Epigenomics pp 119-147 | Cite as

Epigenetic Phenomena and Epigenomics in Maize

  • Jay B. Hollick
  • Nathan Springer


Maize research has provided much of the initial documentation and characterization of epigenetic phenomena such as transposable element inactivation, paramutation and imprinting. Current efforts are beginning to yield an understanding of the molecular mechanisms responsible for these epigenetic behaviors. Complementary research in many organisms has now provided strong evidence for the role of repetitive DNA features in facilitating epigenetic control of genome functions. The repetitive and complex structure of the maize genome together with the high level of structural diversity between maize haplotypes suggests that maize research has a significant role to play in understanding the dynamic relationships between genome structure and function.


Paramutation Imprinting Transposons Maize Epigenomics 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alleman M, Doctor J (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43: 147–161PubMedCrossRefGoogle Scholar
  2. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE, White J, Sikkink K, Chandler VL (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442: 295–298PubMedCrossRefGoogle Scholar
  3. Banks J, Masson P, Fedoroff N (1988) Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev 2: 1364–1380PubMedCrossRefGoogle Scholar
  4. Barkan A, Martienssen R (1991) Inactivation of maize transposon mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of mu1. Proc Natl Acad Sci U S A 88: 3502–3506PubMedCrossRefGoogle Scholar
  5. Baroux C, Pecinka A, Fuchs J, Schubert I, Grossniklaus U (2007) The triploid endosperm genome of Arabidopsis adopts a peculiar, parental-dosage-dependent chromatin organization. Plant Cell 19: 1782–1794PubMedCrossRefGoogle Scholar
  6. Beckmann JS, Estivill X, Antonarakis SE (2007) Copy number variants and genetic traits: closer to the resolution of phenotypic to genotypic variability. Nat Rev Genet 8: 639–646PubMedCrossRefGoogle Scholar
  7. Bennetzen JL, Schrick K, Springer PS, Brown WE, SanMiguel P (1994) Active maize genes are unmodified and flanked by diverse classes of modified, highly repetitive DNA. Genome 37: 565–576PubMedCrossRefGoogle Scholar
  8. Bennetzen J (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15: 621–627PubMedCrossRefGoogle Scholar
  9. Bercury SD, Panavas T, Irenze K, Walker EL (2001) Molecular analysis of the Doppia transposable element of maize. Plant Mol Biol 47: 341–351PubMedCrossRefGoogle Scholar
  10. Birchler J, Veitia R (2007) The gene balance hypothesis: From classical genetics to modern genomics. Plant Cell 19: 395–402PubMedCrossRefGoogle Scholar
  11. Bortiri E, Jackson D, Hake S (2006) Advances in maize genomics: the emergence of positional cloning. Curr Opin Plant Biol 9: 164–171PubMedCrossRefGoogle Scholar
  12. Brink RA (1973) Paramutation. Annu Rev Genet 7: 129–152PubMedCrossRefGoogle Scholar
  13. Brink RA (1958) Paramutation at the R locus in maize. Cold Spring Harb Symp Quant Biol 23: 379–391PubMedGoogle Scholar
  14. Brink RA (1956) A Genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41: 872–889PubMedGoogle Scholar
  15. Brown DF (1966) Paramutability of R and r mutant genes derived from an R Allele in maize. Genetics 54: 899–910PubMedGoogle Scholar
  16. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005a) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343–360CrossRefGoogle Scholar
  17. Brunner S, Pea G, Rafalski A (2005b) Origins, genetic organization and transcription of a family of non-autonomous helitron elements in maize. Plant J 43: 799–810CrossRefGoogle Scholar
  18. Buckler E, Gaut B, McMullen M (2006) Molecular and functional diversity of maize. Curr Opin Plant Biol 9: 172–176PubMedCrossRefGoogle Scholar
  19. Buhler M, Haas W, Gygi SP, Moazed D (2007) RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129: 707–721PubMedCrossRefGoogle Scholar
  20. Bureau T, White S, Wessler S (1994) Transduction of a cellular gene by a plant retroelement. Cell 77: 479–480PubMedCrossRefGoogle Scholar
  21. Casa AM, Brouwer C, Nagel A, Wang L, Zhang Q, Kresovich S, Wessler SR (2000) Inaugural article: the MITE family heartbreaker (Hbr): molecular markers in maize. Proc Natl Acad Sci U S A 97: 10083–10089PubMedCrossRefGoogle Scholar
  22. Cavalli G, Paro R (1998) Chromo-domain proteins: linking chromatin structure to epigenetic regulation. Curr Opin Cell Biol 10: 354–360PubMedCrossRefGoogle Scholar
  23. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303: 1336PubMedCrossRefGoogle Scholar
  24. Chandler VL, Stam M (2004) Chromatin conversations: mechanisms and implications of paramutation. Nat Rev Genet 5: 532–54PubMedCrossRefGoogle Scholar
  25. Chandler VL, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A 83: 1767–1771PubMedCrossRefGoogle Scholar
  26. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110: 33–42PubMedCrossRefGoogle Scholar
  27. Chomet P, Lisch D, Hardeman KJ, Chandler VL, Freeling M (1991) Identification of a regulatory transposon that controls the Mutator transposable element system in maize. Genetics 129:261–270PubMedGoogle Scholar
  28. Chomet PS, Wessler S, Dellaporta SL (1987) Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J 6: 295–302PubMedGoogle Scholar
  29. Cocciolone SM, Cone KC (1993) Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics 135: 575–588PubMedGoogle Scholar
  30. Cocciolone SM, Sidorenko LV, Chopra S, Dixon PM, Peterson T (2000) Hierarchical patterns of transgene expression indicate involvement of developmental mechanisms in the regulation of the maize P1-rr promoter. Genetics 156: 839–846PubMedGoogle Scholar
  31. Coe EH (1966) The properties, origin, and mechanism of conversion-type inheritance at the B locus in maize. Genetics 53: 1035–1063PubMedGoogle Scholar
  32. Danilevskaya ON, Hermon P, Hantke S, Muszynski MG, Kollipara K, Ananiev EV (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15: 425–438PubMedCrossRefGoogle Scholar
  33. Das OP, Messing J (1994) Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. Genetics 136: 1121–1141PubMedGoogle Scholar
  34. Dilkes BP, Comai L (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell 16: 3174–3180PubMedCrossRefGoogle Scholar
  35. Ding Y, Wang X, Su L, Zhai J, Cao S, Zhang D, Liu C, Bi Y, Qian Q, Cheng Z, Chu C, Cao X (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19: 9–22PubMedCrossRefGoogle Scholar
  36. Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25: 173–199PubMedCrossRefGoogle Scholar
  37. Dorweiler JE, Carey CC, Kubo KM, Hollick JB, Kermicle JL, Chandler VL (2000) Mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12: 2101–2118PubMedCrossRefGoogle Scholar
  38. Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166–1176PubMedCrossRefGoogle Scholar
  39. Eggleston WB, Alleman M, Kermicle JL (1995) Molecular organization and germinal instability of R-stippled maize. Genetics 141: 347–360PubMedGoogle Scholar
  40. Fedoroff N, Botstien D (1992) The dynamic genome. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  41. Fedoroff N (1989) The heritable activation of cryptic Suppressor-mutator elements by an active element. Genetics 121: 591–608PubMedGoogle Scholar
  42. Fedoroff NV (1999) Transposable elements as a molecular evolutionary force. Ann N Y Acad Sci 870: 251–264PubMedCrossRefGoogle Scholar
  43. Flaus A, Martin DM, Barton GJ, Owen-Hughes T (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34: 2887–2905PubMedCrossRefGoogle Scholar
  44. Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44: 1054–1064PubMedCrossRefGoogle Scholar
  45. Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci U S A 99: 9573–9578PubMedGoogle Scholar
  46. Fu H, Park W, Yan X, Zheng Z, Shen B, Dooner HK (2001) The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc Natl Acad Sci U S A 98: 8903–8908PubMedCrossRefGoogle Scholar
  47. Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB, Fischer RL (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495–506PubMedCrossRefGoogle Scholar
  48. Gierl A, Lutticke S, Saedler H (1988) TnpA product encoded by the transposable element En-1 of Zea mays is a DNA binding protein. EMBO J 7: 4045–4053PubMedGoogle Scholar
  49. Grandbastien MA (2004) Stress activation and genomic impact of plant retrotransposons. J Soc Biol 198: 425–432PubMedGoogle Scholar
  50. Gross SM, Hollick JB (2007) Multiple trans-sensing interactions affect meiotically heritable epigenetic states at the maize pl1 locus. Genetics 176: 829–839PubMedCrossRefGoogle Scholar
  51. Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16: 1707–1716PubMedCrossRefGoogle Scholar
  52. Gustafsson MGL, Shao L, Carlton PM, Wang CJR, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW. (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94(12) 4957–4970CrossRefGoogle Scholar
  53. Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E, Perez P, Dickinson HG (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38: 876–878PubMedCrossRefGoogle Scholar
  54. Gutierrez-Marcos JF, Pennington PD, Costa LM, Dickinson HG (2003) Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos Trans R Soc Lond B Biol Sci 358: 1105–1111PubMedCrossRefGoogle Scholar
  55. Haberer G, Young S, Bharti AK, Gundlach H, Raymond C, Fuks G, Butler E, Wing RA, Rounsley S, Birren B, Nusbaum C, Mayer KF, Messing J (2005) Structure and architecture of the maize genome. Plant Physiol 139: 1612–1624PubMedCrossRefGoogle Scholar
  56. Haig D, Westoby M (1989) Parent-specific gene-expression and the triploid endosperm. Am Nat 134: 147–155CrossRefGoogle Scholar
  57. Hale CJ, Stonaker JL, Gross SM, Hollick JB (2007) A novel Snf2 protein maintains trans-generational regulatory states established by paramutation in maize. PLoS Biol 5: 2156–2165CrossRefGoogle Scholar
  58. Haun WJ, Laoueille-Duprat S, O’connell MJ, Spillane C, Grossniklaus U, Phillips AR, Kaeppler SM, Springer NM (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J 49: 325–337PubMedCrossRefGoogle Scholar
  59. Hermon P, Srilunchang KO, Zou J, Dresselhaus T, Danilevskaya ON (2007) Activation of the imprinted Polycomb Group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64: 387–395PubMedCrossRefGoogle Scholar
  60. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12: 2521–2528PubMedGoogle Scholar
  61. Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12: 357–369PubMedCrossRefGoogle Scholar
  62. Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A 93: 7783–7788PubMedCrossRefGoogle Scholar
  63. Hollick JB, Chandler VL (2001) Genetic factors required to maintain repression of a paramutagenic maize pl1 allele. Genetics 157: 369–378PubMedGoogle Scholar
  64. Hollick JB, Chandler VL (1998) Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action. Genetics 150: 891–897PubMedGoogle Scholar
  65. Hollick JB, Kermicle JL, Parkinson SE (2005) Rmr6 maintains meiotic inheritance of paramutant states in Zea mays. Genetics 171: 725–740PubMedCrossRefGoogle Scholar
  66. Hollick JB, Patterson GI, Asmundsson IM, Chandler VL (2000) Paramutation alters regulatory control of the maize pl1 locus. Genetics 154: 1827–1838PubMedGoogle Scholar
  67. Hollick JB, Patterson GI, Coe EH,Jr, Cone KC, Chandler VL (1995) Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics 141: 709–719PubMedGoogle Scholar
  68. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJM, Matzke M (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. ENBO J. 25: 2828–2836Google Scholar
  69. Huettel B, Kanno T, Daxinger L, Bucher E, van der Winden J, Matzke AJ, Matzke M (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim Biophys Acta 1769: 358–374PubMedGoogle Scholar
  70. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431: 569–573PubMedCrossRefGoogle Scholar
  71. Jin YK, Bennetzen JL (1994) Integration and nonrandom mutation of a plasma membrane proton ATPase gene fragment within the Bs1 retroelement of maize. Plant Cell 6: 1177–1186PubMedCrossRefGoogle Scholar
  72. Jullien PE, Kinoshita T, Ohad N, Berger F (2006) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18: 1360–1372PubMedCrossRefGoogle Scholar
  73. Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci U S A 90: 8773–8776PubMedCrossRefGoogle Scholar
  74. Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ (2005) A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep 6: 649–655PubMedCrossRefGoogle Scholar
  75. Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJ (2004) Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14: 801–805PubMedCrossRefGoogle Scholar
  76. Kapitonov VV, Jurka J (2001) Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A 98: 8714–8719PubMedCrossRefGoogle Scholar
  77. Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5: e57PubMedCrossRefGoogle Scholar
  78. Kato A, Lamb JC, Birchler JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci U S A 101: 13554–13559PubMedCrossRefGoogle Scholar
  79. Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13: 421–426PubMedCrossRefGoogle Scholar
  80. Kermicle JL (1996) Epigenetic silencing and activation of a maize r gene. In VEA Russo, RA Martienssen, AD Riggs, eds, Epigenetic mechanisms of gene regulation. Cold Spring Harbor Laboratory Press, New York, pp 267–287Google Scholar
  81. Kermicle JL (1978) Imprinting of gene action in maize endosperm. Maize breeding and genetics. Wiley, New York, pp 357–371Google Scholar
  82. Kermicle JL (1970) Dependence of the R-mottled aleurone phenotype in maize on mode of sexual transmission. Genetics 66: 69–85PubMedGoogle Scholar
  83. Kermicle JL, Alleman M (1990) Gametic imprinting in maize in relation to the angiosperm life cycle. Dev Suppl 9–14Google Scholar
  84. Kermicle JL, Eggleston WB, Alleman M (1995) Organization of paramutagenicity in R-stippled maize. Genetics 141: 361–372PubMedGoogle Scholar
  85. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521–523PubMedCrossRefGoogle Scholar
  86. Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, Kakutani T (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49: 38–45PubMedCrossRefGoogle Scholar
  87. Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38: 233–271PubMedCrossRefGoogle Scholar
  88. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33: 479–532PubMedCrossRefGoogle Scholar
  89. Kunze R, Starlinger P, Schwartz D (1988) DNA methylation of the maize transposable element Ac interferes with its transcription. Mol Gen Genet 214: 325–327CrossRefGoogle Scholar
  90. Lai J, Li Y, Messing J, Dooner HK (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci U S A 102: 9068–9073PubMedCrossRefGoogle Scholar
  91. Lamb JC, Meyer JM, Corcoran B, Kato A, Han F, Birchler JA (2007) Distinct chromosomal distributions of highly repetitive sequences in maize. Chromosome Res 15: 33–49PubMedCrossRefGoogle Scholar
  92. Lauria M, Rupe M, Guo M, Kranz E, Pirona R, Viotti A, Lund G (2004) Extensive maternal DNA hypomethylation in the endosperm of Zea mays. Plant Cell 16: 510–522PubMedCrossRefGoogle Scholar
  93. Laurie DA, Bennett MD (1985) Nuclear DNA content in the genera Zea and Sorghum. Intergeneric, interspecific and intraspecific variation. Heredity 55: 307–313CrossRefGoogle Scholar
  94. Lee EA, Ahmadzadeh A, Tollenaar M (2005) Quantitative genetic analysis of the physiological processes underlying maize grain yield. Crop Sci 45: 981–987CrossRefGoogle Scholar
  95. Lin BY (1984) Ploidy barrier to endosperm development in maize. Genetics 107: 103–115PubMedGoogle Scholar
  96. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077–2080PubMedCrossRefGoogle Scholar
  97. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476PubMedCrossRefGoogle Scholar
  98. Lippman Z, May B, Yordan C, Singer T, Martienssen R (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1: E67PubMedCrossRefGoogle Scholar
  99. Lisch D, Carey CC, Dorweiler JE, Chandler VL (2002) A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc Natl Acad Sci U S A 99: 6130–6135PubMedCrossRefGoogle Scholar
  100. Liu R, Vitte C, Ma J, Mahama AA, Dhliwayo T, Lee M, Bennetzen JL (2007) A GeneTrek analysis of the maize genome. Proc Natl Acad Sci U S A 104: 11844–11849PubMedCrossRefGoogle Scholar
  101. Makarevitch I, Stupar RM, Iniguez AL, Haun WJ, Barbazuk WB, Kaeppler SM, Springer NM (2007) Natural variation for alleles under epigenetic control by the maize chromomethylase Zmet2. Genetics 177: 749–760PubMedCrossRefGoogle Scholar
  102. Martienssen R (1996) Epigenetic phenomena: paramutation and gene silencing in plants. Curr Biol 6: 810–813PubMedCrossRefGoogle Scholar
  103. Martienssen R, Baron A (1994) Coordinate suppression of mutations caused by Robertson’s mutator transposons in maize. Genetics 136: 1157–1170PubMedGoogle Scholar
  104. Masson P, Surosky R, Kingsbury JA, Fedoroff NV (1987) Genetic and molecular analysis of the Spm-dependent a-m2 alleles of the maize a locus. Genetics 117: 117–137PubMedGoogle Scholar
  105. McClintock B (1964) Aspects of gene regulation in maize. Carnegie Inst Wash Year Book 63: 592–602Google Scholar
  106. McClintock B, Kato A, Blumenschein A (1981) Chromosome constitution of races of maize. Its significance in the interpretation of relationships between races and varieties in the Americas. Colegio de Postgraduados, MexicoGoogle Scholar
  107. McClintock B (1984) The significance of responses of the genome to challenge. Science 226: 792–801PubMedCrossRefGoogle Scholar
  108. McClintock B (1951) Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol 16: 13–47PubMedGoogle Scholar
  109. McGinnis KM, Springer C, Lin Y, Carey CC, Chandler V (2006) Transcriptionally silenced transgenes in maize are activated by three mutations defective in paramutation. Genetics 173: 1637–1647PubMedCrossRefGoogle Scholar
  110. McGinnis K, Murphy N, Carlson AR, Akula A, Akula C, Basinger H, Carlson M, Hermanson P, Kovacevic N, McGill MA, Seshadri V, Yoyokie J, Cone K, Kaeppler HF, Kaeppler SM, Springer NM (2007) Assessing the Efficiency of RNA Interference for Maize Functional Genomics. Plant Physiol 143: 1441–1451PubMedCrossRefGoogle Scholar
  111. Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, Wing RA (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci U S A 101: 14349–14354PubMedCrossRefGoogle Scholar
  112. Messing J, Dooner H (2006) Organization and variability of the maize genome. Curr Opin Plant Biol 9: 157–163PubMedCrossRefGoogle Scholar
  113. Meyers B, Tingey S, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11: 1660–1676PubMedCrossRefGoogle Scholar
  114. Mikula BC (1995) Environmental programming of heritable epigenetic changes in paramutant r-gene expression using temperature and light at a specific stage of early development in maize seedlings. Genetics 140: 1379–1387PubMedGoogle Scholar
  115. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212–214PubMedCrossRefGoogle Scholar
  116. Moose SP, Dudley JW, Rocheford TR (2004) Maize selection passes the century mark: a unique resource for 21st century genomics. Trends Plant Sci 9: 358–364PubMedCrossRefGoogle Scholar
  117. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23: 314–318PubMedCrossRefGoogle Scholar
  118. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37: 997–1002PubMedCrossRefGoogle Scholar
  119. Nakayama J, Klar AJ, Grewal SI (2000) A chromodomain protein, Swi6, performs imprinting functions in fission yeast during mitosis and meiosis. Cell 101: 307–317PubMedCrossRefGoogle Scholar
  120. Ohtsu K, Smith MB, Emrich SJ, Borsuk LA, Zhou R, Chen T, Zhang X, Timmermans MC, Beck J, Buckner B, Janick-Buckner D, Nettleton D, Scanlon MJ, Schnable PS (2007) Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J 52: 391–404PubMedCrossRefGoogle Scholar
  121. Panavas T, Weir J, Walker EL (1999) The structure and paramutagenicity of the R-marbled haplotype of Zea mays. Genetics 153: 979–991PubMedGoogle Scholar
  122. Parkinson SE, Gross SM, Hollick JB (2007) Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states. Dev Biol 308: 462–473PubMedCrossRefGoogle Scholar
  123. Patterson GI, Thorpe CJ, Chandler VL (1993) Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135: 881–894PubMedGoogle Scholar
  124. Philips RL (1999) Research needs in heterosis. The genetics and exploitation of heterosis in crops. Crop Science Society of America, Madison, WI, pp 501–508Google Scholar
  125. Pooma W, Gersos C, Grotewold E (2002) Transposon insertions in the promoter of the Zea mays a1 gene differentially affect transcription by the Myb factors P and C1. Genetics 161: 793–801PubMedGoogle Scholar
  126. Pouteau S, Spielmann A, Meyer C, Grandbastien MA, Caboche M (1991) Effects of Tnt1 tobacco retrotransposon insertion on target gene transcription. Mol Gen Genet 228: 233–239PubMedCrossRefGoogle Scholar
  127. Rabinowicz PD, Schutz K, Dedhia N, Yordan C, Parnell LD, Stein L, McCombie WR, Martienssen RA (1999) Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome. Nat Genet 23: 305–308PubMedCrossRefGoogle Scholar
  128. Rangwala SH, Richards EJ (2007) Differential epigenetic regulation within an Arabidopsis retroposon family. Genetics 176: 151–160PubMedCrossRefGoogle Scholar
  129. Rasmusson DC, Phillips RL (1997) Plant breeding progress and genetic diversity from de novo variation and elevated epistasis. Crop Sci 37: 303–310CrossRefGoogle Scholar
  130. Rhoades MM (1978) Genetic effects of heterochromatin in maize. Maize breeding and genetics., Ed Walden, J.B. John Wiley and Sons, Toronto, pp 641–671Google Scholar
  131. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20: 43–45PubMedCrossRefGoogle Scholar
  132. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768PubMedCrossRefGoogle Scholar
  133. Saze H, Kakutani T (2007) Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J 26: 3641–3652PubMedCrossRefGoogle Scholar
  134. Schwartz D, Dennis E (1986) Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol Gen Genet 205: 476–482CrossRefGoogle Scholar
  135. Schwarz-Sommer Z, Shepherd N, Tacke E, Gierl A, Rohde W, Leclercq L, Mattes M, Berndtgen R, Peterson PA, Saedler H (1987) Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J 6: 287–294PubMedGoogle Scholar
  136. Sidorenko LV, Peterson T (2001) Transgene-induced silencing identifies sequences involved in the establishment of paramutation of the maize p1 gene. Plant Cell 13: 319–335PubMedCrossRefGoogle Scholar
  137. Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37: 641–644PubMedCrossRefGoogle Scholar
  138. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272–285PubMedCrossRefGoogle Scholar
  139. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19: 1507–1521PubMedCrossRefGoogle Scholar
  140. Sprague GF, Russell WA, Penny LH (1960) Mutations affecting quantitative traits in the selfed progeny of doubled monoploid maize stocks. Genetics 45: 855–866PubMedGoogle Scholar
  141. Springer NM, Gutierrez-Marcos J (2008) Imprinting in maize. The maize handbook. Springer, New YorkGoogle Scholar
  142. Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17: 264–275PubMedCrossRefGoogle Scholar
  143. Stam M, Belele C, Dorweiler JE, Chandler VL (2002a) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16: 1906–1918CrossRefGoogle Scholar
  144. Stam M, Belele C, Ramakrishna W, Dorweiler JE, Bennetzen JL, Chandler VL (2002b) The regulatory regions required for B’paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 162: 917–930Google Scholar
  145. Stupar RM, Hermanson PJ, Springer NM (2007) Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol 145: 411–425PubMedCrossRefGoogle Scholar
  146. Styles ED, Brink RA (1969) The metastable nature of paramutable R alleles in maize. IV. Parallel enhancement of R action in heterozygotes with r and in hemizygotes. Genetics 61: 801–811PubMedGoogle Scholar
  147. Styles ED, Brink RA (1966) The metastable nature of paramutable R alleles in maize. I. Heritable enhancement in level of standard R action. Genetics 54: 433–439PubMedGoogle Scholar
  148. Tompa R, McCallum CM, Delrow J, Henikoff JG, van Steensel B, Henikoff S (2002) Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr Biol 12: 65–68PubMedCrossRefGoogle Scholar
  149. Turcich M, Bokhari-Riza A, Hamilton, He C, Messier W, Stewart C (1996) PREM-2, a copia-type retroelement in maize is expressed preferentially in early microspores. Sex Plant Reprod 9: 65–74CrossRefGoogle Scholar
  150. Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125: 1283–1292PubMedCrossRefGoogle Scholar
  151. Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci U S A 103: 17638–17643PubMedCrossRefGoogle Scholar
  152. Walbot V (2001) Imprinting of R-r, paramutation of B-I and Pl, and epigenetic silencing of MuDR/Mu transposons in Zea mays L. are coordinately affected by inbred background. Genet Res 77: 219–226PubMedCrossRefGoogle Scholar
  153. Walker EL (1998) Paramutation of the r1 locus of maize is associated with increased cytosine methylation. Genetics 148: 1973–1981PubMedGoogle Scholar
  154. Walker EL, Robbins TP, Bureau TE, Kermicle J, Dellaporta SL (1995) Transposon-mediated chromosomal rearrangements and gene duplications in the formation of the maize R-r complex. EMBO J 14: 2350–2363PubMedGoogle Scholar
  155. Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci U S A 103: 17644–17649PubMedCrossRefGoogle Scholar
  156. Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, Fuks G, Sanchez-Villeda H, Schroeder S, Fang Z, McMullen M, Davis G, Bowers JE, Paterson AH, Schaeffer M, Gardiner J, Cone K, Messing J, Soderlund C, Wing RA (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3: e123PubMedCrossRefGoogle Scholar
  157. Weiler KS, Wakimoto BT (1995) Heterochromatin and gene expression in Drosophila. Annu Rev Genet 29: 577–605PubMedCrossRefGoogle Scholar
  158. Wessler SR (1996) Turned on by stress. Plant retrotransposons. Curr Biol 6: 959–961PubMedCrossRefGoogle Scholar
  159. Whitelaw E, Martin DI (2001) Retrotransposons as epigenetic mediators of phenotypic variation in mammals. Nat Genet 27: 361–365PubMedCrossRefGoogle Scholar
  160. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973–982PubMedCrossRefGoogle Scholar
  161. 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 : e339Google Scholar
  162. 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: 579–592CrossRefGoogle Scholar
  163. Xiao W, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, Goldberg RB, Pennell RI, Fischer RL (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5: 891–901PubMedCrossRefGoogle Scholar
  164. Yi H, Richards EJ (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19: 2929–2939PubMedCrossRefGoogle Scholar
  165. Zhao W, Canaran P, Jurkuta R, Fulton T, Glaubitz J, Buckler E, Doebley J, Gaut B, Goodman M, Holland J, Kresovich S, McMullen M, Stein L, Ware D (2006) Panzea: a database and resource for molecular and functional diversity in the maize genome. Nucleic Acids Res 34: D752–7PubMedCrossRefGoogle Scholar
  166. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716–719PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Jay B. Hollick
    • 1
  • Nathan Springer
    • 2
  1. 1.Department of Plant and Microbial BiologyUniversity of CaliforniaUSA 94720-3102
  2. 2.Department of Plant Biology, 250 Biosciences centerUniversity of MinnesotaSaint Paul

Personalised recommendations