate for engineering. Genome Biol 17(1):183–185PubMedPubMedCentralCrossRefGoogle Scholar
  74. Pecinka A, Scheid OM (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol p.pcs 044Google Scholar
  75. Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91(12):5222–5226PubMedCrossRefPubMedCentralGoogle Scholar
  76. Rabinowicz PD et al (2005) Differential methylation of genes and repeats in land plants. Genome Res 15(10):1431–1440PubMedPubMedCentralCrossRefGoogle Scholar
  77. Regulski M et al (2013) The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res 23(10):1651–1662PubMedPubMedCentralCrossRefGoogle Scholar
  78. Reinders J et al (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23(8):939–950PubMedPubMedCentralCrossRefGoogle Scholar
  79. Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7(5):395–401PubMedCrossRefPubMedCentralGoogle Scholar
  80. Schmitz RJ, Ecker JR (2012) Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci 17:149–154PubMedPubMedCentralCrossRefGoogle Scholar
  81. Schmitz RJ et al (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334(6054):369–373PubMedPubMedCentralCrossRefGoogle Scholar
  82. Schnable PS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. 326Google Scholar
  83. Secco D et al (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4.  https://doi.org/10.7554/elife.09343
  84. Selinger DA, Chandler VL (2001) B-Bolivia, an allele of the maize b1 gene with variable expression, contains a high copy retrotransposon-related sequence immediately upstream. Plant Physiol 125(3):1363–1379PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sidorenko LV, Peterson T (2001) Transgene-induced silencing identifies sequences involved in the establishment of paramutation of the maize p1 gene. Plant Cell 13(2):319–335PubMedPubMedCentralCrossRefGoogle Scholar
  86. Smith AM, Hansey CN, Kaeppler SM (2012) TCUP: a novel hAT transposon active in maize tissue culture. Front Plant Sci 3:6PubMedPubMedCentralCrossRefGoogle Scholar
  87. Springer NM, Schmitz RJ (2017) Exploiting induced and natural epigenetic variation for crop improvement. Nat Rev Genet. In pressGoogle Scholar
  88. Stam M (2009) Paramutation: a heritable change in gene expression by allelic interactions in trans. Mol Plant 2(4):578–588PubMedCrossRefPubMedCentralGoogle Scholar
  89. Stelpflug SC et al (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198(1):209–218PubMedPubMedCentralCrossRefGoogle Scholar
  90. Stonaker JL et al (2009) Diversity of Pol IV function is defined by mutations at the maize rmr7 locus. PLoS Genet 5(11)PubMedPubMedCentralCrossRefGoogle Scholar
  91. Stroud H et al (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21(1):64–72PubMedCrossRefPubMedCentralGoogle Scholar
  92. Stroud H et al (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152(1–2):352–364PubMedPubMedCentralCrossRefGoogle Scholar
  93. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815CrossRefGoogle Scholar
  94. To TK, Saze H, Kakutani T (2015) DNA methylation within transcribed regions. Plant Physiol 4(1):00543Google Scholar
  95. Underwood CJ, Henderson IR, Martienssen RA (2017) Genetic and epigenetic variation of transposable elements in Arabidopsis. Curr Opin Plant Biol 36:135–141PubMedPubMedCentralCrossRefGoogle Scholar
  96. van der Graaf A et al (2015) Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc Natl Acad Sci USA 112(21):6676–6681PubMedCrossRefPubMedCentralGoogle Scholar
  97. Walker EL (1998) Paramutation of the r1 locus of maize is associated with increased cytosine methylation. Genetics 148(4):1973–1981PubMedPubMedCentralGoogle Scholar
  98. Wang P et al (2015) Genome-wide high-resolution mapping of DNA methylation identifies epigenetic variation across embryo and endosperm in Maize (Zea may). BMC Genom 16:21CrossRefGoogle Scholar
  99. Waters AJ et al (2011) Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23(12):4221–4233PubMedPubMedCentralCrossRefGoogle Scholar
  100. West PT et al (2014) Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS ONE 9(8):1–10CrossRefGoogle Scholar
  101. Wolff P et al (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet 7(6):e1002126PubMedPubMedCentralCrossRefGoogle Scholar
  102. Woo HR, Dittmer TA, Richards EJ (2008) Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in arabidopsis. PLoS Genet 4(8)PubMedPubMedCentralCrossRefGoogle Scholar
  103. Woodhouse MR, Freeling M, Lisch D (2006a) Initiation, establishment, and maintenance of heritable MuDR transposon silencing in maize are mediated by distinct factors. PLoS Biol 4(10):e339PubMedPubMedCentralCrossRefGoogle Scholar
  104. Woodhouse MR, Freeling M, Lisch D (2006b) The mop1 (mediator of paramutation1) mutant progressively reactivates one of the two genes encoded by the MuDR transposon in maize. Genetics 172(1):579–592PubMedPubMedCentralCrossRefGoogle Scholar
  105. Zemach A et al (2013) The arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153(1):193–205PubMedPubMedCentralCrossRefGoogle Scholar
  106. Zemach A et al (2010) Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA 107(43):18729–18734PubMedCrossRefPubMedCentralGoogle Scholar
  107. Zhang H, Zhu JK (2012) Active DNA demethylation in plants and animals. Cold Spring Harb Symp Quant Biol 77:161–173PubMedPubMedCentralCrossRefGoogle Scholar
  108. Zhang M et al (2014) Genome-wide high resolution parental-specific DNA and histone methylation maps uncover patterns of imprinting regulation in maize. Genome Res 24(1):167–176PubMedPubMedCentralCrossRefGoogle Scholar
  109. Zhang M et al (2011) Tissue-specific differences in cytosine methylation and their association with differential gene expression in sorghum. Plant Physiol 156(4):1955–1966PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zilberman D et al (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39(1):61–69PubMedCrossRefPubMedCentralGoogle Scholar
  111. Zong W et al (2013) Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol Biol 81(1–2):175–188PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Jaclyn M. Noshay
    • 1
  • Peter A. Crisp
    • 1
  • Nathan M. Springer
    • 1
    Email author
  1. 1.Department of Plant and Microbial BiologyUniversity of MinnesotaSaint PaulUSA

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