CHH hypermethylation contributes to the early ripening of grapes revealed by DNA methylome landscape of ‘Kyoho’ and its bud mutant

Tong-Lu Wei , Yu-Tong Wan , Hai-Nan Liu , Mao-Song Pei , Guang-Qi He , Da-Long Guo

Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) : 285

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) : 285 DOI: 10.1093/hr/uhae285
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CHH hypermethylation contributes to the early ripening of grapes revealed by DNA methylome landscape of ‘Kyoho’ and its bud mutant

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Abstract

DNA methylation is a stable epigenetic mark that plays a crucial role in plant life processes. However, the specific functions of DNA methylation in grape berry development remain largely unknown. In this study, we performed whole-genome bisulfite sequencing on ‘Kyoho’ grape and its early-ripening bud mutant ‘Fengzao’ at different developmental stages. Our results revealed that transposons (TEs) and gene flanking regions exhibited high levels of methylation, particularly in ‘Fengzao’, attributed to CHH site methylation. Interestingly, the methylation patterns in these two cultivars showed distinct dynamics during berry development. While methylation levels of genes and TEs increased gradually in ‘Kyoho’ throughout berry development, ‘Fengzao’ did not display consistent changes. Notably, ‘Fengzao’ exhibited higher methylation levels in promoters compared to ‘Kyoho’, suggesting that hypermethylation of promoters may contribute to its early ripening phenotype. Integration of methylome and transcriptome data highlighted differentially methylated genes (DMGs) and expressed genes (DEGs) associated with secondary metabolite biosynthesis, with 38 genes identified as potential candidates involved in grape berry development. Furthermore, the study identified a jasmonate-induced oxygenase gene (JOX1) as a negative regulator of ripening in Arabidopsis and grapes, indicating that hypermethylation of JOX1 may play a role in the early ripening of ‘Fengzao’. Overall, our findings provide insights into the distinct DNA methylation patterns during grape berry development, shedding light on the epigenetic regulatory mechanisms underlying the early-ripening bud mutant.

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Tong-Lu Wei, Yu-Tong Wan, Hai-Nan Liu, Mao-Song Pei, Guang-Qi He, Da-Long Guo. CHH hypermethylation contributes to the early ripening of grapes revealed by DNA methylome landscape of ‘Kyoho’ and its bud mutant. Horticulture Research, 2025, 12(1): 285 DOI:10.1093/hr/uhae285

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Acknowledgements

This work was financially supported by National Natural Science Foundation of China (NSFC: 32472662, 32202409), Natural Science Foundation of Henan Province (232300421112), and Ph.D. Research Startup Foundation of Henan University of Science and Technology (13480066).

Author contributions

D.L.G. designed this project. T.L.W. and Y.T.W. conducted experiments and data analysis. T.L.W. collected data and wrote the manuscript. G.Q.H., H.N.L. and M.S.P. assisted in the data analysis. T.L.W., H.N.L., and D.L.G. revised the manuscript. All authors read and approved the final manuscript.

Data Availability

The transcriptome data underlying this article are available in the NCBI SRA repository (https://www.ncbi.nlm.nih.gov/sra/) under the BioProject ID: SRR1557134 and SRR1558172. The data generated or analyzed during this study are included in this article, which may be provided by the corresponding author upon reasonable request.

Conflict of interest statement

The authors declare that they have no competing interests.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Saze H, Tsugane K, Kanno T. et al. DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol. 2012;37:766-84

[2]

Mirouze M, Lieberman-Lazarovich M, Aversano R. et al. Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci USA. 2012;37:5880-5

[3]

He X-J, Chen T, Zhu J-K. Regulation and function of DNA methy-lation in plants and animals. Cell Res. 2011;37:442-65

[4]

Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;37:204-20

[5]

Zhu J-K. Active DNA demethylation mediated by DNA glycosy-lases. Annu Rev Genet. 2009;37:143-66

[6]

Zhou F, Zhou S, Cui S. et al. Effects of TDZ and IBA on DNA methylation during callus induction in pear (Pyrus ussuriensis maxim). Fruit Research. 2023;37:1-8

[7]

Yu H, Zhang C, Lu C. et al. The lemon genome and DNA methy-lome unveil epigenetic regulation of citric acid biosynthesis during fruit development. Hortic Res. 2024;37:uhae005

[8]

Li X, Wang X, Zhang Y. et al. Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications. Hortic Res. 2022;37:uhac013

[9]

Jung AM, Furlong MA, Goodrich JM. et al. Associations between epigenetic age acceleration and microRNA expression among U.S. firefighters. Epigenet Insights. 2023;37:25168657231206301

[10]

Maleknia M, Ahmadirad N, Golab F. et al. DNA methylation in cancer: epigenetic view of dietary and lifestyle factors. Epigenet Insights. 2023;37:25168657231199893

[11]

Jones CA, Tansey WP, Weissmiller AM. Emerging themes in mechanisms of tumorigenesis by SWI/SNF subunit mutation. Epigenet Insights. 2022;37:25168657221115656

[12]

Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014;37:394-408

[13]

Zemach A, Kim MY, Hsieh P-H. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;37:193-205

[14]

Osorio S, Scossa F, Fernie A. Molecular regulation of fruit ripen-ing. Front Plant Sci. 2013;37:198

[15]

Gapper NE, McQuinn RP, Giovannoni JJ. Molecular and genetic regulation of fruit ripening. Plant Mol Biol. 2013;37:575-91

[16]

Mounet F, Moing A, Garcia V. et al. Gene and metabolite regula-tory network analysis of early developing fruit tissues highlights new candidate genes for the control of tomato fruit composition and development. Plant Physiol. 2009;37:1505-28

[17]

Wei W, Yang Y-y, Wu C-j. et al. MaSPL 16 positively regulates fruit ripening in bananas via the direct transcriptional induction of MaNAC029. Horticulture Advances. 2023;37:

[18]

Huang H, Liu R, Niu Q. et al. Global increase in DNA methylation during orange fruit development and ripening. Proc Natl Acad Sci USA. 2019;37:1430-6

[19]

Lang Z, Wang Y, Tang K. 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 USA. 2017;37:E4511-9

[20]

Manning K, Tör M, Poole M. et al. A naturally occurring epi-genetic mutation in a gene encoding an SBP-box transcrip-tion factor inhibits tomato fruit ripening. Nat Genet. 2006;37:948-52

[21]

Zhong S, Fei Z, Chen Y-R. et al. Single-base resolution methy-lomes of tomato fruit development reveal epigenome modifica-tions associated with ripening. Nat Biotechnol. 2013;37:154-9

[22]

Cao D, Ju Z, Gao C. et al. Genome-wide identification of cytosine-5 DNA methyltransferases and demethylases in Solanum lycoper-sicum. Gene. 2014;37:230-7

[23]

Liu R, How-Kit A, Stammitti L. et al. A DEMETER-like DNA demethylase governs tomato fruit ripening. Proc Natl Acad Sci USA. 2015;37:10804-9

[24]

Jiang S, Wang N, Chen M. et al. Methylation of MdMYB1 locus mediated by RdDM pathway regulates anthocyanin biosynthesis in apple. Plant Biotechnol J. 2020;37:1736-48

[25]

Xing L, Li Y, Qi S. et al. Comparative RNA-sequencing and DNA methylation analyses of apple (Malus domestica Borkh.) buds with diverse flowering capabilities reveal novel insights into the regulatory mechanisms of flower bud formation. Plant Cell Physiol. 2019;37:1702-21

[26]

Cheng J, Niu Q, Zhang B. et al. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018;37:1-14

[27]

He GQ, Huang XX, Pei MS. et al. Dissection of the pearl of Csaba pedigree identifies key genomic segments related to early ripening in grape. Plant Physiol. 2023;37:1153-66

[28]

Guo D, Wang Z, Li Q. et al. Hydrogen peroxide treatment pro-motes early ripening of Kyoho grape. Aust J Grape Wine R. 2019;37:357-62

[29]

Jia H, Zhang C, Pervaiz T. et al. Jasmonic acid involves in grape fruit ripening and resistant against Botrytis cinerea. Funct Integr Genomics. 2015;37:79-94

[30]

Li Z, Chen C, Zou D. et al. Ethylene accelerates grape ripening via increasing VvERF75-induced ethylene synthesis and chlorophyll degradation. Fruit Research. 2023;37:1-9

[31]

Li YM, Zhang HX, Tang XS. et al. Abscisic acid induces DNA methylation alteration in genes related to berry ripening and stress response in grape (Vitis vinifera L). J Agric Food Chem. 2024;37:15027-39

[32]

Shangguan L, Fang X, Jia H. et al. Characterization of DNA methylation variations during fruit development and ripening of Vitis vinifera ( cv. ‘Fujiminori’). Physiol Mol Biol Plants. 2020;37:617-37

[33]

Jia H, Zhang Z, Zhang S. et al. Effect of the methylation level on the grape fruit development process. J Agric Food Chem. 2020;37:2099-115

[34]

Magris G, Di Gaspero G, Marroni F. et al. Genetic, epigenetic and genomic effects on variation of gene expression among grape varieties. Plant J. 2019;37:895-909

[35]

Guo D-L, Wang Z-G, Pei M-S. et al. Transcriptome analysis reveals mechanism of early ripening in Kyoho grape with hydrogen peroxide treatment. BMC Genomics. 2020;37:1-18

[36]

Guo D-L, Yu Y-H, Xi F-F. et al. Histological and molecular char-acterization of grape early ripening bud mutant. Int J Genomics. 2016;37:5620106

[37]

Guo D-L, Xi F-F, Yu Y-H. et al. Comparative RNA-Seq profiling of berry development between table grape ‘Kyoho’ and its early-ripening mutant ‘Fengzao’. BMC Genomics. 2016;37:1-17

[38]

Coombe BG. Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine R. 1995;37:104-10

[39]

Giovannoni J, Nguyen C, Ampofo B. et al. The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Plant Biol. 2017;37:61-84

[40]

Jia H, Zuo Q, Sadeghnezhad E. et al. HDAC 19 recruits ERF4 to the MYB5a promoter and diminishes anthocyanin accumulation during grape ripening. Plant J. 2022;37:127-44

[41]

Lister R, O’Malley RC, Tonti-Filippini J. et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;37:523-36

[42]

Teyssier E, Bernacchia G, Maury S. et al. Tissue dependent vari-ations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta. 2008;37:391-9

[43]

Aufsatz W, Mette MF, et al.Van Der Winden J. RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci USA. 2002;37:16499-506

[44]

Zuo J, Grierson D, Courtney LT. et al. Relationships between genome methylation, levels of non-coding RNAs, mRNAs and metabolites in ripening tomato fruit. Plant J. 2020;37:980-94

[45]

Wang Y, Zuo L, Wei T. et al. CHH methylation of genes associated with fatty acid and jasmonate biosynthesis contributes to cold tolerance in autotetraploids of Poncirus trifoliata. J Integr Plant Biol. 2022;37:2327-43

[46]

Feng S, Jiang X, Huang Z. et al. DNA methylation remodeled amino acids biosynthesis regulates flower senescence in carna-tion (Dianthus caryophyllus). New Phytol. 2024;37:1605-20

[47]

Wang ZG, Guo LL, Ji XR. et al. Transcriptional analysis of the early ripening of ’Kyoho’ grape in response to the treatment of riboflavin. Genes. 2019;37:514

[48]

Farrow SC, Facchini PJ.Functional diversity of 2-oxoglutarate/Fe (II)-dependent dioxygenases in plant metabolism. Front Plant Sci. 2014;37:524

[49]

Zhang M, Li W, Zhang T. et al. Botrytis cinerea-induced F-box protein 1 enhances disease resistance by inhibiting JAO/JOX-mediated jasmonic acid catabolism in Arabidopsis. Mol Plant. 2024;37:297-311

[50]

Ding Q, Wang F, Xue J. et al. Identification and expression analy-sis of hormone biosynthetic and metabolism genes in the 2OGD family for identifying genes that may be involved in tomato fruit ripening. Int J Mol Sci. 2020;37:5344

[51]

Zhang X, Wang D, Elberse J. et al. Structure-guided analysis of Arabidopsis JASMONATE-INDUCED OXYGENASE (JOX) 2 reveals key residues for recognition of jasmonic acid substrate by plant JOXs. Mol Plant. 2021;37:820-8

[52]

Caarls L, Elberse J, Awwanah M. et al. Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc Natl Acad Sci USA. 2017;37:6388-93

[53]

Li M, Yan Y, Zeng L. et al. Methyl jasmonate activated regula-tory module Ma14-3-3e-MbHLH130-MbACO13/MbACS 7 promot-ing ethylene biosynthesis and fruit ripening in banana. Posthar-vest Biol Technol. 2025;37:113215

[54]

Wasternack C, Song S. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcrip-tion. JExp Bot. 2017;37:1303-21

[55]

Li Y, Li Y, Liu Y. et al. The sHSP22 heat shock protein requires the ABI1 protein phosphatase to modulate polar auxin transport and downstream responses. Plant Physiol. 2018;37:2406-25

[56]

Ji XR, Yu YH, Ni PY. et al. Genome-wide identification of small heat-shock protein (HSP20) gene family in grape and expres-sion profile during berry development. BMC Plant Biol. 2019; 19:433

[57]

Zhang C, Zhang Y, Su Z. et al. Integrated analysis of HSP 20 genes in the developing flesh of peach: identification, expres-sion profiling, and subcellular localization. BMC Plant Biol. 2023; 23:663

[58]

Gerós H, Lionetti V, Raiola A. et al. The grapevine VvPMEI 1 gene encodes a novel functional pectin methylesterase inhibitor associated to grape berry development. PLoS One. 2015;37:e0133810

[59]

Wang W, Zheng X, Liu S. et al. Polyamine oxidase (PAO)-mediated polyamine catabolism plays potential roles in peach (Prunus persica L.) fruit development and ripening. Tree Genet Genom. 2021;37:10

[60]

Cuellar T, Azeem F, Andrianteranagna M. et al. Potassium transport in developing fleshy fruits: the grapevine inward K+ channel VvK1.2 is activated by CIPK-CBL complexes and induced in ripening berry flesh cells. Plant J. 2013;37:1006-18

[61]

Forlani S, Masiero S, Mizzotti C. Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. JExp Bot. 2019;37:2993-3006

[62]

Hou B-Z, Xu C, Shen Y-Y. A leu-rich repeat receptor-like pro-tein kinase, FaRIPK1, interacts with the ABA receptor, FaABAR, to regulate fruit ripening in strawberry. JExp Bot. 2018;37:1569-82

[63]

Zyprian E, Ochßner I, Schwander F. et al. Quantitative trait loci affecting pathogen resistance and ripening of grapevines. Mol Gen Genomics. 2016;37:1573-94

[64]

Krueger F, Andrews SR. Bismark: a flexible aligner and methyla-tion caller for bisulfite-Seq applications. Bioinformatics. 2011;37:1571-2

[65]

Xu J, Zhou S, Gong X. et al. Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J. 2018;37:672-87

[66]

Feng H, Conneely KN, Wu H. A Bayesian hierarchical model to detect differentially methylated loci from single nucleotide resolution sequencing data. Nucleic Acids Res. 2014;37:e69

[67]

Clough SJ, Bent AF. Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;37:735-43

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