Progressive loss of DNA methylation releases epigenetic gene silencing from a tandemly repeated maize Myb gene

Genetics

Volumn 181, Issue 1, 2009, Pages 81-91

  Sekhon, Rajandeep S ^a,b   Chopra, Surinder ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c 116 Agricultural Sciences and Industries Bldg ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PIGMENT; FLAVONOID; PHLOBAPHENE; PROTEIN C MYB; TRANSCRIPTION FACTOR; UFO1 PROTEIN, MAIZE;

ARTICLE; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; MAIZE; MYB GENE; PLANT DEVELOPMENT; PLANT GENE; PRIORITY JOURNAL; TANDEM REPEAT; UFO 1 GENE; ALLELE; BIOSYNTHESIS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; METABOLISM; MITOSIS; MOSAICISM; NUCLEOTIDE SEQUENCE; PENETRANCE; PHENOTYPE; PIGMENTATION; UPREGULATION;

ZEA MAYS;

ALLELES; BASE SEQUENCE; DNA METHYLATION; FLAVONOIDS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; INHERITANCE PATTERNS; MITOSIS; MOSAICISM; PENETRANCE; PHENOTYPE; PIGMENTATION; PROTO-ONCOGENE PROTEINS C-MYB; TANDEM REPEAT SEQUENCES; TRANSCRIPTION FACTORS; UP-REGULATION; ZEA MAYS;

EID: 61549127207     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.097170     Document Type: Article

References (62)

1. ALLEMAN, M., L. SIDORENKO, K. MCG INNIS, V. SESHADRI, J. E. DORWEILER et al., 2006 An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442: 295-298.
2. BARLOW, J. J., A. P. MATHIAS, R. WILLIAMSON and D. B. GAMMACK, 1963 A simple method for the quantitative isolation of undegraded high molecular weight ribonucleic acid. Biochem. Biophys. Res. Commun. 13: 61-66.
3. BENDER, J., 2004 Chromatin-based silencing mechanisms. Curr. Opin. Plant Biol. 7: 521-526.
4. BIRD, A., 2002 DNA methylation patterns and epigenetic memory. Genes Dev. 16: 6-21.
5. BODDU, J., C. SVABEK, R. SEKHON, A. GEVENS, R. NICHOLSON et al., 2004 Expression of a putative flavonoid 3′-hydroxylase in sorghum mesocotyls synthesizing 3-deoxyanthocyanidin phytoalexins. Physiol. Mol. Plant Pathol. 65: 101-113.
6. BRINK, R. A., and E. D. STYLES, 1966 A collection of pericarp factors. Maize Genet. Coop. News Lett. 40: 149-160.
7. CAO, X., and S. E. JACOBSEN, 2002 Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc. Natl. Acad. Sci. USA 99(Suppl 4): 16491-16498.
8. CHAN, S. W., I. R. HENDERSON and S. E. JACOBSEN, 2005 Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6: 351-360.
9. CHOPRA, S., P. ATHMA, X. G. LI and T. PETERSON, 1998 A maize Myb homolog is encoded by a multicopy gene complex. Mol. Gen. Genet. 260: 372-380.
10. CHOPRA, S., P. ATHMA and T. PETERSON, 1996 Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements. Plant Cell 8: 1149-1158.
11. CHOPRA, S., S. M. COCCIOLONE, S. BUSHMAN, V. SANGAR, M. D. MCMULLEN et al., 2003 The maize Unstable factor for orange1 is a dominant epigenetic modifier of a tissue specifically silent allele of pericarp color1. Genetics 163: 1135-1146.
12. COCCIOLONE, S. M., S. CHOPRA, S. A. FLINT-GARCIA, M. D. MCMULLEN and T. PETERSON, 2001 Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated. Plant J. 27: 467-478.
13. COE, E. H., M. G. NEUFFER and D. A. HOISINGTO, 1988 The genetics of corn, pp. 81-258 in Corn and Corn Improvement, edited by G. F. SPRAGUE and J. DUDLEY. American Society of Agronomy, Madison, WI.
14. FINNEGAN, E. J., W. J. PEACOCK and E. S. DENNIS, 1996 Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl. Acad. Sci. USA 93: 8449-8454.
15. FOSS, H. M., C. J. ROBERTS, K. M. CLAEYS and E. U. SELKER, 1993 Abnormal chromosome behavior in Neurospora mutants defective in DNA methylation. Science 262: 1737-1741.
16. GEHRING, M., and S. HENIKOFF, 2007 DNA methylation dynamics in plant genomes. Biochim. Biophys. Acta 1769: 276-286.
17. GOLL, M. G., and T. H. BESTOR, 2005 Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74: 481-514.
18. GREENBLATT, I. M., 1985 The pericarp of maize: a major tool to study transposable elements, pp. 405-417 in Plant Genetics, edited by M. FREELING. Alan R. Liss, New York.
19. GROTEWOLD, E., P. ATHMA and T. PETERSON, 1991 Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. Proc. Natl. Acad. Sci. USA 88: 4587-4591.
20. GROTEWOLD, E., M. CHAMBERLIN, M. SNOOK, B. SIAME, L. BUTLER et al., 1998 Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10: 721-740.
21. GROTEWOLD, E., and T. PETERSON, 1994 Isolation and characterization of a maize gene encoding chalcone flavonone isomerase. Mol. Gen. Genet. 242: 1-8.
22. HANSEN, R. S., C. WIJMENGA, P. LUO, A. M. STANEK, T. K. CANFIELD et al., 1999 The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. Proc. Natl. Acad. Sci. USA 96: 14412-14417.
23. HOEKENGA, O. A., M. G. MUSZYNSKI and K. C. CONE, 2000 Developmental patterns of chromatin structure and DNA methylation responsible for epigenetic expression of a maize regulatory gene. Genetics 155: 1889-1902.
24. JACOBSEN, S. E., H. SAKAI, E. J. FINNEGAN, X. CAO and E. M. MEYEROWITZ, 2000 Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr. Biol. 10: 179-186.
25. JEDDELOH, J. A., T. L. STOKES and E. J. RICHARDS, 1999 Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22: 94-97.
26. KAKUTANI, T., 1997 Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana. Plant J. 12: 1447-1451.
27. KATO, M., A. MIURA, J. BENDER, S. E. JACOBSEN and T. KAKUTANI, 2003 Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr. Biol. 13: 421-426.
28. KLOSE, R. J., and A. P. BIRD, 2006 Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31: 89-97.
29. LECHELT, C., T. PETERSON, A. LAIRD, J. CHEN, S. L. DELLAPORTA et al., 1989 Isolation and molecular analysis of the maize P locus. Mol. Gen. Genet. 219: 225-234.
30. LI, E., T. H. BESTOR and R. JAENISCH, 1992 Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915-926.
31. LU, Y., T. RONG and M. CAO, 2008 Analysis of DNA methylation in different maize tissues. J. Genet. Gen. 35: 41-48.
32. MALAGNAC, F., B. WENDEL, C. GOYON, G. FAUGERON, D. ZICKLER et al., 1997 A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91: 281-290.
33. MARTIENSSEN, R., A. BARKAN, W. C. TAYLOR and M. FREELING, 1990 Somatically heritable switches in the DNA modification of Mu transposable elements monitored with a suppressible mutant in maize. Genes Dev. 4: 331-343.
34. MATZKE, M. A., and A. J. MATZKE,1991 Differential inactivation and methylation of a transgene in plants by two suppressor loci containing homologous sequences. Plant Mol. Biol. 16: 821-830.
35. MATZKE, M. A., and A. J. MATZKE, 1998 Epigenetic silencing of plant transgenes as a consequence of diverse cellular defence responses. Cell. Mol. Life Sci. 54: 94-103.
36. MCGOWAN, R., R. CAMPBELL, A. PETERSON and C. SAPIENZA, 1989 Cellular mosaicism in the methylation and expression of hemizygous loci in the mouse. Genes Dev. 3: 1669-1676.
37. MESSING, J., A. K. BHARTI, W. M. KARLOWSKI, H. GUNDLACH, H. R. KIM et al., 2004 Sequence composition and genome organization of maize. Proc. Natl. Acad. Sci. USA 101: 14349-14354.
38. MIURA, A., S. YONEBAYASHI, K. WATANABE, T. TOYAMA, H. SHIMADA et al., 2001 Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212-214.
39. OKANO, M., D. W. BELL, D. A. HABER and E. LI, 1999 DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
40. POETHIG, R. S., 1990 Phase change and the regulation of shoot morphogenesis in plants. Science 250: 923-930.
41. POETHIG, R. S., 2003 Phase change and the regulation of developmental timing in plants. Science 301: 334-336.
42. RICHARDS, E. J., 2006 Inherited epigenetic variation-revisiting soft inheritance. Nat. Rev. Genet. 7: 395-401.
43. ROBBINS, M. L., R. S. SEKHON, R. MEELEY and S. CHOPRA, 2008 A mutator transposon insertion is associated with ectopic expression of a tandemly repeated multicopy Myb gene pericarp color1 of maize. Genetics 178: 1859-1874.
44. RONEMUS, M. J., M. GALBIATI, C. TICKNOR, J. CHEN and S. L. DELLAPORTA, 1996 Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273: 654-657.
45. SAGHAI-MAROOF, M. A., K. M. SOLIMAN, R. A. JORGENSEN and R. W. ALLARD, 1984 Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc. Natl. Acad. Sci. USA 81: 8014-8018.
46. SATO, Y., N. SENTOKU, Y. MIURA, H. HIROCHIKA, H. KITANO et al., 1999 Loss-of-function mutations in the rice homeobox gene OSH15 affect the architecture of internodes resulting in dwarf plants. EMBO J. 18: 992-1002.
47. SCHOB, H., and U. GROSSNIKLAUS, 2006 The first high-resolution DNA "methylome". Cell 126: 1025-1028.
48. SCHWARZ-SOMMER, Z., N. SHEPHERD, E. TACKE, A. GIERL, W. ROHDE et al., 1987 Influence of transposable elements on the structure and function of the A1 gene of Zea mays. EMBO J. 6: 287-294.
49. SEKHON, R. S., T. PETERSON and S. CHOPRA, 2007 Epigenetic modifications of distinct sequences of the p1 regulatory gene specify tissue-specific expression patterns in maize. Genetics 175: 1059-1070.
50. SINGER, T., C. YORDAN and R. A. MARTIENSSEN, 2001 Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 15: 591-602.
51. STYLES, E. D., and O. CESKA,1977 The genetic control of flavonoid synthesis in maize. Can. J. Genet. Cytol. 19: 289-302.
52. STYLES, E. D., and O. CESKA, 1989 Pericarp flavonoids in genetic strains of Zea mays. Maydica 34: 227-237.
53. TARIQ, M., and J. PASZKOWSKI, 2004 DNA and histone methylation in plants. Trends Genet. 20: 244-251.
54. VEGA, S. H., M. SAUER, J. A. ORKWISZEWSKI and R. S. POETHIG, 2002 The early phase change gene in maize. Plant Cell 14: 133-147.
55. VONGS, A., T. KAKUTANI, R. A. MARTIENSSEN and E. J. RICHARDS, 1993 Arabidopsis thaliana DNA methylation mutants. Science 260: 1926-1928.
56. WATERSON, J. J., and G. L. BUTLER, 1983 Occurrence of an unusual leucoanthocyanidin and absence of proanthocyanidins in sorghum leaves. J. Agric. Food Chem. 31: 41-45.
57. WIENAND, U., U. WEYDEMANN, U. NIESBACH- KLOSGEN, P. A. PETERSON and H. SAEDLER, 1986 Molecular cloning of the c2 locus of Zea mays, the gene coding for chalcone syntahse. Mol. Gen. Genet. 203: 202-207.
58. WOODHOUSE, M. R., M. FREELING and D. LISCH, 2006 The mop1 (mediator of paramutation1) mutant progressively reactivates one of the two genes encoded by the MuDR transposon in maize. Genetics 172: 579-592.
59. XU, G. L., T. H. BESTOR, D. BOURC'HIS, C. L. HSIEH, N. TOMMERUP et al., 1999 Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402: 187-191.
60. ZHANG, P., 1999 Molecular characterization of myb-homologous transcription factors of the flavonoid pathway in Zea mays. Ph.D. Thesis, Iowa State University, Ames, IA.
61. ZHANG, X., J. YAZAKI, A. SUNDARESAN, S. COKUS, S. W. CHAN et al., 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
62. ZILBERMAN, D., M. GEHRING, R. K. TRAN, T. BALLINGER and S. HENIKOFF, 2007 Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39: 61-69.