Identification of DNA methyltransferases and demethylases in Solanum melongena L., and their transcription dynamics during fruit development and after salt and drought stresses

Autoři: Andrea Moglia aff001;  Silvia Gianoglio aff001;  Alberto Acquadro aff001;  Danila Valentino aff001;  Anna Maria Milani aff001;  Sergio Lanteri aff001;  Cinzia Comino aff001
Působiště autorů: Department of Agricultural, Forest and Food Sciences, Plant Genetics and Breeding, University of Torino, Grugliasco, Italy aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


DNA methylation through the activity of cytosine-5-methyltransferases (C5-MTases) and DNA demethylases plays important roles in genome protection as well as in regulating gene expression during plant development and plant response to environmental stresses. In this study, we report on a genome-wide identification of six C5-MTases (SmelMET1, SmelCMT2, SmelCMT3a, SmelCMT3b, SmelDRM2, SmelDRM3) and five demethylases (SmelDemethylase_1, SmelDemethylase_2, SmelDemethylase_3, SmelDemethylase_4, SmelDemethylase_5) in eggplant. Gene structural characteristics, chromosomal localization and phylogenetic analyses are also described. The transcript profiling of both C5-MTases and demethylases was assessed at three stages of fruit development in three eggplant commercial F1 hybrids: i.e. ‘Clara’, ‘Nite Lady’ and ‘Bella Roma’, representative of the eggplant berry phenotypic variation. The trend of activation of C5-MTases and demethylase genes varied in function of the stage of fruit development and was genotype dependent. The transcription pattern of C5MTAses and demethylases was also assessed in leaves of the F1 hybrid ‘Nite Lady’ subjected to salt and drought stresses. A marked up-regulation and down-regulation of some C5-MTases and demethylases was detected, while others did not vary in their expression profile. Our results suggest a role for both C5-MTases and demethylases during fruit development, as well as in response to abiotic stresses in eggplant, and provide a starting framework for supporting future epigenetic studies in the species.

Klíčová slova:

Arabidopsis thaliana – DNA methylation – Fruits – Phylogenetic analysis – Plant resistance to abiotic stress – Protein domains – Solanum – Tomatoes


1. Finnegan EJ, Peacock WJ, Dennis ES. DNA methylation, a key regulator of plant development and other processes. Current Opinion in Genetics and Development. 2000. doi: 10.1016/S0959-437X(00)00061-7

2. Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008; doi: 10.1016/j.cell.2008.03.029 18423832

3. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008; doi: 10.1038/nature06745 18278030

4. Henikoff S, Comai L. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics. 1998;

5. Sudan J, Raina M, Singh R. Plant epigenetic mechanisms: role in abiotic stress and their generational heritability. 3 Biotech. 2018. doi: 10.1007/s13205-018-1202-6 29556426

6. Du J, Zhong X, Bernatavichute Y V., Stroud H, Feng S, Caro E, et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell. 2012; doi: 10.1016/j.cell.2012.07.034 23021223

7. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics. 2010. doi: 10.1038/nrg2719 20142834

8. Zhang H, Lang Z, Zhu JK. Dynamics and function of DNA methylation in plants. Nature Reviews Molecular Cell Biology. 2018. doi: 10.1038/s41580-018-0016-z 29784956

9. Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol. 2014; doi: 10.1038/nsmb.2735 24336224

10. Yaari R, Katz A, Domb K, Harris KD, Zemach A, Ohad N. RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs. Nat Commun. 2019; doi: 10.1038/s41467-019-09496-0 30962443

11. Saze H, Tsugane K, Kanno T, Nishimura T. DNA methylation in plants: Relationship to small rnas and histone modifications, and functions in transposon inactivation. Plant and Cell Physiology. 2012. doi: 10.1093/pcp/pcs008 22302712

12. Takuno S, Gaut BS. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc Natl Acad Sci. 2013; doi: 10.1073/pnas.1215380110 23319627

13. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim K Do, Li Q, et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 2016; doi: 10.1186/s13059-016-1059-0 27671052

14. Choi J, Lyons DB, Kim MY MJ and, D Z. DNA methylation and histone H1 cooperatively repress transposable elements and aberrant intragenic transcripts. bioRxiv. 2019;

15. Tran RK, Henikoff JG, Zilberman D, Ditt RF, Jacobsen SE, Henikoff S. DNA methylation profiling identifies CG methylation clusters in Arabidopsis genes. Curr Biol. 2005; doi: 10.1016/j.cub.2005.01.008 15668172

16. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet. 2006; doi: 10.1038/ng1841 16832354

17. Gallusci P, Hodgman C, Teyssier E, Seymour GB. DNA Methylation and Chromatin Regulation during Fleshy Fruit Development and Ripening. Front Plant Sci. 2016; doi: 10.3389/fpls.2016.00807 27379113

18. Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol. 2013; doi: 10.1038/nbt.2462 23354102

19. Candaele J, Demuynck K, Mosoti D, Beemster GTS, Inze D, Nelissen H. Differential Methylation during Maize Leaf Growth Targets Developmentally Regulated Genes. PLANT Physiol. 2014; doi: 10.1104/pp.113.233312 24488968

20. Xing M-Q, Zhang Y-J, Zhou S-R, Hu W-Y, Wu X-T, Ye Y-J, et al. Global Analysis Reveals the Crucial Roles of DNA Methylation during Rice Seed Development. Plant Physiol. 2015; doi: 10.1104/pp.15.00414 26145151

21. Li Y, Kumar S, Qian W. Active DNA demethylation: mechanism and role in plant development. Plant Cell Reports. 2018. doi: 10.1007/s00299-017-2215-z 29026973

22. Kawanabe T, Ishikura S, Miyaji N, Sasaki T, Wu LM, Itabashi E, et al. Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc Natl Acad Sci. 2016; doi: 10.1073/pnas.1613372113 27791039

23. Lauss K, Wardenaar R, Oka R, van Hulten MHA, Guryev V, Keurentjes JJB, et al. Parental DNA methylation states are associated with heterosis in epigenetic hybrids. Plant Physiol. 2017; doi: 10.1104/pp.17.01054 29196538

24. Liu R, How-Kit A, Stammitti L, Teyssier E, Rolin D, Mortain-Bertrand A, et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc Natl Acad Sci. 2015; doi: 10.1073/pnas.1503362112 26261318

25. Conde D, Moreno-Cortés A, Dervinis C, Ramos-Sánchez JM, Kirst M, Perales M, et al. Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant Cell Environ. 2017; doi: 10.1111/pce.13056 28810288

26. Chinnusamy V, Zhu JK. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology. 2009. doi: 10.1016/j.pbi.2008.12.006 19179104

27. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, et al. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci. 2012; doi: 10.1073/pnas.1209329109 22733782

28. Shaik R, Ramakrishna W. Bioinformatic Analysis of Epigenetic and MicroRNA Mediated Regulation of Drought Responsive Genes in Rice. PLoS One. 2012; doi: 10.1371/journal.pone.0049331 23145152

29. Uthup TK, Ravindran M, Bini K, Thakurdas S. Divergent DNA methylation patterns associated with abiotic stress in hevea brasiliensis. Mol Plant. 2011; doi: 10.1093/mp/ssr039 21705581

30. Ashapkin V V., Kutueva LI, Vanyushin BF. Plant DNA methyltransferase genes: Multiplicity, expression, methylation patterns. Biochem. 2016; doi: 10.1134/S0006297916020085 27260394

31. Ahmad F, Huang X, Lan HX, Huma T, Bao YM, Huang J, et al. Comprehensive gene expression analysis of the DNA (cytosine-5) methyltransferase family in rice (Oryza sativa L.). Genet Mol Res. 2014; doi: 10.4238/2014.July.7.9 25061741

32. Cao D, Ju Z, Gao C, Mei X, Fu D, Zhu H, et al. Genome-wide identification of cytosine-5 DNA methyltransferases and demethylases in Solanum lycopersicum. Gene. 2014; doi: 10.1016/j.gene.2014.08.034 25149677

33. Garg R, Kumari R, Tiwari S, Goyal S. Genomic survey, gene expression analysis and structural modeling suggest diverse roles of DNA methyltransferases in legumes. PLoS One. 2014; doi: 10.1371/journal.pone.0088947 24586452

34. Qian Y, Xi Y, Cheng B, Zhu S. Genome-wide identification and expression profiling of DNA methyltransferase gene family in maize. Plant Cell Rep. 2014; doi: 10.1007/s00299-014-1645-0

35. Wang P, Gao C, Bian X, Zhao S, Zhao C, Xia H, et al. Genome-Wide Identification and Comparative Analysis of Cytosine-5 DNA Methyltransferase and Demethylase Families in Wild and Cultivated Peanut. Front Plant Sci. 2016; doi: 10.3389/fpls.2016.00007 26870046

36. Gianoglio S, Moglia A, Acquadro A, Comino C, Portis E. The genome-wide identification and transcriptional levels of DNA methyltransferases and demethylases in globe artichoke. PLoS One. 2017; doi: 10.1371/journal.pone.0181669 28746368

37. Bernacchia G, Primo A, Giorgetti L, Pitto L, Cella R. Carrot DNA-methyltransferase is encoded by two classes of genes with differing patterns of expression. Plant J. 1998; doi: 10.1046/j.1365-313X.1998.00034.x 9680985

38. Giannino D, Mele G, Cozza R, Bruno L, Testone G, Ticconi C, et al. Isolation and characterization of a maintenance DNA-methyltransferase gene from peach (Prunus persica [L.] Batsch): Transcript localization in vegetative and reproductive meristems of triple buds. J Exp Bot. 2003; doi: 10.1093/jxb/erg292 14563834

39. Gu T, Ren S, Wang Y, Han Y, Li Y. Characterization of DNA methyltransferase and demethylase genes in Fragaria vesca. Mol Genet Genomics. 2016; doi: 10.1007/s00438-016-1187-y 26956009

40. Rival A, Jaligot E, Beulé T, Finnegan EJ. 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. 2008; doi: 10.1093/jxb/ern178 18640997

41. Victoria D, Aliki K, Venetia K, Georgios M, Zoe H. Spatial and temporal expression of cytosine-5 DNA methyltransferase and DNA demethylase gene families of the Ricinus communis during seed development and drought stress. Plant Growth Regul. 2018; doi: 10.1007/s10725-017-0323-y

42. Dai Y, Ni Z, Dai J, Zhao T, Sun Q. Isolation and expression analysis of genes encoding DNA methyltransferase in wheat (Triticum aestivum L.). Biochim Biophys Acta—Gene Struct Expr. 2005; doi: 10.1016/j.bbaexp.2005.04.001 15946751

43. Barchi L, Pietrella M, Venturini L, Minio A, Toppino L, Acquadro A, Andolfo G, Aprea G, Avanzato C, Bassolino L, et al. A chromosome-anchored eggplant genome sequence reveals key events in Solanaceae evolution. Sci. Rep. 2019 doi: 10.1038/s41598-019-47985-w 31409808

44. Zhou X, Liu J, Zhuang Y. Selection of appropriate reference genes in eggplant for quantitative gene expression studies under different experimental conditions. Sci Hortic (Amsterdam). 2014; doi: 10.1016/j.scienta.2014.07.010

45. Cerruti, E., Comino, C., Catoni, M., Barchi, L., Valentino, D., Gisbert, C., Prohens, J., Portis, E., Lanteri S. Integrated Dna methylome and transcriptome analyses highlight epigenomic changes in grafted eggplant plants. In: SIGA, editor. LXII SIGA Annual Congress Verona. Verona; 2018. p. 6.01.

46. Wang H, Beyene G, Zhai J, Feng S, Fahlgren N, Taylor NJ, et al. CG gene body DNA methylation changes and evolution of duplicated genes in cassava. Proc Natl Acad Sci. 2015; doi: 10.1073/pnas.1519067112 26483493

47. Wang L, Shi Y, Chang X, Jing S, Zhang Q, You C, et al. DNA methylome analysis provides evidence that the expansion of the tea genome is linked to TE bursts. Plant Biotechnology Journal. 2018. doi: 10.1111/pbi.13018 30256509

48. Kumar R, Chauhan PK, Khurana A. Identification and expression profiling of DNA methyltransferases during development and stress conditions in Solanaceae. Funct Integr Genomics. 2016; doi: 10.1007/s10142-016-0502-3 27380018

49. Lang Z, Wang Y, Tang K, Tang D, Datsenka T, Cheng J, et al. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci. 2017; doi: 10.1073/pnas.1705233114 28507144

50. Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017; doi: 10.1038/ng.3886 28581499

51. Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, et al. Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta. 2008; doi: 10.1007/s00425-008-0743-z 18488247

52. Cheng J, Niu Q, Zhang B, Chen K, Yang R, Zhu JK, Zhang YLZ. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018;19: 212. doi: 10.1186/s13059-018-1587-x 30514401

53. Xu J, Xu H, Xu Q, Deng X. Characterization of DNA methylation variations during fruit development and ripening of sweet orange. Plant Mol Biol Report. 2015; doi: 10.1007/s11105-014-0732-2

54. Wang L, Xie J, Hu J, Lan B, You C, Li F, et al. Comparative epigenomics reveals evolution of duplicated genes in potato and tomato. Plant J. 2018; doi: 10.1111/tpj.13790 29178145

55. El-Sharkawy I, Liang D, Xu K. 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. 2015; doi: 10.1093/jxb/erv433 26417021

56. Al-Lawati A, Al-Bahry S, Victor R, Al-Lawati AH, Yaish MW. Salt stress alters DNA methylation levels in alfalfa (Medicago spp). Genet Mol Res. 2016; doi: 10.4238/gmr.15018299 26985924

57. Wang B, Fu R, Zhang M, Ding Z, Chang L, Zhu X, et al. Analysis of methylation-sensitive amplified polymorphism in different cotton accessions under salt stress based on capillary electrophoresis. Genes and Genomics. 2015; doi: 10.1007/s13258-015-0301-6

58. Wang W, Huang F, Qin Q, Zhao X, Li Z, Fu B. Comparative analysis of DNA methylation changes in two rice genotypes under salt stress and subsequent recovery. Biochem Biophys Res Commun. 2015; doi: 10.1016/j.bbrc.2015.08.089 26319557

59. Wibowo A, Becker C, Marconi G, Durr J, Price J, Hagmann J, et al. Hyperosmotic stress memory in arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by dna glycosylase activity. Elife. 2016; doi: 10.7554/eLife.13546 27242129

60. Liu C, Li H, Lin J, Wang Y, Xu X, Max Cheng ZM, et al. Genome-wide characterization of DNA demethylase genes and their association with salt response in pyrus. Genes (Basel). 2018; doi: 10.3390/genes9080398 30082643

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden