Abstract
Aluminum (Al) is the most abundant element in the earth crust. Due to the abuse of phosphate fertilizer, acid rain has been frequently observed in recent years, resulting in the conversion of non-toxic aluminosilicates in the soil into Al ions, thereby causing stress to plants. As a DNA methylation inhibitor, curcumin can effectively counteract the Al stress on plants, while the epigenetic mechanism remains unclear. This study discusses the epigenetic mechanism of curcumin counteracting Al stress on grape. The results demonstrated that curcumin could significantly relieve the Al stress symptoms of grapes and reduce its whole genome methylation level. Al stress and curcumin treatment did not cause variations in the methylation level in each chromosome. While Al stress led to a slight increase in the average methylation level of each chromosome, and treatment by curcumin led to a significant decrease in the average methylation level of each chromosome. Specifically, the sites of CG and CHG were decreased significantly, and the site of CHH was increased or decreased significantly. Analysis of differentially-methylated regions (DMRs) revealed that treatment by curcumin led to an increase in hypo-DMRs in the whole genome of grape, and analysis of differentially-methylated genes (DMGs) also identified differentially related genes of hypo-DMRs in the whole genome of grapes, suggesting that curcumin triggers responses to Al stress by regulating hypo-methylation mode of the whole genome of grape. Additionally, Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis demonstrated that DMGs of grapes generate responses to Al stress by participating in galactose metabolism, ascorbate, and aldarate metabolism, and amino sugar and nucleotide sugar metabolism pathways of carbohydrate metabolism in the KEGG subclass.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Plant Physiol 121:472–480
Baránek M, Čechová J, Raddová J, Holleinová V, Ondrušíková E, Pidra M (2015) Dynamics and reversibility of the DNA methylation landscape of grapevine plants (Vitis vinifera) stressed by in vitro cultivation and thermotherapy. PLoS ONE 10(5):e0126638
Bernardo S, Dinis LT, Luzio A, Glória P, Mónica M, Luís V, Conde A, Gerós H, Correia CM, Moutinho-Pereira J (2017) Kaolin particle film application lowers oxidative damage and DNA methylation on grapevine (Vitis vinifera L). Environ Exp Bot 139:39–47
Bewick AJ, Niederhuth CE, Rohr NA, Griffin PT, Leebens-Mack J, Schmitz RJ (2017) The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. Genome Biol 18:65
Borrero JC, Pandey S, Ceballos H, Magnavaca R, Bahia FAFC (1995) Genetic variances for tolerance to soil acidity in a tropical maize population [Brazil, Colombia]. Maydica (Italy) 53(3):263–287
Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagenesis: J Environ Mutagen Soc 49(1):61–72
Chang Y, Zhu C, Jiang J, Zhang H, Zhu JK, Duan CG (2020) Epigenetic regulation in plant abiotic stress responses. J Integr Plant Biol 62(5):563–580
Davis-richardson AG, Russell JT, Dias R, McKinlay AJ, Canepa R, Fagen JR, Rusoff KT, Drew JC, Kolaczkowski B, Emerich DW, Triplett EW (2016) Corrigendum: integrating DNA methylation and gene expression data in the development of the soybean-Bradyrhizobium N2-fixing symbiosis. Front Microbiol 7:952
Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Am Soc Plant Biologists 107:315–321
Du YQ (2011) Effects of four drug treatments on DNA methylation in. Arabidopsis thaliana. Henan University
Ge CL, Yang XY, Liu XN, Sun JH, Wang ZG (2002) Effect of heavy metal on levels of methylation in DNA of riceand wheat. J Plant Physiol Mol Biology 28(5):363–368
Greco M, Chiappetta A, Bruno L, Bitonti MB (2012) In Posidonia oceanic cadmium induces changes in DNA methylation and chromatin patterning. J Exp Bot 63:695–709
Guo T, An P, Wei Z, Jia G, Xu X, Wei G, Huang W (2021) Research progress on plant DNA methylation under heavy metal stress. J Henan Agricultural Sci 50(10):1–9
Habu Y, Kakutani T, Paszkowski J (2001) Epigenetic developmental mechanisms in plants: molecules and targets of plant epigenetic regulation. Curr Opin Genet Dev 11(2):215–220
Harris CJ, Scheibe M, Wongpalee SP, Liu W, Cornett EM, Vaughan RM, Li X, Chen W, Xue Y, Zhong Z, Yen L, Barshop WD, Rayatpisheh S, Gallego-Bartolome J, Groth M, Wang Z, Wohlschlegel JA, Du J, Rothbart SB, Butter F, Jacobsen SE (2018) A DNA methylation reader complex that enhances gene transcription. Science 362:1182–1186
He YN, Xu ZR, Xiong ZT (2017) DNA methylation patterns of acid invertase gene promoters from Cu- tolerant and non-tolerant populations of Elsholtzia haichowensis under copper stress. Plant Sci J 35(4):574–582
Jiménez-Ariasa D, Borgesa AA, Luisb JC, Valdésb F, Sandalioc LM, Pérez JA (2015) Priming effect of menadione sodium bisulphite againstsalinity stress in Arabidopsis involves epigenetic changes in genes controlling proline metabolism. Environ Experimental Bot 120:23–30
Jones DL, Kochian LV (1995) Aluminum inhibition of 1,4,5-trisphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity. Plant Cell 7:1913–1922
Kinraide T, Parker D (1989) Assessing the phytotoxicity of mononuclear hydroxy-aluminum. Plant Cell Environ 12:478–487
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Biol 46:237–260. https://doi.org/10.1146/annurev.pp.46.060195.001321
Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002) Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol 4:694–699
Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV (1998) Aluminium-resistant Arabodopsis mutants with increased aluminum resistance exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117:9–17
Li ZQ, Ding XC, Lu H, Hu YL, Yue J, Huang Z, Mo LY, Chen L, Chen T, Chen P (2021) Physiological characteristics and DNA methylation analysis under lead stress in kenaf (Hibiscus cannabinus L). Acta Agron Sinica 47(6):1031–1042
Liu CY (2020) Functional analysis of DNA demethylase GmDMEs in soybean. Northeast Forestry University
Liu J, He Z (2020) Small DNA methylation, big player in plant abiotic stress responses and memory. Front Plant Sci 11:595603
Liu YH, Li ZA, Li J, Liu X, Wang Z (2017) Effects of curcumin on DNA methylation and development of chrysanthemum. J Henan Agricultural Sci 46(5):100–105
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
Marfil C, Ibañez V, Alonso R, Varela A, Bottini R, Masuelli R, Fontana A, Berli F (2019) Changes in grapevine DNA methylation and polyphenols content induced by solar ultraviolet-B radiation, water deficit and abscisic acid spray treatments. Plant Physiol Biochem Ppb 135:287–294
Morimula S, Takahashi E, Matsumoto H (1978) Association of aluminum with nuclei and inhibition of cell division in onion (Allium cepa) roots. Ztschrift Für Pflanzenphysiologie 88(5):395–401
Rothkegel K, Espinoza A, Sanhueza D, Victoria L, Aníbal R, Reinaldo C, Claudio M (2021) Identification of DNA methylation and transcriptomic profiles associated with fruit mealiness in Prunus persica (L.) Batsch. Front Plant Sci 12:684130
Schellenbaum P, Mohler V, Wenzel G, Walter B (2008) Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L). BMC Plant Biol 8(1):78
Shen XH (2022) Analysis of DNA methylation map of Alfalfa whole genome under two kinds of mutagenesis treatments. Acta Agrestia Sinica 30(1):46–54
Song Y, Ji D, Li S, Peng W, Li Q, Xiang F, Zhang X (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS ONE 7:e41274
Song Q, Decato B, Hong EE, Meng Z, Smith AD (2013) A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLoS ONE 8(12):e81148
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Publishing Group 21:64–72
Sun X, Zheng H, Sui N (2018) Regulation mechanism of long non-coding RNA in plant response to stress. Biochem Biophys Res Commun 503(2):402–407
Tyunin AP, Kiselev KV (2016) Alternations in VaSTS gene cytosine methylation and t-resveratrol production in response to UV-C irradiation in Vitis amurensis. Planr Cell Tissue Organ Cult 124:33–45
Wang S (2019) Aluminum toxicity of citrus seedlings is controlled by stress concentration and stress time. China Fruit News 36(06):68–69
Wang X, Moazed D (2017) DNA sequence-dependent epigenetic inheritance of gene silencing and histone H3K9 methylation. Science 356(6333):88–91
Wang M, Wang Y (2013) Role of epigenetic modifications in plant stress response. Chin Bull Life Sci 25(6):574–579
Wendte JM, Zhang Y, Ji L, Shi X, Schmitz RJ (2019) Epimutations are associated with CHROMOMETHYLASE 3-induced d e novo DNA methylation. eLife 8:e47891
Xie H, Konate M, Sai N, Tesfamicael KG, Timothy C, Matthew G, James B, Andrew M, Stephen JR, Roberta DB (2017) Global DNA methylation patterns can play a role in defining terroir in grapevine (Vitis vinifera Cv. Shiraz). Front Plant Sci 8:1860
Ye J, Li X, Tang S, Yan Z, Chen S, Liu H, Huang A (2020) Effects of aluminum treatment on resistance physiology and DNA methylation level of liupao tea seedlings. Shandong Agricultural Sciences 52(4):112–116
Yuan Y (2019) Effects of curcumin on physiological and biochemical indexes and DNA methylation of maize seedlings. Jilin Agricultural University
Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM 1 allows DNA methyltransferases to access Hl-contain in gheterochromatin. Cell 153:193–205
Zhang H, Lang Z, Zhu JK (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506
Zhao WQ (2015) Effects of curcumin and dicitabine on DNA methylation and development of chrysanthemum. Henan University
Zhao MM (2020) Study on the function of curcumin compounds. Hebei University of Science and Technology
Zhao H, He L, Zhang A, Men Y (2008) Advance in the study of effects of aluminum stress on plant photosynthesis and its mechanism. J Huazhong Agricultural Univ 27(1):155–160
Zhu F, Li M, Yan M, Qiao F, Jiang X (2021) Integrated transcriptome analysis and single-base resolution methylomes of watermelon (Citrullus lanatus) reveal epigenome modifications in response to osmotic stress. Front Plant Sci 12:769712
Zubko E, Gentry M, Kunova A, Meyer P (2012) Denovo DNA methylation activity of methyltransferase 1 (MET1) partially restores body methylation in Arabidopsis thaliana. Plant J Cell Mol Biology 71(6):1029–1037
Acknowledgements
This study was supported by the National Natural Science Foundation of China [grant numbers 32060645]; the Yunnan Provincial Joint Fund for Local Colleges and Universities [grant number 202101BA070001-036; 202101BA070001-172]; the Science Research Fund Project for Education Department of Yunnan Province [grant number 2023Y0876; 2023Y0860].
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Yongfu Zhang and Zhen Ren conceived and designed the experiments; Shiqin Xu, Kai Wang, Zhao Liu and Zuqin Qiao performed the experiments; Shiqin Xu, Xiaoqin Li and Yongfu Zhang analyzed the data; Yongfu Zhang contributed the reagents/materials/analytical tools; Xiaoqin Li and Yongfu Zhang wrote the manuscript. All authors reviewed and approved the manuscript.
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Li, X., Zhang, Y., Ren, Z. et al. Curcumin leads to responses of grapes to aluminum stress by inducing whole genome hypo-methylation. Hortic. Environ. Biotechnol. (2024). https://doi.org/10.1007/s13580-023-00565-4
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DOI: https://doi.org/10.1007/s13580-023-00565-4