Epigenetic orchestration of sugar signaling in plant development and stress adaptation

Abstract

Sugars are not only metabolites but also signals that gate plant growth, fruit ripening, and stress responses. Carbon-sensing pathways (HEXOKINASE 1, TOR-SnRK1, and the sucrose Trehalose-6-phosphate pathway) reprogram gene expression by engaging DNA methylation, histone modification, chromatin remodeling, regulatory RNAs, and RNA modifications. Cutting-edge quantitative epigenomic and epitranscriptomic methods, integrated with novel bioinformatics tools, are driving unprecedented resolution in epigenetic landscape analysis. Benefitting from state-of-the-art technologies, we summarize epigenetic control points for pigmentation, softening, sugar–acid balance, and stress acclimation (e.g. SlDML2, PH5, RdDM-ABA modules). This synthesis underscores that decoding the sugar–epigenome interplay is key to understanding plant phenotypic plasticity and improving crop performance. Finally, we explore how leveraging epigenetic regulation via CRISPR-based epigenome editing, transgenerational inheritance patterns, and epigenomic biomarker-based (epibreeding) approaches holds promise for improving crop resilience and productivity.

References

[1] Tirnaz S, Batley J . Epigenetics: potentials and challenges in crop breeding. Mol Plant. 2019; 12: 1309-11

[2] Norouzitallab P, Baruah K, Vanrompay D, et al. Can epigenetics translate environmental cues into phenotypes? Sci Total Environ . 2019; 647: 1281-93

[3] Lloyd JPB, Lister R . Epigenome plasticity in plants. Nat Rev Genet. 2022; 23: 55-68

[4] Misra V, Mall AK, Ansari SA, et al. Sugar transporters, sugar-metabolizing enzymes, and their interaction with phytohormones in sugarcane. J Plant Growth Regul. 2023; 42: 4975-88

[5] Yang X, Todd J, Arundale R, et al. Identifying loci controlling fiber composition in polyploid sugarcane (Saccharum spp.) through genome-wide association study . Ind Crop Prod. 2019; 130: 598-605

[6] Nakamura M, Gao Y, Dominguez AA, et al. CRISPR technologies for precise epigenome editing. Nat Cell Biol. 2021; 23: 11-22

[7] Willyard C . An epigenetics gold rush: new controls for gene expression. Nature. 2017; 542: 406-8

[8] Alleman M, Sidorenko L, McGinnis K, et al. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature. 2006; 442: 295-8

[9] Cao S, Wang L, Han T, et al. Small RNAs mediate transgenerational inheritance of genome-wide trans-acting epialleles in maize. Genome Biol. 2022; 23: 1-25

[10] Ritter EJ, Niederhuth CE . Intertwined evolution of plant epigenomes and genomes. Curr Opin Plant Biol. 2021; 61: 101990

[11] Li X, Xiong X, Yi C . Epitranscriptome sequencing technologies: decoding RNA modifications. Nat Methods. 2016; 14: 23-31

[12] Moshitch-Moshkovitz S, Dominissini D, Rechavi G . The epitranscriptome toolbox. Cell. 2022; 185: 764-76

[13] Xiong X, Yi C, Peng J . Epitranscriptomics: toward a better understanding of RNA modifications. Genomics Proteomics Bioinformatics. 2017; 15: 147-53

[14] Cerneckis J, Ming G-L, Song H, et al. The rise of epitranscriptomics: recent developments and future directions. Trends Pharmacol Sci. 2024; 45: 24-38

[15] Can SN, Nunn A, Galanti D, et al. The epidiverse plant epigenome-wide association studies (Ewas) pipeline. Epigenomes. 2021; 5: 12

[16] Lu Y, Bu Q, Chuan M, et al. Metabolic regulation of the plant epigenome. Plant J. 2023; 114: 1001-13

[17] Hüther P, Hagmann J, Nunn A, et al. MethylScore, a pipeline for accurate and context-aware identification of differentially methylated regions from population-scale plant whole-genome bisulfite sequencing data. Quant Plant Biol. 2022; 3: e19

[18] Colicchio JM, Amstutz CL, Garcia N, et al. A tool for rapid, automated characterization of population epigenomics in plants. Sci Rep. 2023; 13: 1-11

[19] Wanga MA, Shimelis H, Mashilo J, et al. Opportunities and challenges of speed breeding: a review. Plant Breed. 2021; 140: 185-94

[20] Ni P, Huang N, Nie F, et al. Genome-wide detection of cytosine methylations in plant from nanopore data using deep learning. Nat Commun. 2021; 12: 1-11

[21] Song M, Zhao J, Zhang C, et al. PEA-m6A: an ensemble learning framework for accurately predicting N6-methyladenosine modifications in plants. Plant Physiol. 2024; 195: 1200-13

[22] Song J, Zhai J, Bian E, et al. Transcriptome-wide annotation of m5C RNA modifications using machine learning. Front Plant Sci. 2018; 9: 519

[23] Zhai J, Song J, Zhang T, et al. deepEA: a containerized web server for interactive analysis of epitranscriptome sequencing data. Plant Physiol. 2021; 185: 29-33

[24] Zhang Z, Zhan Q, Eckert M, et al. RADAR: differential analysis of MeRIP-seq data with a random effect model. Genome Biol. 2019; 20: 294

[25] Pratanwanich PN, Yao F, Chen Y, et al. Identification of differential RNA modifications from nanopore direct RNA sequencing with xPore. Nat Biotechnol. 2021; 39: 1394-402

[26] Acera Mateos P, J Sethi A, Ravindran A, et al. Prediction of m6A and m5C at single-molecule resolution reveals a transcriptome-wide co-occurrence of RNA modifications. Nat Commun. 2024; 15: 1-17

[27] Farmer A, Thibivilliers S, Ryu KH, et al. Single-nucleus RNA and ATAC sequencing reveals the impact of chromatin accessibility on gene expression in Arabidopsis roots at the single-cell level. Mol Plant. 2021; 14: 372-83

[28] Grones C, Eekhout T, Shi D, et al. Best practices for the execution, analysis, and data storage of plant single-cell/nucleus transcriptomics. Plant Cell. 2024; 36: 812-28

[29] Li X, Chen L, Zhang Q, et al. BRIF-Seq: bisulfite-converted randomly integrated fragments sequencing at the single-cell level. Mol Plant. 2019;12:438-46

[30] Buenrostro JD, Wu B, Chang HY, et al. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr Protoc Mol Biol. 2015; 109: 21.29.1-9

[31] Cui Y, Su Y, Bian J, et al. Single-nucleus RNA and ATAC sequencing analyses provide molecular insights into early pod development of peanut fruit. Plant Commun. 2024; 5: 100979

[32] Zhang X, Luo Z, Marand AP, et al. A spatially resolved multi-omic single-cell atlas of soybean development. Cell. 2025; 188: 550-567.e19

[33] Ouyang W, Luan S, Xiang X, et al. Profiling plant histone modification at single-cell resolution using snCUT&tag. Plant Biotechnol J. 2022; 20: 420-2

[34] Zhou S, Jiang W, Zhao Y, et al. Single-cell three-dimensional genome structures of rice gametes and unicellular zygotes. Nat Plants. 2019; 5: 795-800

[35] Wiener D, Schwartz S . The epitranscriptome beyond m6A. Nat Rev Genet. 2021; 22: 119-31

[36] Xue Y, Zou C, Zhang C, et al. Dynamic DNA methylation changes reveal tissue-specific gene expression in sugarcane. Front Plant Sci. 2022; 13: 1036764

[37] Gladman N, Hufnagel B, Regulski M, et al. Sorghum root epigenetic landscape during limiting phosphorus conditions. Plant Direct. 2022; 6: e393

[38] Guo S, Ji Y, Zheng Y, et al. Transcriptomic, metabolomic, and ATAC-seq analysis reveal the regulatory mechanism of senescence of post-harvest tomato fruit. Front Plant Sci. 2023; 14: 1142913

[39] Ren C, Li H, Wang Z, et al. Characterization of chromatin accessibility and gene expression upon cold stress reveals that the RAV1 transcription factor functions in cold response in Vitis amurensis . Plant Cell Physiol. 2021; 62: 1615-29

[40] Gallego-Bartolomé J, Liu W, Kuo PH, et al. Co-targeting RNA polymerases IV and V promotes efficient de novo DNA methylation in Arabidopsis . Cell. 2019; 176: 1068-1082.e19

[41] Zheng Y, He R . Targeted DNA demethylation of the Arabidopsis genome using the SunTag-dCpf1-TET1cd system. MicroPubl Biol. 2023; 2023: 10.17912/micropub.biology.000814

[42] Liu L, Wang W, Lu X, et al. Methyl-sensitive amplification polymorphism (MSAP) analysis provides insights into the DNA methylation changes underlying adaptation to low temperature of Brassica rapa L. Plants. 2024; 13: 1748

[43] Liu G, Wang J, Hou X . Transcriptome-wide N6-methyladenosine (m6A) methylome profiling of heat stress in Pak-choi (Brassica rapa ssp. chinensis) . Plants. 2020; 9: 1080

[44] Huang W, Tan C, Guo H . Ethylene in fruits: beyond ripening control. Hortic Res. 2024; 11: uhae229

[45] Pei H, Li Y, Liu Y, et al. Chromatin accessibility landscapes revealed the subgenome-divergent regulation networks during wheat grain development. aBIOTECH. 2023; 4: 8-19

[46] Ghoshal B, Picard CL, Vong B, et al. CRISPR-based targeting of DNA methylation in Arabidopsis thaliana by a bacterial CG-specific DNA methyltransferase. Proc Natl Acad Sci U S A. 2021; 118: e2125016118

[47] Matzke MA, Mosher RA . RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014; 15: 394-408

[48] Ye R, Wang M, du H, et al. Glucose-driven TOR-FIE-PRC2 signalling controls plant development. Nature. 2022; 609: 986-93

[49] Li T, Chen X, Zhong X, et al. Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27 trimethylation is involved in defense-related gene activation in rice. Plant Cell. 2013; 25: 4725-36

[50] Li Z, Wang Z, Wang C, et al. LATERAL FLORET 2 encoding a sucrose non-fermenting 2 chromatin remodeling factor regulates axillary meristem of spikelet development in rice (Oryza sativa) . New Phytol. 2025; 246: 598-615

[51] Wang J, Wang J, Li Y, et al. Epigenomic mechanism regulating the quality and ripeness of apple fruit with differing harvest maturity. Physiol Plant. 2024; 176: e14278

[52] Liu Y, Bai Y, Li N, et al. HEXOKINASE1 forms a nuclear complex with the PRC2 subunits CURLY LEAF and SWINGER to regulate glucose signaling. J Integr Plant Biol. 2022; 64: 1168-80

[53] Heisel TJ, Li CY, Grey KM, et al. Mutations in HISTONE ACETYLTRANSFERASE1 affect sugar response and gene expression in Arabidopsis . Front Plant Sci. 2013; 4: 245

[54] Pasternak T, Kircher S, Palme K, et al. Regulation of early seedling establishment and root development in Arabidopsis thaliana by light and carbohydrates. Planta. 2023; 258: 76

[55] Jamsheer KM, Jindal S, Sharma M, et al. A negative feedback loop of TOR signaling balances growth and stress-response trade-offs in plants. Cell Rep. 2022; 39: 110631

[56] An C, Liu Z, Pan X, et al. Effect of histone modifications on fruit ripening. Physiol Plant. 2024; 176: e14639

[57] Peng M, Li Z, Zhou N, et al. Linking PHYTOCHROME-INTERACTING FACTOR to histone modification in plant shade avoidance. Plant Physiol. 2018; 176: 1341-51

[58] Kim JM, Sasaki T, Ueda M, et al. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci. 2015; 6: 124925

[59] Swapna M, Kumar S . MicroRNAs and their regulatory role in sugarcane. Front Plant Sci. 2017; 8: 997

[60] Tian L, Liu H, Ren L, et al. MicroRNA 399 as a potential integrator of photo-response, phosphate homeostasis, and sucrose signaling under long day condition. BMC Plant Biol. 2018; 18: 290

[61] Xu M, Hu T, Smith MR, et al. Epigenetic regulation of vegetative phase change in Arabidopsis . Plant Cell. 2016; 28: 28-41

[62] Azad MF, Dawar P, Esim N, et al. Role of miRNAs in sucrose stress response, reactive oxygen species, and anthocyanin biosynthesis in Arabidopsis thaliana. Front Plant Sci. 2023; 14: 1278320

[63] Islam W, Waheed A, Naveed H, et al. MicroRNAs mediated plant responses to salt stress. Cells. 2022; 11: 2806

[64] An N, Fan S, Wang Y, et al. Genome-wide identification, characterization and expression analysis of long non-coding RNAs in different tissues of apple. Gene. 2018; 666: 44-57

[65] Li J, Cui J, Dai C, et al. Whole-transcriptome RNA sequencing reveals the global molecular responses and CeRNA regulatory network of mRNAs, lncRNAs, miRNAs and circRNAs in response to salt stress in sugar beet (Beta vulgaris) . Int J Mol Sci. 2020; 22: 289

[66] Pacheco JM, Canal MV, Pereyra CM, et al. The tip of the iceberg: emerging roles of TORC1, and its regulatory functions in plant cells. J Exp Bot. 2021; 72: 4085-101

[67] Sharma M, Jamsheer KM, Shukla BN, et al. Arabidopsis target of rapamycin coordinates with transcriptional and epigenetic machinery to regulate thermotolerance. Front Plant Sci. 2021; 12: 741965

[68] Pilala K-M, Panoutsopoulou K, Papadimitriou M-A, et al. Exploring the methyl-verse: dynamic interplay of epigenome and m6A epitranscriptome. Mol Ther. 2025; 33: 447-64

[69] Kan RL, Chen J, Sallam T . Crosstalk between epitranscriptomic and epigenetic mechanisms in gene regulation. Trends Genet. 2022; 38: 182-93

[70] Deng S, Zhang J, Su J, et al. RNA m6A regulates transcription via DNA demethylation and chromatin accessibility. Nat Genet. 2022; 54: 1427-37

[71] Xu C, Wu Z, Duan HC, et al. R-loop resolution promotes co-transcriptional chromatin silencing. Nat Commun. 2021; 12: 1-9

[72] Wei J, Li H, Gui Y, et al. Coordination of m6A mRNA methylation and gene transcriptome in sugarcane response to drought stress. Plants. 2023; 12: 3668

[73] Su D, Shu P, Hu N, et al. Dynamic m6A mRNA methylation reveals the involvement of AcALKBH10 in ripening-related quality regulation in kiwifruit. New Phytol. 2024; 243: 2265-78

[74] Zhou L, Tang R, Li X, et al. N6-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner. Genome Biol. 2021; 22: 168

[75] Zhou L, Tian S, Qin G . RNA methylomes reveal the m6A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 2019; 20: 156

[76] Hu J, Cai J, Umme A, et al. Unique features of mRNA m6A methylomes during expansion of tomato (Solanum lycopersicum) fruits . Plant Physiol. 2022; 188: 2215-27

[77] Hu J, Cai J, Park SJ, et al. N6-methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis . Plant J. 2021; 106: 1759-75

[78] Edger PP, Poorten TJ, VanBuren R, et al. Origin and evolution of the octoploid strawberry genome. Nat Genet. 2019; 51: 541-7

[79] Renny-Byfield S, Rodgers-Melnick E, Ross-Ibarra J . Gene fractionation and function in the ancient subgenomes of maize. Mol Biol Evol. 2017; 34: 1825-32

[80] Zhang Q, Guan P, Zhao L, et al. Asymmetric epigenome maps of subgenomes reveal imbalanced transcription and distinct evolutionary trends in Brassica napus . Mol Plant. 2021; 14: 604-19

[81] Marfil CF, Duarte PF, Masuelli RW . Phenotypic and epigenetic variation induced in newly synthesized allopolyploids and autopolyploids of potato. Sci Hortic. 2018; 234: 101-9

[82] Wang M, Li AM, Liao F, et al. Control of sucrose accumulation in sugarcane (Saccharum spp. hybrids) involves miRNA-mediated regulation of genes and transcription factors associated with sugar metabolism . GCB Bioenergy. 2022; 14: 173-91

[83] Jia HF, Chai YM, Li CL, et al. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011; 157: 188-99

[84] Li M, Ou M, He X, et al. DNA methylation role in subgenome expression dominance of Juglans regia and its wild relative J. mandshurica . Plant Physiol. 2023; 193: 1313-29

[85] Law JA, Jacobsen SE . Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010; 11: 204-20

[86] Cao Q, Feng Y, Dai X, et al. Dynamic changes of DNA methylation during wild strawberry (Fragaria nilgerrensis) tissue culture . Front Plant Sci. 2021; 12: 765383

[87] Liu D, Mu Q, Li X, et al. The callus formation capacity of strawberry leaf explants is modulated by DNA methylation. Hortic Res. 2022; 9: uhab073

[88] Cheng J, Niu Q, Zhang B, et al. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018; 19: 1-14

[89] Zhang L, Wang Y, Zhang X, et al. Dynamics of phytohormone and DNA methylation patterns changes during dormancy induction in strawberry (Fragaria × ananassa Duch.) . Plant Cell Rep. 2012; 31: 155-65

[90] Song Y, Peng Y, Liu L, et al. Phased gap-free genome assembly of octoploid cultivated strawberry illustrates the genetic and epigenetic divergence among subgenomes. Hortic Res. 2024; 11: uhad252

[91] Mu W, Li K, Yang Y, et al. Subgenomic stability of progenitor genomes during repeated allotetraploid origins of the same grass Brachypodium hybridum . Mol Biol Evol. 2023; 40:msad259

[92] Wyler M, Stritt C, Walser JC, et al. Impact of transposable elements on methylation and gene expression across natural accessions of Brachypodium distachyon . Genome Biol Evol. 2020; 12: 1994-2001

[93] Colle M, Leisner CP, Wai CM, et al. Haplotype-phased genome and evolution of phytonutrient pathways of tetraploid blueberry. Gigascience. 2019; 8: giz012

[94] Wang Z, Zhang W, Zhou Y, et al. Genetic and epigenetic signatures for improved breeding of cultivated blueberry. Hortic Res. 2024; 11: uhae138

[95] Osorio S, Vallarino JG, Szecowka M, et al. Alteration of the interconversion of pyruvate and malate in the plastid or cytosol of ripening tomato fruit invokes diverse consequences on sugar but similar effects. Plant Physiol. 2012; 161: 628-43

[96] Jia H, Zuo Q, Sadeghnezhad E, et al. HDAC19 recruits ERF4 to the MYB5a promoter and diminishes anthocyanin accumulation during grape ripening. Plant J. 2023; 113: 127-44

[97] Lü P, Yu S, Zhu N, et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nat Plants. 2018; 4: 784-91

[98] Lin D, Zhu X, Qi B, et al. SlMIR164A regulates fruit ripening and quality by controlling SlNAM2 and SlNAM3 in tomato. Plant Biotechnol J. 2022; 20: 1456-69

[99] Venios X, Gkizi D, Nisiotou A, et al. Emerging roles of epigenetics in grapevine and winegrowing. Plants. 2024; 13: 515

[100] Tang R, Duan X, Zhou L, et al. The FvABF3-FvALKBH10B-FvSEP3 cascade regulates fruit ripening in strawberry. Nat Commun. 2024; 15: 1-20

[101] Zhao H, Luo X, Guo C, et al. Transcriptome and MicroRNA analysis of Juglans regia in response to low-temperature stress. Int J Mol Sci. 2025; 26: 1401

[102] Gutschker S, Corral JM, Schmiedl A, et al. Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold . BMC Genomics. 2022; 23: 144

[103] Huang H, Liu R, Niu Q, et al. Global increase in DNA methylation during orange fruit development and ripening. Proc Natl Acad Sci U S A. 2019; 116: 1430-6

[104] 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. 2015; 33: 1-11

[105] Garg R, Narayana Chevala V, Shankar R, et al. Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep. 2015; 5: 5

[106] Czajka K, Mehes-Smith M, Nkongolo K . DNA methylation and histone modifications induced by abiotic stressors in plants. Genes Genomics. 2022; 44: 279-97

[107] Jiang H, Zhang Z-H, Kovalchuk I, et al. Small DNA methylation, big player in plant abiotic stress responses and memory. Front Plant Sci. 2020; 11: 595603

[108] He X, Guo S, Wang Y, et al. Systematic identification and analysis of heat-stress-responsive lncRNAs, circRNAs and miRNAs with associated co-expression and ceRNA networks in cucumber. Physiol Plant. 2020; 168: 736-54

[109] Jia H, Wang Y, Sun M, et al. Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol. 2013; 198: 453-65

[110] Guo JE, Hu Z, Yu X, et al. A histone deacetylase gene, SlHDA3, acts as a negative regulator of fruit ripening and carotenoid accumulation. Plant Cell Rep. 2018; 37: 125-35

[111] Zheng Y, Tian L, Liu H, et al. Sugars induce anthocyanin accumulation and flavanone 3-hydroxylase expression in grape berries. Plant Growth Regul. 2009; 58: 251-60

[112] Li D, Zhang X, Xu Y, et al. Effect of exogenous sucrose on anthocyanin synthesis in postharvest strawberry fruit. Food Chem. 2019; 289: 112-20

[113] Dai ZW, Meddar M, Renaud C, et al. Long-term in vitro culture of grape berries and its application to assess the effects of sugar supply on anthocyanin accumulation. J Exp Bot. 2014; 65: 4665-77

[114] Télef N, Stammitti-Bert L, Mortain-Bertrand A, et al. Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol. 2006; 62: 453-69

[115] Guo JE, Hu Z, Zhu M, et al. The tomato histone deacetylase SlHDA1 contributes to the repression of fruit ripening and carotenoid accumulation. Sci Rep. 2017; 7: 1-10

[116] 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; 72: 15027-39

[117] Manning K, Tör M, Poole M, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet. 2006; 38: 948-52

[118] Lv J, Han X, Bai L, et al. Effects of calcium chloride treatment on softening in red raspberry fruit during low-temperature storage. J Food Biochem. 2020; 44: e13419-9

[119] Liu R, How-Kit A, Stammitti L, et al. A DEMETER-like DNA demethylase protein governs tomato fruit ripening. Proc Natl Acad Sci U S A. 2015; 112: 10804-9

[120] Jia H, Zhang Z, Zhang S, et al. Effect of the methylation level on the grape fruit development process. J Agric Food Chem. 2020; 68: 2099-115

[121] Durán-Soria S, Pott DM, Osorio S, et al. Sugar signaling during fruit ripening. Front Plant Sci. 2020; 11: 564917

[122] Deng H, Chen Y, Liu Z, et al. SlERF.F12 modulates the transition to ripening in tomato fruit by recruiting the co-repressor TOPLESS and histone deacetylases to repress key ripening genes. Plant Cell. 2022; 34: 1250-72

[123] Feng K, Hou XL, Xing GM, et al. Advances in AP2/ERF superfamily transcription factors in plant. Crit Rev Biotechnol. 2020; 40: 750-76

[124] Zhang M, Leng P, Zhang G, et al. Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol. 2009; 166: 1241-52

[125] Sun Y, Yang X, Wu R, et al. DNA methylation controlling abscisic acid catabolism responds to light to mediate strawberry fruit ripening. J Integr Plant Biol. 2024; 66: 1718-34

[126] Mccormick AJ, Watt DA, Cramer MD . Supply and demand: sink regulation of sugar accumulation in sugarcane. J Exp Bot. 2009; 60: 357-64

[127] Zhu L, Lan J, Zhao T, et al. How vacuolar sugar transporters evolve and control cellular sugar homeostasis, organ development and crop yield. Nat Plants. 2025; 11: 1102-15

[128] Yolcu S, Skorupa M, Uras ME, et al. Genome-wide identification, phylogenetic classification of histone acetyltransferase genes, and their expression analysis in sugar beet (Beta vulgaris L.) under salt stress. Planta. 2024; 259: 1-19

[129] Yu Q, Guo Q, Li B, et al. Identification of RPD3/HDA1 family genes in sugar beet and response to abiotic stresses. Sugar Tech. 2023; 25: 834-45

[130] Gutschker C, Schmidt T, Sprink T . Deep learning predicts plant traits from bisulfite sequencing data. Plant Biotechnol J. 2022; 20: 2257-69

[131] Li B, Zhu L, Yang N, et al. Transcriptional landscape and dynamics involved in sugar and acid accumulation during apple fruit development. Plant Physiol. 2024; 195: 2772-86

[132] Zhu X, Chen A, Butler NM, et al. Molecular dissection of an intronic enhancer governing cold-induced expression of the vacuolar invertase gene in potato. Plant Cell. 2024; 36: 1985-99

[133] Zeng Z, Zhang W, Marand AP, et al. Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato. Genome Biol. 2019; 20: 123

[134] Wang Y, Zeng Y, Wang Y, et al. Haplotype-resolved genome and multi-omics landscape reveal an epigenetic regulation of citric acid accumulation in lemon. Plant Physiol. 2025; 199: kiaf400

[135] Yu H, Zhang C, Lu C, et al. The lemon genome and DNA methylome unveil epigenetic regulation of citric acid biosynthesis during fruit development. Hortic Res. 2024; 11: uhae005

[136] Li X, Guo W, Li J, et al. Histone acetylation at the promoter for the transcription factor PuWRKY31 affects sucrose accumulation in pear fruit. Plant Physiol. 2020; 182: 2035-46

[137] Yang J, Deng G, Lian J, et al. The chromosome-scale genome of melon dissects genetic architecture of important agronomic traits. iScience. 2020; 23: 101422

[138] Giordano A, Santo Domingo M, Quadrana L, et al. CRISPR/Cas9 gene editing uncovers the roles of CONSTITUTIVE TRIPLE RESPONSE 1 and REPRESSOR OF SILENCING 1 in melon fruit ripening and epigenetic regulation. J Exp Bot. 2022; 73: 4022-33

[139] Bai S, Tian Y, Tan C, et al. Genome-wide identification of microRNAs involved in the regulation of fruit ripening and climacteric stages in melon (Cucumis melo) . Hortic Res. 2020; 7: 106

[140] Kirkbride RC, Fischer RL, Harada JJ . Maternal NRPD1a regulates parental genome dosage in hybrid endosperm. Plant Cell. 2019; 31: 2663-82

[141] Lai T, Wang X, Ye B, et al. Molecular and functional characterization of the SBP-box transcription factor SPL-CNR in tomato fruit ripening and cell death. J Exp Bot. 2020; 71: 2995-3011

[142] Aamir M, Karmakar P, Singh VK, et al. A novel insight into transcriptional and epigenetic regulation underlying sex expression and flower development in melon (Cucumis melo L.) . Physiol Plant. 2021; 173: 1729-64

[143] Eleblu JSY, Haraghi A, Mania B, et al. The gynoecious CmWIP1 transcription factor interacts with CmbZIP48 to inhibit carpel development. Sci Rep. 2019; 9: 15443

[144] Miura K, Agetsuma M, Kitano H, et al. A metastable DWARF1 epigenetic mutant affecting plant stature in rice. Proc Natl Acad Sci U S A. 2009; 106: 11218-23

[145] Ong-Abdullah M, Ordway JM, Jiang N, et al. Loss of karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature. 2015; 525: 533-7

[146] López ME, Denoyes B, Bucher E . Epigenomic and transcriptomic persistence of heat stress memory in strawberry (Fragaria vesca) . BMC Plant Biol. 2024; 24: 405

[147] Ma W, Li B, Zheng L, et al. Combined profiling of transcriptome and DNA methylome reveal genes involved in accumulation of soluble sugars and organic acid in apple fruits. Foods. 2021; 10: 2198

[148] Kong J, Ma Y, Huang H, et al. The grape berry methylome reveals tissue-specific features associated with metabolism in ripening. Hortic Res. 2025; 12: uhaf238

[149] Luo J, Peng F, Zhang S, et al. The protein kinase FaSnRK1 α regulates sucrose accumulation in strawberry fruits . Plant Physiol Biochem. 2020; 151: 369-77

[150] Zhang H, Zhu J-K . RNA-directed DNA methylation dynamics in hybrid vigor. Nat Plants. 2024; 10: 857-73

[151] Cao X, Zhang Y, Chen L . Trans-acting siRNA-mediated paramutation persists over generations in maize-teosinte hybrids. Nat Commun. 2022; 13: 6123

[152] Whittaker C, Dean C . The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol. 2017; 33: 555-75

[153] Vojta A, Dobrinić P, Tadić V, et al. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 2016; 44: 5615-28

[154] Pan C, Sretenovic S, Qi Y . CRISPR/dCas-mediated transcriptional and epigenetic regulation in plants. Curr Opin Plant Biol. 2021; 60: 101980

[155] Tanenbaum ME, Gilbert LA, Qi LS, et al. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell. 2014; 159: 635-46

[156] Gallego-Bartolomé J, Gardiner J, Liu W, et al. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc Natl Acad Sci U S A. 2018; 115: E2125-34

[157] Papikian A, Liu W, Gallego-Bartolomé J, et al. Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat Commun. 2019; 10: 729

[158] 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 U S A. 2017; 114: E4511-9

[159] Kawaguchi K, Takei-Hoshi R, Yoshikawa I, et al. Functional disruption of cell wall invertase inhibitor by genome editing increases sugar content of tomato fruit without decrease fruit weight. Sci Rep. 2021; 11: 21534

[160] Zhang J, Lyu H, Chen J, et al. Releasing a sugar brake generates sweeter tomato without yield penalty. Nature. 2024; 635: 647-56

[161] Ren C, Liu Y, Guo Y, et al. Optimizing the CRISPR/Cas9 system for genome editing in grape by using grape promoters. Hortic Res. 2021; 8: 52

[162] Wang M, He L, Chen B, et al. Transgenerationally transmitted DNA demethylation of a spontaneous epialleles using CRISPR/dCas9-TET1cd targeted epigenetic editing in Arabidopsis. Int J Mol Sci. 2022; 23: 10492