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Characterization of DNA Methylation Variations During Fruit Development and Ripening of Sweet Orange

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Abstract

DNA methylation is a type of epigenetic modification involved in many biological processes. Recent studies have shown that DNA methylation plays important roles in regulating fruit development and ripening. In the present study, sweet oranges at six developmental stages were investigated to understand the possible roles of DNA methylation during fruit development and ripening. Analysis of genomic DNA methylation levels in different fruit tissues and developmental stages indicated that methylation levels were not static during fruit development and ripening. To explore the possible contributions of methylation-related genes in fruit development and ripening process, the full-length coding sequences corresponding to three types of DNA methyltransferase families (CsMET1, CsCMT3, and CsDRM1), a chromatin-remodeling gene (CsDDM1), and a demethylation gene (CsDME1) were isolated. The expression profiles of these methylation-related genes were analyzed in vegetative tissues (seedlings and leaves) and reproductive tissues (three stages of flowering and six stages of fruit development). The results showed that CsDRM1 was highly expressed in seedlings, leaves, and flowers compared with other genes. During fruit development and ripening, CsMET1, CsCMT1, CsCMT2, CsDRM1, and CsDMEs showed higher expression in the peel than in the flesh. However, global DNA methylation level changes could not be explained by the expression of a single gene, suggesting that the methylation and demethylation system may cooperatively contribute to the final global DNA methylation pattern.

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References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796

    Article  Google Scholar 

  • Aufsatz W, Mette MF, Matzke AJ, Matzke M (2004) The role of MET1 in RNA-directed de novo and maintenance methylation of CG dinucleotides. Plant Mol Biol 54(6):793–804

    Article  CAS  PubMed  Google Scholar 

  • Bain JM (1958) Morphological, anatomical, and physiological changes in the developing fruit of the Valencia orange, Citrus sinensis (L) Osbeck. Aust J Bot 6(1):1–23

    Article  CAS  Google Scholar 

  • Bartee L, Malagnac F, Bender J (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev 15(14):1753–1758

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12(13):1138–1144

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Zhang J, Xu J, Ye J, Yun Z, Xu Q, Deng X (2012) Comprehending crystalline β-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus. J Exp Bot 63(12):4403–4417

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng Y-J, Guo W-W, Yi H-L, Pang X-M, Deng X (2003) An efficient protocol for genomic DNA extraction from Citrus species. Plant Mol Biol Report 21(2):177–178

    Article  Google Scholar 

  • 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(1):33–42

    Article  CAS  PubMed  Google Scholar 

  • Ecker JR (2013) Epigenetic trigger for tomato ripening. Nat Biotechnol 31(2):119–120

    Article  CAS  PubMed  Google Scholar 

  • Ergle DR, Katterman FR (1961) Deoxyribonucleic acid of cotton. Plant Physiol 36(6):811

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fang J, Song C, Qian J, Zhang XY, Shangguan L, Yu H, Wang X (2010) Variation of cytosine methylation in 57 sweet orange cultivars. Acta Physiol Plant 32(6):1023–1030

    Article  CAS  Google Scholar 

  • Fraga MF, Uriol E, Diego LB, Berdasco M, Esteller M, Canal MJ, Rodriguez R (2002) High-performance capillary electrophoretic method for the quantification of 5-methyl 2′-deoxycytidine in genomic DNA: application to plant, animal and human cancer tissues. Electrophoresis 23(11):1677–1681

    Article  CAS  PubMed  Google Scholar 

  • Gehring M, Henikoff S (2007) DNA methylation dynamics in plant genomes. Biochim Biophys Acta 1769(5–6):276–286

    Article  CAS  PubMed  Google Scholar 

  • Gehring M, Reik W, Henikoff S (2009) DNA demethylation by DNA repair. Trends Genet 25(2):82–90

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111(6):803–814

    Article  CAS  PubMed  Google Scholar 

  • Hasbún R, Valledor L, Berdasco M, Santamaría E, Canal M, Rodríguez R, Ríos D, Sánchez M (2005) In vitro proliferation and genome DNA methylation in adult chestnuts. Acta Horticult 693:333

    Google Scholar 

  • He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Comai L (1998) A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149(1):307–318

    CAS  PubMed Central  PubMed  Google Scholar 

  • Higo H, Tahir M, Takashima K, Miura A, Watanabe K, Tagiri A, Ugaki M, Ishikawa R, Eiguchi M, Kurata N, Sasaki T, Richards E, Takano M, Kishimoto N, Kakutani T, Habu Y (2012) DDM1 (decrease in DNA methylation) genes in rice (Oryza sativa). Mol Genet Genomics 287(10):785–792

    Article  CAS  PubMed  Google Scholar 

  • Hsieh CL (2000) Dynamics of DNA methylation pattern. Curr Opin Genet Dev 10(2):224–228

    Article  CAS  PubMed  Google Scholar 

  • Katz E, Fon M, Lee YJ, Phinney BS, Sadka A, Blumwald E (2007) The citrus fruit proteome: insights into citrus fruit metabolism. Planta 226(4):989–1005

    Article  CAS  PubMed  Google Scholar 

  • Ladanyia M (2010) Citrus fruit: biology, technology and evaluation. San Diego, Academic Press, p 193–196

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, Zhang G, Zheng X, Zhang H, Zhang S (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13(1):300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133(3):523–536

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Q, Xu J, Liu Y, Zhao X, Deng X, Guo L, Gu J (2007) A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). J Exp Bot 58(15–16):4161–4171

    Article  CAS  PubMed  Google Scholar 

  • Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38(8):948–952

    Article  CAS  PubMed  Google Scholar 

  • Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16(5):753–770

    Article  CAS  PubMed  Google Scholar 

  • Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marín MI, Martínez-Macías MI, Ariza RR, Roldán-Arjona T (2006) Demeter and repressor of silencing 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci U S A 103(18):6853–6858

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci U S A 104(16):6752–6757

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rival A, Jaligot E, Beule T, Finnegan EJ (2008) Isolation and expression analysis of genes encoding MET, CMT, and DRM methyltransferases in oil palm (Elaeis guineensis Jacq.) in relation to the ‘mantled’ somaclonal variation. J Exp Bot 59(12):3271–3281

    Article  CAS  PubMed  Google Scholar 

  • Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S, Kaneko T, Nakamura Y, Shibata D, Egholm M (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  CAS  Google Scholar 

  • Scharer OD, Jiricny J (2001) Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23(3):270–281

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Zubko E, Meyer P (2008) Cooperative activity of DNA methyltransferases for maintenance of symmetrical and non-symmetrical cytosine methylation in Arabidopsis thaliana. Plant J 56(5):814–823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Telias A, Lin-Wang K, Stevenson DE, Cooney JM, Hellens RP, Allan AC, Hoover EE, Bradeen JM (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11(1):93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, Gallusci P (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228(3):391–399

    Article  CAS  PubMed  Google Scholar 

  • Valledor L, Hasbun R, Meijon M, Rodriguez JL, Santamaria E, Viejo M, Berdasco M, Feito I, Fraga MF, Canal MJ, Rodriguez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Org 91(2):75–86

    Article  CAS  Google Scholar 

  • Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss SH (2012) Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13:27

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang Z, Meng D, Wang A, Li T, Jiang S, Cong P, Li T (2013) The methylation of the PcMYB10 promoter is associated with green-skinned sport in Max Red Bartlett pear. Plant Physiol 162(2):885–896

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu Q, Liu Y, Zhu A, Wu X, Ye J, Yu K, Guo W, Deng X (2010) Discovery and comparative profiling of microRNAs in a sweet orange red-flesh mutant and its wild type. BMC Genomics 11(1):246

    Article  PubMed Central  PubMed  Google Scholar 

  • Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45(1):59–66

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi T, Moritoh S, Johzuka-Hisatomi Y, Ono A, Terada R, Nakamura I, Iida S (2008) Alternative splicing of the rice OsMET1 genes encoding maintenance DNA methyltransferase. J Plant Physiol 165(17):1774–1782

    Article  CAS  PubMed  Google Scholar 

  • Yu K, Xu Q, Da X, Guo F, Ding Y, Deng X (2012) Transcriptome changes during fruit development and ripening of sweet orange (Citrus sinensis). BMC Genomics 13:10

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153(1):193–205

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang H, Zhu JK (2012) Active DNA demethylation in plants and animals. Cold Spring Harb Symp Quant Biol 77:161–173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31(2):154–159

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Cao X, Johansen LK, Xie Z, Carrington JC, Jacobsen SE (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol 14(13):1214–1220

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project was supported by the Ministry of Science and Technology of China (2011CB100600) and the National Natural Science Foundation of China (31272148 and 31222047).

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Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology of Ministry of Education, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

    Jidi Xu, Haidan Xu, Qiang Xu & Xiuxin Deng

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  1. Jidi Xu
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  2. Haidan Xu
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  3. Qiang Xu
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  4. Xiuxin Deng
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Correspondence to Qiang Xu.

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Xu, J., Xu, H., Xu, Q. et al. Characterization of DNA Methylation Variations During Fruit Development and Ripening of Sweet Orange. Plant Mol Biol Rep 33, 1–11 (2015). https://doi.org/10.1007/s11105-014-0732-2

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