Locus- and site-specific DNA methylation of 19 kDa zein genes in maize

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Xu, Jian Hong ^a   Wang, Ruixian ^a,d   Li, Xinxin ^a   Miclaus, Mihai ^b   Messing, Joachim ^c  

^a ZHEJIANG UNIVERSITY   (China)

^b NATIONAL INSTITUTE FOR RESEARCH AND DEVELOPMENT IN MICROTECHNOLOGIES   (Romania)

^c RUTGERS UNIVERSITY   (United States)

^d ANKANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DNA METHYLATION; ENDOSPERM; GENE CLUSTER; GENE DOSAGE; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; MAIZE; NONHUMAN; PLANT DEVELOPMENT; PLANT GENE; PLANT LEAF; PROMOTER REGION; TISSUE CULTURE; TRANSGENIC PLANT; Z1A GENE; Z1B GENE; ANTIBODY SPECIFICITY; CHROMOSOMAL MAPPING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; MULTIGENE FAMILY; OPEN READING FRAME; PLANT CHROMOSOME; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUE;

ISOPROTEIN; ZEIN;

CHROMOSOME MAPPING; CHROMOSOMES, PLANT; DNA METHYLATION; ENDOSPERM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENETIC LOCI; MULTIGENE FAMILY; OPEN READING FRAMES; ORGAN SPECIFICITY; PLANT LEAVES; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; TISSUE CULTURE TECHNIQUES; ZEA MAYS; ZEIN;

EID: 84954117142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146416     Document Type: Article

References (51)

1. Gavery MR, Roberts SB (2013) Predominant intragenic methylation is associated with gene expression characteristics in a bivalve mollusc. PeerJ 1:e215. doi: 10.7717/peerj.215 PMID: 24282674
2. Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351-360. PMID: 15861207
3. Gehring M, Henikoff S (2007) DNA methylation dynamics in plant genomes. Biochim Biophys Acta 1769:276-286. PMID: 17341434
4. Zhang M, Kimatu JN, Xu K, Liu B (2010) DNA cytosine methylation in plant development. Journal of Genetics and Genomics 37:1-12. doi: 10.1016/S1673-8527 (09) 60020-5 PMID: 20171573
5. Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418-424. PMID: 17522675
6. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, et al. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466. PMID: 17334365
7. Park JY, Kim D, Yang M, Park HY, Lee SH, Rincon M, et al. (2013) Gene silencing of SLC5A8 identified by genome-wide methylation profiling in lung cancer. Lung Cancer 79:198-204. doi: 10.1016/j. lungcan. 2012.11.019 PMID: 23273563
8. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, et al. (2006) Genome-wide highresolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126:1189-1201. PMID: 16949657
9. Zemach A, Kim MY, Silva P, Rodrigues JA, Dotson B, Brooks MD, et al. (2010) Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA 107:18729-18734. doi: 10.1073/pnas.1009695107 PMID: 20937895
10. Goettel W, Messing J (2013) Epiallele biogenesis in maize. Gene 516:8-23. doi: 10.1016/j.gene.2012. 12.034 PMID: 23266636
11. Morel JB, Mourrain P, Beclin C, Vaucheret H (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10:1591-1594. PMID: 11137011
12. Reddy MS, Dinkins RD, Collins GB (2003) Gene silencing in transgenic soybean plants transformed via particle bombardment. Plant Cell Rep 21:676-683. PMID: 12789418
13. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, et al. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107:8689-8694. doi: 10. 1073/pnas.1002720107 PMID: 20395551
14. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315-322. doi: 10.1038/nature08514 PMID: 19829295
15. Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328:916-919. doi: 10.1126/science.1186366 PMID: 20395474
16. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature genetics 39:61-69. PMID: 17128275
17. Wang X, Wheeler D, Avery A, Rago A, Choi JH, Colbourne JK, et al. (2013) Function and evolution of DNA methylation in Nasonia vitripennis. PLoS Genet 9:e1003872. doi: 10.1371/journal.pgen. 1003872 PMID: 24130511
18. Wang Y, Wang X, Lee TH, Mansoor S, Paterson AH (2013) Gene body methylation shows distinct patterns associated with different gene origins and duplication modes and has a heterogeneous relationship with gene expression in Oryza sativa (rice). New Phytol 198:274-283. doi: 10.1111/nph.12137 PMID: 23356482
19. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nature Reviews Genetics 9:465-476. doi: 10.1038/nrg2341 PMID: 18463664
20. Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12:2521-2528. PMID: 8389699
21. 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 USA 93:7783-7788. PMID: 8755553
22. La H, Ding B, Mishra GP, Zhou B, Yang H, Bellizzi Mdel R, et al. (2011) A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc Natl Acad Sci USA 108:15498-15503. doi: 10.1073/pnas.1112704108 PMID: 21896764
23. Peschke VM, Phillips RL, Gengenbach BG (1991) Genetic and molecular analysis of tissue-culturederived Ac elements. Theor Appl Genet 82:121-129. doi: 10.1007/BF00226202 PMID: 24213055
24. Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Thompson WF, et al. (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880-2895. doi: 10.1371/journal.pbio.0060302 PMID: 19071958
25. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM (2014) Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics 198:209-218. doi: 10. 1534/genetics.114.165480 PMID: 25023398
26. Rhee Y, Sekhon RS, Chopra S, Kaeppler S (2010) Tissue Culture-Induced Novel Epialleles of a Myb Transcription Factor Encoded by pericarp color1 in Maize. Genetics 186:843-U151. doi: 10.1534/genetics.110.117929 PMID: 20823340
27. Shibukawa T, Yazawa K, Kikuchi A, Kamada H (2009) Possible involvement of DNA methylation on expression regulation of carrot LEC1 gene in its 5 '-upstream region. Gene 437:22-31. doi: 10.1016/j. gene.2009.02.011 PMID: 19264116
28. Shewry PR, Napier JA, Tatham AS (1995) Seed storage proteins: structures and biosynthesis. Plant Cell 7:945-956. PMID: 7640527
29. Xu JH, Messing J (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor Appl Genet 119:1397-1412. doi: 10.1007/s00122-009-1143-x PMID: 19727653
30. Miclaus M, Xu JH, Messing J (2011) Differential gene expression and epiregulation of alpha zein gene copies in maize haplotypes. PLoS Genet 7:e1002131. doi: 10.1371/journal.pgen. 1002131 PMID: 21731501
31. Bezdek M, Koukalova B, Kuhrova V, Vyskot B (1992) Differential sensitivity of CG and CCG DNAsequences to ethionine-induced hypomethylation of the nicotiana-tabacum genome. Febs Letters 300:268-270. PMID: 1372869
32. Jeddeloh JA, Richards EJ (1996) (m) CCG methylation in angiosperms. Plant Journal 9:579-586. PMID: 8653110
33. Bianchi MW, Viotti A (1988) DNA Methylation and tissue-specific transcription of the storage protein genes of maize. Plant Mol Biol 11:203-214. doi: 10.1007/BF00015672 PMID: 24272262
34. Goettel W, Messing J (2013) Paramutagenicity of a p1 epiallele in maize. Theor Appl Genet 126:159-177. doi: 10.1007/s00122-012-1970-z PMID: 22986680
35. Kodrzycki R, Boston RS, Larkins BA (1989) The opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1:105-114. PMID: 2535458
36. Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci USA 94:7685-7690. PMID: 9207153
37. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, et al. (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451-1454. doi: 10.1126/science.1172417 PMID: 19520962
38. Ueda T, Messing J (1991) A homologous expression system for cloned zein genes. Theoretical and Applied Genetics 82:93-100. doi: 10.1007/BF00231282 PMID: 24212865
39. Yu X, Li X, Zhao X, Jiang L, Miao G, Pang J, et al. (2011) Tissue culture-induced genomic alteration in maize (Zea mays) inbred lines and F1 hybrids. Annals of Applied Biology 158:237-247.
40. Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci USA 90:8773-8776. PMID: 8415605
41. Lin CJ, Lin XY, Hu LJ, Yang JJ, Zhou TQ, Long L, et al. (2012) Dramatic genotypic difference in, and effect of genetic crossing on, tissue culture-induced mobility of retrotransposon Tos17 in rice. Plant Cell Rep 31:2057-2063. doi: 10.1007/s00299-012-1316-y PMID: 22945626
42. Stroud H, Ding B, Simon SA, Feng SH, Bellizzi M, Pellegrini M, et al. (2013) Plants regenerated from tissue culture contain stable epigenome changes in rice. Elife 2:e00354. doi: 10.7554/eLife.00354 PMID: 23539454
43. Temel A, Gozukirmizi N (2013) Analysis of retrotransposition and DNA methylation in barley callus culture. Acta Biol Hung 64:86-95. doi: 10.1556/ABiol.64.2013.1.8 PMID: 23567833
44. Gonzalez A, Saiz A, Acedo A, Ruiz M, Polanco C (2013) Analysis of genomic DNA methylation patterns in regenerated and control plants of rye (Secale cereale L.). Plant Growth Regulation 70:227-236.
45. Krizova K, Fojtova M, Depicker A, Kovarik A (2009) Cell culture-induced gradual and frequent epigenetic reprogramming of invertedly repeated tobacco transgene epialleles. Plant Physiol 149:1493-1504. doi: 10.1104/pp. 108.133165 PMID: 19129419
46. Cao X, Jacobsen SE (2002) Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138-1144. PMID: 12121623
47. Cao X, Jacobsen SE (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. PMID: 12151602
48. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215-219. doi: 10.1038/nature06745 PMID: 18278030
49. Chen J, Zeng B, Zhang M, Xie S, Wang G, Hauck A, et al. (2014) Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol 166:252-264. doi: 10.1104/pp. 114. 240689 PMID: 25037214
50. Zhang M, Xu C, Von Wettstein D, Liu B (2011) Tissue-specific differences in cytosine methylation and their association with differential gene expression in sorghum. Plant Physiol 156:1955-1966. doi: 10. 1104/pp. 111.176842 PMID: 21632971
51. Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13:207-209.