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Genome-wide analysis of genes encoding MBD domain-containing proteins from tomato suggest their role in fruit development and abiotic stress responses

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Abstract

In tomato, DNA methylation has an inhibitory effect on fruit ripening. The inhibition of DNA methyltransferase by 5-azacytidine results in premature fruit ripening. Methyl CpG binding domain (MBD) proteins are the readers of DNA methylation marks and help in the recruitment of chromatin-modifying enzymes which affect gene expression. Therefore, we investigate their contribution during fruit development. In this study, we identified and analyzed 18 putative genes of Solanum lycopersicum and Solanum pimpinellifolium encoding MBD proteins. We also identified tomato MBD syntelogs in Capsicum annum and Solanum tuberosum. Sixty-three MBD genes identified from four different species of solanaceae were classified into three groups. An analysis of the conserved domains in these proteins identified additional domains along with MBD motif. The transcript profiling of tomato MBDs in wild-type and two non-ripening mutants, rin and Nr, indicated constructive information regarding their involvement during fruit development. When we performed a stage-specific expression analysis during fruit ripening, a gradual decrease in transcript accumulation in the wild-type fruit was detected. However, a very low expression was observed in the ripening mutants. Furthermore, many ethylene-responsive cis-elements were found in SlMBD gene promoters, and some of them were induced in the presence of exogenous ethylene. Further, we detected the possible role of these MBDs in abiotic stresses. We found that few genes were differentially expressed under various abiotic stress conditions. Our results provide an evidence of the involvement of the tomato MBDs in fruit ripening and abiotic stress responses, which would be helpful in further studies on these genes in tomato fruit ripening.

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References

  1. Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539

    Article  Google Scholar 

  2. Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983–1993

    CAS  PubMed  Google Scholar 

  3. Inamdar NM, Ehrlich KC, Ehrlich M (1991) Cpg methylation inhibits binding of several sequence-specific DNA-binding proteins from pea, wheat, soybean and cauliflower. Plant Mol Biol 17:111–123

    Article  CAS  Google Scholar 

  4. Watt F, Molloy PL (1988) Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 2:1136–1143

    Article  CAS  Google Scholar 

  5. Bird AP, Wolffe AP (1999) Methylation-induced repression–belts, braces, and chromatin. Cell 99:451–454

    Article  CAS  Google Scholar 

  6. Ehrlich KC (1993) Characterization of DBPm, a plant protein that binds to DNA containing 5-methylcytosine. biochimica et biophysica acta 1172:108–116

    Article  CAS  Google Scholar 

  7. Springer NM, Kaeppler SM (2005) Evolutionary divergence of monocot and dicot methyl-CpG-binding domain proteins. Plant Physiol 138:92–104

    Article  CAS  Google Scholar 

  8. Berg A, Meza TJ, Mahic M, Thorstensen T, Kristiansen K, Aalen RB (2003) Ten members of the Arabidopsis gene family encoding methyl-CpG-binding domain proteins are transcriptionally active and at least one, AtMBD11, is crucial for normal development. Nucleic Acids Res 31:5291–5304

    Article  CAS  Google Scholar 

  9. Ohki I, Shimotake N, Fujita N, Jee J, Ikegami T, Nakao M, Shirakawa M (2001) Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105:487–497

    Article  CAS  Google Scholar 

  10. Wakefield RID et al (1999) The solution structure of the domain from MeCP2 that binds to methylated DNA. J Mol Biol 291:1055–1065

    Article  CAS  Google Scholar 

  11. Ito M, Koike A, Koizumi N, Sano H (2003) Methylated DNA-binding proteins from Arabidopsis. Plant Physiol 133:1747–1754

    Article  CAS  Google Scholar 

  12. Zemach A, Grafi G (2003) Characterization of Arabidopsis thaliana methyl-CpG-binding domain (MBD) proteins. Plant J 34:565–572

    Article  CAS  Google Scholar 

  13. Scebba F et al (2003) Arabidopsis MBD proteins show different binding specificities and nuclear localization. Plant Mol Biol 53:755–771

    Article  Google Scholar 

  14. Yano A et al (2006) Interaction between methyl CpG-binding protein and Ran GTPase during cell division in tobacco cultured cells. Ann Bot 98:1179–1187

    Article  CAS  Google Scholar 

  15. Zemach A et al (2005) DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17:1549–1558

    Article  CAS  Google Scholar 

  16. Preuss SB et al (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684

    Article  CAS  Google Scholar 

  17. Parida AP, Sharma A, Sharma AK (2017) AtMBD6, a methyl CpG binding domain protein, maintains gene silencing in Arabidopsis by interacting with RNA binding proteins. J Biosci 42:57–68

    Article  CAS  Google Scholar 

  18. Jones PL et al (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187–191

    Article  CAS  Google Scholar 

  19. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386–389

    Article  CAS  Google Scholar 

  20. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 23:62–66

    Article  CAS  Google Scholar 

  21. Fujita N et al (2003) Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J Biol Chem 278:24132–24138

    Article  CAS  Google Scholar 

  22. Sarraf SA, Stancheva I (2004) Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol Cell 15:595–605

    Article  CAS  Google Scholar 

  23. Wang CL et al (2015) Methyl-CpG-binding domain protein MBD7 is required for active DNA demethylation in Arabidopsis. Plant Physiol 167:905–905

    Article  CAS  Google Scholar 

  24. Lang Z et al (2015) The methyl-CpG-binding protein MBD7 facilitates active DNA demethylation to limit DNA hyper-methylation and transcriptional gene silencing. Mol Cell 57:971–983

    Article  CAS  Google Scholar 

  25. Scebba F, De Bastiani M, Bernacchia G, Andreucci A, Galli A, Pitto L (2007) PRMT11: a new Arabidopsis MBD7 protein partner with arginine methyltransferase activity. Plant J 52:210–222

    Article  CAS  Google Scholar 

  26. Stangeland B et al (2009) AtMBD8 is involved in control of flowering time in the C24 ecotype of Arabidopsis thaliana. Physiol Plant 136:110–126

    Article  CAS  Google Scholar 

  27. Peng M, Cui Y, Bi YM, Rothstein SJ (2006) AtMBD9: a protein with a methyl-CpG-binding domain regulates flowering time and shoot branching in Arabidopsis. Plant J 46:282–296

    Article  CAS  Google Scholar 

  28. Yaish MWF, Peng MS, Rothstein SJ (2009) AtMBD9 modulates Arabidopsis development through the dual epigenetic pathways of DNA methylation and histone acetylation. Plant J 59:123–135

    Article  CAS  Google Scholar 

  29. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  30. Sato S et al (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  CAS  Google Scholar 

  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. 25:402–408

  32. Bolger A et al (2014) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat Genet 46:1034–1038

    Article  CAS  Google Scholar 

  33. Kim S et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–270

    Article  CAS  Google Scholar 

  34. Zhong S et al (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159

    Article  CAS  Google Scholar 

  35. Lincoln JE, Fischer RL (1988) Regulation of gene expression by ethylene in wild-type and rin tomato (Lycopersicon esculentum) Fruit. Plant Physiol 88:370–374

    Article  CAS  Google Scholar 

  36. Yen HC, Lee SY, Tanksley SD, Lanahan MB, Klee HJ, Giovannoni JJ (1995) The tomato never-ripe locus regulates ethylene-inducible gene-expression and is linked to a homolog of the Arabidopsis etr1 gene. Plant Physiol 107:1343–1353

    Article  CAS  Google Scholar 

  37. Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861

    Article  CAS  Google Scholar 

  38. Ohmetakagi M, Shinshi H (1995) Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  CAS  Google Scholar 

  39. Kakutani T, Kato M, Kinoshita T, Miura A (2004) Control of development and transposon movement by DNA methylation in Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 69:139–143

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  41. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408

    Article  CAS  Google Scholar 

  42. Li Q, Wang X, Sun H, Zeng J, Cao Z, Li Y, Qian W (2015) Regulation of active DNA demethylation by a methyl-CpG-binding domain protein in Arabidopsis thaliana. PLoS Genet 11:e1005210

    Article  Google Scholar 

  43. Wu FN, Eannetta NT, Xu YM, Durrett R, Mazourek M, Jahn MM, Tanksley SD (2009) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118:1279–1293

    Article  CAS  Google Scholar 

  44. Aasland R, Gibson TJ, Stewart AF (1995) The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem Sci 20:56–59

    Article  CAS  Google Scholar 

  45. Razin A (1998) CpG methylation, chromatin structure and gene silencing–a three-way connection. EMBO J 17:4905–4908

    Article  CAS  Google Scholar 

  46. Nan X, Bird A (2001) The biological functions of the methyl-CpG-binding protein MeCP2 and its implication in Rett syndrome. Brain Dev 23(Suppl 1):S32–S37

    Article  Google Scholar 

  47. Lyst MJ, Connelly J, Merusi C, Bird A (2016) Sequence-specific DNA binding by AT-hook motifs in MeCP2. FEBS Lett 590:2927–2933

    Article  CAS  Google Scholar 

  48. Aravind L, Landsman D (1998) AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res 26:4413–4421

    Article  CAS  Google Scholar 

  49. Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    Article  CAS  Google Scholar 

  50. Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK (2012) Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Mol Genet Genomics 287:189–203

    Article  CAS  Google Scholar 

  51. Kumar R, Chauhan PK, Khurana A (2016) Identification and expression profiling of DNA methyltransferases during development and stress conditions in Solanaceae. Funct Integr Genomics 16:513–528

    Article  CAS  Google Scholar 

  52. Matarasso N, Schuster S, Avni A (2005) A novel plant cysteine protease has a dual function as a regulator of 1-aminocyclopropane-1-carboxylic Acid synthase gene expression. Plant Cell 17:1205–1216

    Article  CAS  Google Scholar 

  53. Zhao L et al (2009) Molecular evolution of the E8 promoter in tomato and some of its relative wild species. J Biosci 34:71–83

    Article  CAS  Google Scholar 

  54. Liang X, Nazarenus TJ, Stone JM (2008) Identification of a consensus DNA-binding site for the Arabidopsis thaliana SBP domain transcription factor, AtSPL14, and binding kinetics by surface plasmon resonance. Biochemistry 47:3645–3653

    Article  CAS  Google Scholar 

  55. Manning K et al (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    Article  CAS  Google Scholar 

  56. Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ (1995) An ethylene-inducible component of signal transduction encoded by never-ripe. Science 270:1807–1809

    Article  CAS  Google Scholar 

  57. Vrebalov J et al (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346

    Article  CAS  Google Scholar 

  58. Wang WS et al (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960

    Article  CAS  Google Scholar 

  59. Garg R, Narayana Chevala V, Shankar R, Jain M (2015) Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep 5:14922

    Article  CAS  Google Scholar 

  60. Li J et al (2016) Global DNA methylation variations after short-term heat shock treatment in cultured microspores of Brassica napus cv. Topas Sci Rep 6:38401

    Article  CAS  Google Scholar 

  61. Sharma R, Mohan Singh RK, Malik G, Deveshwar P, Tyagi AK, Kapoor S, Kapoor M (2009) Rice cytosine DNA methyltransferases– gene expression profiling during reproductive development and abiotic stress. FEBS J 276:6301–6311

    Article  CAS  Google Scholar 

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Acknowledgements

APP acknowledges the Council of Scientific and Industrial Research (CSIR), India for providing research fellowship. AKS acknowledges the Department of Science and Technology, India, for the Purse Grant. The SAP grant of the University Grants Commission to the Department of Plant Molecular Biology for support of infrastructure is also acknowledged.

Funding

This work was supported by a Purse Grant by the Department of Science and Technology, Government of India.

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AKS: Conceptualized and designed the experiments. APP and RK conducted the data analysis and wrote the manuscript. APP and UR performed gene expression profiling and VS and AP performed the in silico promoter analysis.

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Correspondence to Arun Kumar Sharma.

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The authors declare that they have no conflict of interest.

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Parida, A.P., Raghuvanshi, U., Pareek, A. et al. Genome-wide analysis of genes encoding MBD domain-containing proteins from tomato suggest their role in fruit development and abiotic stress responses. Mol Biol Rep 45, 2653–2669 (2018). https://doi.org/10.1007/s11033-018-4435-x

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