DNA methylation and chromatin regulation during fleshy fruit development and ripening

Frontiers in Plant Science

Volumn 7, Issue JUNE2016, 2016, Pages

  Gallusci, Philippe ^a   Hodgman, Charlie ^b   Teyssier, Emeline ^a   Seymour, Graham B ^b  

^a Bordeaux Sciences Agro   (France)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Crop improvement; DNA methylation; Epigenetics; Ripening; Tomato

Indexed keywords

EID: 84975153630     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00807     Document Type: Review

References (109)

1. Ahmad, A., Zhang, Y., and Cao, X. F. (2010). Decoding the epigenetic language of plant development. Mol. Plant 3, 719–728. doi: 10.1093/mp/ssq026
2. Almada, R., Cabrera, N., Casaretto, J. A., Peña-Cortés, H., Ruiz-Lara, S., and Villanueva, E. G. (2011). Epigenetic repressor-like genes are differentially regulated during grapevine (Vitis vinifera L.) development. Plant Cell Rep. 30, 1959–1968. doi: 10.1007/s00299-011-1104-0
3. Aquea, F., Timmermann, T., and Arce-Johnson, P. (2010). Analysis of histone acetyltransferase and deacetylase families of Vitis vinifera. Plant Physiol. Biochem. 48, 194–199. doi: 10.1016/j.plaphy.2009.12.009
4. Aquea, F., Vega, A., Timmermann, T., Poupin, M. J., and Arce-Johnson, P. (2011). Genome-wide analysis of the SET DOMAIN GROUP family in Grapevine. Plant Cell Rep. 30, 1087–1097. doi: 10.1007/s00299-011-1015-0
5. Baulcombe, D. C., and Dean, C. (2014). Epigenetic regulation in plant responses to the environment. Cold Spring Harb. Perspect. Biol. 6:a019471. doi: 10.1101/cshperspect.a019471
6. Benvenuto, G., Formiggini, F., Laflamme, P., Malakhov, M., and Bowler, C. (2002). The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome Context. Curr. Biol. 12, 1529–1534. doi: 10.1016/S0960-9822(02)01105-3
7. Berr, A., Shafiq, S., and Shen, W. H. (2011). Histone modifications in transcriptional activation during plant development. Biochim. Biophys. Acta 1809, 567–576. doi: 10.1016/j.bbagrm.2011.07.001
8. Bond, D. M., and Baulcombe, D. C. (2015). Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 112, 917–922. doi: 10.1073/pnas.1413053112
9. Borges, F., and Martienssen, R. A. (2015). The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 16, 727–741. doi: 10.1038/nrm4085
10. Boureau, L., How-Kit, A., Teyssier, E., Drevensek, S., Rainieri, M., Joubès, J., et al. (2016). A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants. Plant Mol. Biol. 90, 485–501. doi: 10.1007/s11103-016-0436-0
11. Cao, D., Ju, Z., Gao, C., Mei, X., Fu, D., Zhu, H., et al. (2014). Genomewide identification of cytosine-5 DNA methyltransferases and demethylases in Solanum lycopersicum. Gene 550, 230–237. doi: 10.1016/j.gene.2014.08.034
12. Chaïb, J., Devaux, M.-F., Grotte, M.-G., Robini, K., Causse, M., Lahaye, M., et al. (2007). Physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. J. Exp. Bot. 58, 1915–1925. doi: 10.1093/jxb/erm046
13. Chan, S. W. L., Henderson, I. R., and Jacobsen, S. E. (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6, 351–360. doi: 10.1038/nrg1601
14. Chen, H., Shen, Y., Tang, X., Yu, L., Wang, J., Guo, L., et al. (2006). Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. The Plant Cell 18, 1991–2004. doi: 10.1105/tpc.106.043224
15. Chen, W., Kong, J., Qin, C., Yu, S., Tan, J., Chen, Y.-R., et al. (2015). Requirement of CHROMOMETHYLASE3 for somatic inheritance of the spontaneous tomato epimutation colourless non-ripening. Sci. Rep. 5:9192. doi: 10.1038/srep09192
16. Cheniclet, C., Rong, W. Y., Causse, M., Frangne, N., Bolling, L., Carde, J. P., et al. (2005). Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol. 139, 1984–1994. doi: 10.1104/pp.105.068767
17. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J. J., Goldberg, R. B., et al. (2002). DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42. doi: 10.1016/S0092-8674(02)00807-3
18. Cigliano, R. A., Sanseverino, W., Cremona, G., Ercolano, M. R., Conicella, C., and Consiglio, F. M. (2013). Genome-wide analysis of histone modifiers in tomato: gaining an insight into their developmental roles. BMC Genomics 14:57. doi: 10.1186/1471-2164-14-57
19. Cokus, S. J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C. D., et al. (2008). Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219. doi: 10.1038/nature06745
20. Cortijo, S., Wardenaar, R., Colomé-Tatché, M., Gilly, A., Etcheverry, M., Labadie, K., et al. (2014). Mapping the epigenetic basis of complex traits. Science 343, 1145–1148. doi: 10.1126/science.1248127
21. Cubas, P., Vincent, C., and Coen, E. (1999). An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161. doi: 10.1038/43657
22. Dapp, M., Reinders, J., Bédiée, A., Balsera, C., Bucher, E., Theiler, G., et al. (2015). Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nat. Plants 1:15092. doi: 10.1038/nplants.2015.92
23. Du, J., Johnson, L. M., Groth, M., Feng, S., Hale, C. J., Li, S., et al. (2014). Mechanism of DNA methylation-directed histone methylation by KRYPTONITE. Mol. Cell. 55, 495–504. doi: 10.1016/j.molcel.2014.06.009
24. Eichten, S. R., Schmitz, R. J., and Springer, N. M. (2014). Epigenetics: beyond chromatin modifications and complex genetic regulation. Plant Physiol. 165, 933–947. doi: 10.1104/pp.113.234211
25. El-Sharkawy, I., Liang, D., and Xu, K. (2015). Transcriptome analysis of an apple (Malus × domestica) yellow fruit somatic mutation identifies a gene network module highly associated with anthocyanin and epigenetic regulation. J. Exp. Bot. 66, 7359–7376. doi: 10.1093/jxb/erv433
26. Eriksson, E. M., Bovy, A., Manning, K., Harrison, L., Andrews, J., De Silva, J., et al. (2004). Effect of the Colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol. 136, 4184–4197. doi: 10.1104/pp.104.045765
27. Filion, G. J., van Bemmel, J. G., Braunschweig, U., Talhout, W., Kind, J., Ward, L. D., et al. (2010). Systematic protein location mapping reveals five principal chromatin types in drosophila cells. Cell 143, 212–224. doi: 10.1016/j.cell.2010.09.009
28. Finnegan, E. J., Peacock, W. J., and Dennis, E. S. (1996). Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl. Acad. Sci. U.S.A. 93, 8449–8454. doi: 10.1073/pnas.93.16.8449
29. Fisher, A. J., and Franklin, K. A. (2011). Chromatin remodelling in plant light signalling. Physiol. Plant. 142, 305–313. doi: 10.1111/j.1399-3054.2011.01476.x
30. FitzGerald, J., Luo, M., Chaudhury, A., and Berger, F. (2008). DNA methylation causes predominant maternal controls of plant embryo growth. PLoS ONE 3:e2298. doi: 10.1371/journal.pone.0002298
31. Gapper, N. E., McQuinn, R. P., and Giovannoni, J. J. (2013). Molecular and genetic regulation of fruit ripening. Plant Mol. Biol. 82, 575–591. doi: 10.1007/s11103013-0050-3
32. García-Aguilar, M., and Gillmor, C. S. (2015). Zygotic genome activation and imprinting: parent-of-origin gene regulation in plant embryogenesis. Curr. Opin. Plant Biol. 27, 29–35. doi: 10.1016/j.pbi.2015.05.020
33. Gehring, M., Reik, W., and Henikoff, S. (2009). DNA demethylation by DNA repair. Trends Genet. 25, 82–90. doi: 10.1016/j.tig.2008.12.001
34. Gent, J. I., Ellis, N. A., Guo, L., Harkess, A. E., Yao, Y., Zhang, X., et al. (2013). CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 23, 628–637. doi: 10.1101/gr.146985.112
35. Gong, Z., Morales-Ruiz, T., Ariza, R. R., Roldán-Arjona, T., David, L., and Zhu, J. K. (2002). ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814. doi: 10.1016/S00928674(02)01133-9
36. Hadfield, K. A., Dandekar, A. M., and Romani, R. J. (1993). Demethylation of ripening specific genes in tomato fruit. Plant Sci. 92, 13–18. doi: 10.1016/01689452(93)90061-4
37. He, G., Elling, A. A., and Deng, X. W. (2011). The epigenome and plant development. Annu. Rev. Plant Biol. 62, 411–435. doi: 10.1146/annurevarplant-042110-103806
38. He, X.-J., Chen, T., and Zhu, J.-K. (2011). Regulation and function of DNA methylation in plants and animals. Cell Res. 21, 442–465. doi: 10.1038/cr.2011.23
39. How Kit, A. H., Boureau, L., Stammitti-Bert, L., Rolin, D., Teyssier, E., and Gallusci, P. (2010). Functional analysis of SlEZ1 a tomato Enhancer of zeste (E (z)) gene demonstrates a role in flower development. Plant Mol. Biol. 74, 201–213. doi: 10.1007/s11103-010-9657-9
40. Hsieh, T. F., and Fischer, R. L. (2005). Biology of chromatin dynamics. Annu. Rev. Plant Biol. 56, 327–351. doi: 10.1146/annurev.arplant.56.032604.144118
41. Hu, Y., Morota, G., Rosa, G. J., and Gianola, D. (2015). Prediction of plant height in Arabidopsis thaliana using DNA methylation data. Genetics 201, 779–793. doi: 10.1534/genetics.115.177204
42. Jackson, J. P., Lindroth, A. M., Cao, X., and Jacobsen, S. E. (2002). Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560. doi: 10.1038/nature731
43. Janssen, B. J., Thodey, K., Schaffer, R. J., Alba, R., Balakrishnan, L., Bishop, R., et al. (2008). Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol. 8:16. doi: 10.1186/1471-2229-8-16
44. Johannes, F., Porcher, E., Teixeira, F. K., Saliba-Colombani, V., Simon, M., Agier, N., et al. (2009). Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5:e1000530. doi: 10.1371/journal.pgen.1000530
45. Kanno, T., Mette, M. F., Kreil, D. P., Aufsatz, W., Matzke, M., and Matzke, A. J. (2004). Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr. Biol. 14, 801–805. doi: 10.1016/j.cub.2004.04.037
46. Kooke, R., Johannes, F., Wardenaar, R., Becker, F., Etcheverry, M., Colot, V., et al. (2015). Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell 27, 337–348. doi: 10.1105/tpc.114.133025
47. Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693–705. doi: 10.1016/j.cell.2007.02.005
48. Lauria, M., and Rossi, V. (2011). Epigenetic control of gene regulation in plants. Biochim. Biophys. Acta 1809, 369–378. doi: 10.1016/j.bbagrm.2011.03.002
49. Law, J. A., and Jacobsen, S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220. doi: 10.1038/nrg2719
50. Lee, S. I., and Kim, N. S. (2014). Transposable elements and genome size variations in plants. Genomics Inform. 12, 87–97. doi: 10.5808/GI.2014.12.3.87
51. Lei, M., Zhang, H., Julian, R., Tang, K., Xie, S., and Zhu, J. K. (2015). Regulatory link between DNA methylation and active demethylation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 112, 3553–3557. doi: 10.1073/pnas.1502279112
52. Li, B., Carey, M., and Workman, J. L. (2007). The role of chromatin during transcription. Cell 128, 707–719. doi: 10.1016/j.cell.2007.01.015
53. Li, X., Zhu, J., Hu, F., Ge, S., Ye, M., Xiang, H., et al. (2012). Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13:300. doi: 10.1186/1471-2164-13-300
54. Li, Y., Deng, H., Miao, M., Li, H., Huang, S., Wang, S., et al. (2015). Tomato MBD5, a methyl CpG binding domain protein, physically interacting with UVdamaged DNA binding protein-1, functions in multiple processes. New Phytol. 210, 208–226. doi: 10.1111/nph.13745
55. Lindroth, A. M., Cao, X., Jackson, J. P., Zilberman, D., McCallum, C. M., Henikoff, S., et al. (2001). Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080. doi: 10.1126/science.1059745
56. Lippman, Z., Gendrel, A. V., Black, M., Vaughn, M. W., Dedhia, N., McCombie, W. R., et al. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476. doi: 10.1038/nature02651
57. Lister, R., O’Malley, R. C., Tonti-Filippini, J., Gregory, B. D., Berry, C. C., Millar, A. H., et al. (2008). Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133, 523–536. doi: 10.1016/j.cell.2008.03.029
58. Liu, D.-D., Dong, Q.-L., Fang, M.-J., Chen, K.-Q., and Hao, Y.-J. (2012). Ectopic expression of an apple apomixis-related gene MhFIE induces co-suppression and results in abnormal vegetative and reproductive development in tomato. J. Plant physiol. 169, 1866–1873. doi: 10.1016/j.jplph.2012.07.018
59. Liu, R., How-Kit, A., Stammitti, L., Teyssier, E., Rolin, D., MortainBertrand, A., et al. (2015). A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc. Natl. Acad. Sci. U.S.A. 112, 10804–10809. doi: 10.1073/pnas.1503362112
60. Liu, Y., Roof, S., Ye, Z., Barry, C., van Tuinen, A., Vrebalov, J., et al. (2004). Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc. Natl. Acad. Sci. U.S.A 101, 9897–9902. doi: 10.1073/pnas.0400935101
61. Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A. J., King, G. J., et al. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBPbox transcription factor inhibits tomato fruit ripening. Nat. Genet. 38, 948–952. doi: 10.1038/ng1841
62. Martin, A., Troadec, C., Boualem, A., Rajab, M., Fernandez, R., Morin, H., et al. (2009). A transposon-induced epigenetic change leads to sex determination in melon. Nature 461, 1135–1138. doi: 10.1038/nature08498
63. Matzke, M. A., Kanno, T., and Matzke, A. J. M. (2015). RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Ann. Rev. Plant Biol. 66, 243–267. doi: 10.1146/annurev-arplant-043014114633
64. Matzke, M. A., and Mosher, R. A. (2014). RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15, 394–408. doi: 10.1038/nrg3683
65. Messeguer, R., Ganal, M., Steffens, J., and Tanksley, S. D. (1991). Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol. Biol. 16, 753–770. doi: 10.1007/BF00015069
66. Mintz-Oron, S., Mandel, T., Rogachev, I., Feldberg, L., Lotan, O., Yativ, M., et al. (2008). Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol. 147, 823–851. doi: 10.1104/pp.108.116004
67. Mirouze, M., Lieberman-Lazarovich, M., Aversano, R., Bucher, E., Nicolet, J., Reinders, J., et al. (2012). Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109, 5880–5885. doi: 10.1073/pnas.1120841109
68. Mirouze, M., and Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Curr. Opin. Plant Biol 14, 267–274. doi: 10.1016/j.pbi.2011.03.004
69. Mozgova, I., and Hennig, L. (2015). The polycomb group protein regulatory network. Annu. Rev. Plant Biol. 66, 269–296. doi: 10.1146/annurev-arplant043014-115627
70. Msogoya, T. J., Grout, B. W., and Roberts, A. (2011). Reduction in genome size and DNA methylation alters plant and fruit development in tissue culture induced off-type banana (Musa spp.). J. Anim. Plant Sci. 3, 1450–1456.
71. Mustilli, A. C., Fenzi, F., Ciliento, R., Alfano, F., and Bowler, C. (1999). Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11, 145–157. doi: 10.1105/tpc.11.2.145
72. Ong-Abdullah, M., Ordway, J. M., Jiang, N., Ooi, S., Kok, S.-Y., Sarpan, N., et al. (2015). Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525, 533–537. doi: 10.1038/nature15365
73. Paterson, A. H., Freeling, M., Tang, H., and Wang, X. (2010). Insights from the comparison of plant genome sequences. Annu. Rev. Plant Biol. 61, 349–372. doi: 10.1146/annurev-arplant-042809-112235
74. Pikaard, C. S., and Mittelsten Scheid, O. (2014). Epigenetic regulation in plants. Cold Spring Harb. Perspect. Biol. 6:a019315. doi: 10.1101/cshperspect.a019315
75. Probst, A. V., and Scheid, O. M. (2015). Stress-induced structural changes in plant chromatin. Curr. Opin. Plant Biol. 27, 8–16. doi: 10.1016/j.pbi.2015.05.011
76. Qian, W., Miki, D., Lei, M., Zhu, X., Zhang, H., Liu, Y., et al. (2014). Regulation of active DNA demethylation by an alpha-crystallin domain protein in Arabidopsis. Mol. Cell. 55, 361–371. doi: 10.1016/j.molcel.2014.06.008
77. Qian, W., Miki, D., Zhang, H., Liu, Y., Zhang, X., Tang, K., et al. (2012). A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science 336, 1445–1448. doi: 10.1126/science.1219416
78. Quadrana, L., Almeida, J., Asís, R., Duffy, T., Dominguez, P. G., Bermúdez, L., et al. (2014). Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat. Commun. 5:4027. doi: 10.1038/ncomms5027
79. Rensing, S. A. (2014). Gene duplication as a driver of plant morphogenetic evolution. Curr. Opin. Plant Biol. 17, 43–48. doi: 10.1016/j.pbi.2013.11.002
80. Reyes, J. C. (2006). Chromatin modifiers that control plant development. Curr. Opin. Plant Biol. 9, 21–27. doi: 10.1016/j.pbi.2005.11.010
81. Roudier, F., Ahmed, I., Berard, C., Sarazin, A., Mary-Huard, T., Cortijo, S., et al. (2011). Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928–1938. doi: 10.1038/emboj.2011.103
82. Schoft, V. K., Chumaka, N., Choi, Y., Hannonc, M., Garcia-Aguilara, M., Machlicovaa, A., et al. (2011). Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc. Natl. Acad. Sci. U.S.A. 108, 8042–8047. doi: 10.1073/pnas.1105117108
83. Seymour, G. B., Østergaard, L., Chapman, N. H., Knapp, S., and Martin, C. (2013). Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219–241. doi: 10.1146/annurev-arplant-050312-120057
84. Shen, H., He, H., Li, J., Chen, W., Wang, X., Guo, L., et al. (2012). Genomewide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24, 875–892. doi: 10.1105/tpc.111.094870
85. Shivaprasad, P. V., Dunn, R. M., Santos, B. A., Bassett, A., and Baulcombe, D. C. (2012). Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31, 257–266. doi: 10.1038/emboj.2011.458
86. Teixeira, F. K., Heredia, F., Sarazin, A., Roudier, F., Boccara, M., Ciaudo, C., et al. (2009). A role for RNAi in the selective correction of DNA methylation defects. Science 323, 1600–1604. doi: 10.1126/science.1165313
87. Telias, A., Lin-Wang, K., Stevenson, D. E., Cooney, J. M., Hellens, R. P., Allan, A. C., et al. (2011). Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol. 11:93. doi: 10.1186/1471-2229-11-93
88. Tenaillon, M. I., Hollister, J. D., and Gaut, B. S. (2010). A triptych of the evolution of plant transposable elements. Trends Plant Sci. 15, 471–478. doi: 10.1016/j.tplants.2010.05.003
89. Teyssier, E., Bernacchia, G., Maury, S., How Kit, A., Stammitti-Bert, L., Rolin, D., et al. (2008). Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228, 391–399. doi: 10.1007/s00425-008-0743-z
90. Thompson, A. J., Tor, M., Barry, C. S., Vrebalov, J., Orfila, C., Jarvis, M. C., et al. (1999). Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol. 120, 383–390. doi: 10.1104/pp.120.2.383
91. van der Knaap, E., Chakrabarti, M., Chu, Y. H., Clevenger, J. P., Illa-Berenguer, E., Huang, Z., et al. (2014). What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front. Plant Sci. 5:227. doi: 10.3389/fpls.2014.00227
92. Vanneste, K., Baele, G., Maere, S., and Van de Peer, Y. (2014). Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24, 1334–1347. doi: 10.1101/gr.168997.113
93. Vermaak, D., Ahmad, K., and Henikoff, S. (2003). Maintenance of chromatin states: an open-and-shut case. Curr. Opin. Cell Biol. 15, 266–274. doi: 10.1016/S09550674(03)00043-7
94. Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., et al. (2002). A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science 296, 343–346. doi: 10.1126/science.1068181
95. Wang, C., Dong, X., Jin, D., Zhao, Y., Xie, S., Li, X., et al. (2015). Methyl-CpGbinding domain protein MBD7 is required for active DNA demethylation in Arabidopsis. Plant Physiol. 167, 905–914. doi: 10.1104/pp.114.252106
96. Wang, Z., Meng, D., Wang, A., Li, T., Jiang, S., Cong, P., et al. (2013). The methylation of the PcMYB10 promoter is associated with greenskinned sport in Max Red Bartlett pear. Plant Physiol. 162, 885–896. doi: 10.1104/pp.113.214700
97. Williams, B. P., Pignatta, D., Henikoff, S., and Gehring, M. (2015). Methylationsensitive expression of a DNA demethylase gene serves as an epigenetic rheostat. PLoS Genet. 11:e1005142. doi: 10.1371/journal.pgen.1005142
98. Woo, H. R., Dittmer, T. A., and Richards, E. J. (2008). Three SRAdomain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet. 4:e1000156. doi: 10.1371/journal.pgen.1000156
99. Xu, J., Xu, H., Liu, Y., Wang, X., Xu, Q., and Deng, X. (2015a). Genomewide identification of sweet orange (Citrus sinensis) histone modification gene families and their expression analysis during the fruit development and fruit-blue mold infection process. Front. Plant Sci. 6:607. doi: 10.3389/fpls.2015.00607
100. Xu, J., Xu, H., Xu, Q., and Deng, X. (2015b). Characterization of DNA Methylation variations during fruit development and ripening of sweet orange. Plant Mol. Biol. Reporter 33, 1–11. doi: 10.1007/s11105-014-0732-2
101. Yamamuro, C., Miki, D., Zheng, Z., Ma, J., Wang, J., Yang, Z., et al. (2014). Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nat. Commun. 5:462. doi: 10.1038/ncomms5062
102. Yelina, N. E., Lambing, C., Hardcastle, T. J., Zhao, X., Santos, B., and Henderson, I. R. (2015). DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev. 29, 2183–2202. doi: 10.1101/gad.270876.115
103. Yu, A., Lepère, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., et al. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl. Acad. Sci. U.S.A. 110, 2389–2394. doi: 10.1073/pnas.1211757110
104. Zemach, A., Kim, M. Y., Hsieh, P. H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., et al. (2013). The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205. doi: 10.1016/j.cell.2013.02.033
105. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S. W. L., Chen, H., et al. (2006). Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201. doi: 10.1016/j.cell.2006.08.003
106. Zhao, L., Lu, J., Zhang, J., Wu, P. Y., Yang, S., and Wu, K. (2014). Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Front. Plant Sci. 5:760. doi: 10.3389/fpls.2014.00760
107. Zhong, S., Fei, Z., Chen, Y.-R., Zheng, Y., Huang, M., Vrebalov, J., et al. (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31, 154–159. doi: 10.1038/nbt.2462
108. Zhu, J. K. (2009). Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143–166. doi: 10.1146/annurev-genet-102108-134205
109. Zilberman, D., Gehring, M., Tran, R. K., Ballinger, T., and Henikoff, S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61–69. doi: 10.1038/ng1929