DNA methylation dynamics during stress response in woodland strawberry (Fragaria vesca)

Abstract

Environmental stresses can result in a wide range of physiological and molecular responses in plants. These responses can also impact epigenetic information in genomes, especially at the level of DNA methylation (5-methylcytosine). DNA methylation is the hallmark heritable epigenetic modification and plays a key role in silencing transposable elements (TEs). Although DNA methylation is an essential epigenetic mechanism, fundamental aspects of its contribution to stress responses and adaptation remain obscure. We investigated epigenome dynamics of wild strawberry (Fragaria vesca) in response to variable ecologically relevant environmental conditions at the DNA methylation level. F. vesca methylome responded with great plasticity to ecologically relevant abiotic and hormonal stresses. Thermal stress resulted in substantial genome-wide loss of DNA methylation. Notably, all tested stress conditions resulted in marked hot spots of differential DNA methylation near centromeric or pericentromeric regions, particularly in the non-symmetrical DNA methylation context. Additionally, we identified differentially methylated regions (DMRs) within promoter regions of transcription factor (TF) superfamilies involved in plant stress-response and assessed the effects of these changes on gene expression. These findings improve our understanding on stress-response at the epigenome level by highlighting the correlation between DNA methylation, TEs and gene expression regulation in plants subjected to a broad range of environmental stresses.

References

[1] World Meteorological Organization (WMO) . State of the global climate 2021 . 2021. https://library.wmo.int/index.php?lvl=notice_display&id=22080#.YvkTFXZBy3A.

[2] Kersey PJ . Plant genome sequences: past, present, future. Curr Opin Plant Biol. 2019; 48: 1-8.

[3] Roquis D, Robertson M, Yu L et al. Genomic impact of stress-induced transposable element mobility in Arabidopsis. Nucleic Acids Res. 2021; 49: 10431-47.

[4] Wang P, Zhao FJ, Kopittke PM . Engineering crops without genome integration using nanotechnology. Trends Plant Sci. 2019; 24: 574-7.

[5] Varotto S, Tani E, Abraham E et al. Epigenetics: possible applications in climate-smart crop breeding. J Exp Bot. 2020; 71: 5223-36.

[6] Mac Kelprang R, Lemaux PG . Genetic engineering and editing of plants: an analysis of new and persisting questions. Annu Rev Plant Biol. 2020; 71: 659-87.

[7] Zhang H, Lang Z, Zhu JK . Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018; 19: 489-506.

[8] Bewick AJ, Zhang Y, Wendte JM et al. Evolutionary and experimental loss of gene body methylation and its consequence to gene expression. G3 (Bethesda). 2019; 9: 2441-5.

[9] Kenchanmane Raju SK, Ritter EJ, Niederhuth CE . Establishment, maintenance, and biological roles of non-CG methylation in plants. Essays Biochem. 2019; 63: 743-55.

[10] Kawakatsu T, Huang S, Jupe F et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell. 2016; 166: 492-505.

[11] Rendina González AP, Preite V, Verhoeven KJF et al. Transgenerational effects and epigenetic memory in the clonal plant trifolium repens. Front Plant Sci. 2018; 9: 1-11.

[12] Tong W, Li R, Huang J et al. Divergent DNA methylation contributes to duplicated gene evolution and chilling response in tea plants. Plant J. 2021; 106: 1312-27.

[13] Entrambasaguas L, Ruocco M, Verhoeven KJF et al. Gene body DNA methylation in seagrasses: inter- and intraspecific differences and interaction with transcriptome plasticity under heat stress. Sci Rep. 2021; 11: 1-15.

[14] Sun RZ, Liu J, Wang YY et al. DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica. PLoS Genet. 2021; 17: 1-29.

[15] Wang J, Nan N, Li N et al. A DNA methylation reader-chaperone regulator-transcription factor complex activates OsHKT1;5 expression during salinity stress. Plant Cell. 2020; 32: 3535-58.

[16] De Kort H, Panis B, Deforce D et al. Ecological divergence of wild strawberry DNA methylation patterns at distinct spatial scales. Mol Ecol. 2020; 29: 4871-81.

[17] Sammarco I, Münzbergová Z, Latzel V . DNA methylation can mediate local adaptation and response to climate change in the clonal plant Fragaria vesca: evidence from a European-scale reciprocal transplant experiment. Front Plant Sci. 2022; 13: 827166.

[18] Ghaderi N, Siosemardeh A . Esponse to drought stress of two strawberry cultivars (cv. Kurdistan and Selva). Hortic Environ Biotechnol. 2011; 52: 6-12.

[19] Turechek WW, Peres NA . Heat treatment effects on strawberry plant survival and angular leaf spot, caused by Xanthomonas fragariae, in nursery production. Plant Dis. 2009; 93: 299-308.

[20] Lv J, Zheng T, Song Z et al. Strawberry proteome responses to controlled hot and cold stress partly mimic post-harvest storage temperature effects on fruit quality. Front Nutr. 2022; 8: 1-19.

[21] Orsini F, Alnayef M, Bona S et al. Low stomatal density and reduced transpiration facilitate strawberry adaptation to salinity. Environ Exp Bot. 2012; 81: 1-10.

[22] Jamali B, Eshghi S, Shahidi-Rad K . Growth and fruit characteristics of strawberry cv. Selva as affected by different application timing of salicylic acid under saline conditions. Int J Fruit Sci. 2015; 15: 339-52.

[23] Choi HG, Moon BY, Kang NJ . Correlation between strawberry (Fragaria ananassa Duch.) productivity and photosynthesis-related parameters under various growth conditions. Front Plant Sci. 2016; 7: 1607.

[24] Hidaka K, Dan K, Imamura H . Effect of supplemental lighting from different light sources on growth and yield of strawberry. Environ Control Biol. 2013; 51: 41-7.

[25] Mohamed RA, Abdelbaset AK, Abd-Elkader DY . Salicylic acid effects on growth, yield, and fruit quality of strawberry cultivars. J Med Act Plants. 2018; 6: 1-11.

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

[27] 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.

[28] Urrutia M, Bonet J, Arús P et al. A near-isogenic line (NIL) collection in diploid strawberry and its use in the genetic analysis of morphologic, phenotypic and nutritional characters. Theor Appl Genet. 2015; 128: 1261-75.

[29] Schmitz RJ, Schultz MD, Lewsey MG et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011; 334: 369-73.

[30] Becker C, Hagmann J, Müller J et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011; 480: 245-9.

[31] Nunn A, Otto C, Stadler PF et al. Comprehensive benchmarking of software for mapping whole genome bisulfite data: from read alignment to DNA methylation analysis. Brief Bioinform. 2021; 00: 1-9.

[32] Nunn A, Can SN, Otto C et al. EpiDiverse toolkit. a pipeline suite for the analysis of bisulfite sequencing data in ecological plant epigenetics. 2021; 3: 1-7.

[33] Edger PP, Van Buren R, Colle M et al. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. Gigascience. 2018; 7: 1-7.

[34] Li H . Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018; 34: 3094-100.

[35] Li Y, Pi M, Gao Q et al. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hortic Res. 2019; 6: 61.

[36] Ou S, Su W, Liao Y et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 2019; 20: 1-18.

[37] Fojtová M, Kovařík A, Matyášek R . Cytosine methylation of plastid genome in higher plants. Fact or artefact? Plant Sci . 2001; 160: 585-93.

[38] Tian T, Liu Y, Yan H et al. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 2017; 45: W122-9.

[39] Wu T, Hu E, Xu S et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innov. 2021; 2: 100141.

[40] Dong C, Xi Y, Chen X et al. Genome-wide identification of AP2/EREBP in Fragaria vesca and expression pattern analysis of the FvDREB subfamily under drought stress. BMC Plant Biol. 2021; 21: 295.

[41] Xie Z, Nolan TM, Jiang H et al. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front Plant Sci. 2019; 10: 1-17.

[42] Hu Y, Han YT, Wei W et al. Identification, isolation, and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria Vesca. Front Plant Sci. 2015; 6: 1-16.

[43] Wei W, Hu Y, Han YT et al. The WRKY transcription factors in the diploid woodland strawberry Fragaria vesca: identification and expression analysis under biotic and abiotic stresses. Plant Physiol Biochem. 2016; 105: 129-44.

[44] Li H, Zhou Y, Ma Z et al. Genome-wide identification and expression analysis of myb transcription factors and their responses to abiotic stresses in woodland strawberry (Fragaria vesca). Horticulturae. 2021; 7: 97.

[45] Bucher E, Reinders J, Mirouze M . Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol. 2012; 15: 503-10.

[46] Li A, Chen L, Liu Z et al. Characterization of strawberry (Fragaria vesca) sequence genome. 2018. bioRxiv 244418.

[47] Xiong W, Dooner HK, Du C . Rolling-circle amplification of centromeric Helitrons in plant genomes. Plant J. 2016; 88: 1038-45.

[48] Zhang H, Zhu J, Gong Z et al. Abiotic stress responses in plants. Nat Rev Genet. 2022; 23: 104-19.

[49] De Kort H, Toivainen T, Van Nieuwerburgh F et al. Standing covariation between genomic and epigenomic patterns as source for natural selection in wild strawberry plants. 2021. bioRxiv 2021.03.31.437859.

[50] Rakei A, Maali-Amiri R, Zeinali H et al. DNA methylation and physio-biochemical analysis of chickpea in response to cold stress. Protoplasma. 2016; 253: 61-76.

[51] Qian Y, Hu W, Liao J et al. The dynamics of DNA methylation in the maize (Zea mays L.) inbred line B73 response to heat stress at the seedling stage. Biochem Biophys Res Commun. 2019; 512: 742-9.

[52] Hossain MS, Kawakatsu T, Do KK et al. Divergent cytosine DNA methylation patterns in single-cell, soybean root hairs. New Phytol. 2017; 214: 808-19.

[53] Suriyasak C, Hatanaka K, Tanaka H et al. Alterations of DNA methylation caused by cold plasma treatment restore delayed germination of heat-stressed Rice (Oryza sativa L.) seeds. ACS Agric Sci Technol. 2021; 1: 5-10.

[54] Wibowo A, Becker C, Marconi G et al. Elife-13546-V2. 2016: 1-27.

[55] Omidvar V, Fellner M . DNA methylation and transcriptomic changes in response to different lights and stresses in 7B-1 male-sterile tomato. PLoS One. 2015; 10: 1-23.

[56] Li R, Hu F, Li B et al. Whole genome bisulfite sequencing methylome analysis of mulberry (Morus alba) reveals epigenome modifications in response to drought stress. Sci Rep. 2020; 10: 1-17.

[57] Zheng X, Chen L, Li M et al. Transgenerational variations in DNA methylation induced by drought stress in two rice varieties with distinguished difference to drought resistance. PLoS One. 2013; 8: 1-13.

[58] Ou X, Zhang Y, Xu C et al. Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in Rice (Oryza sativa L.). PLoS One. 2012; 7: e41143.

[59] Kou HP, Li Y, Song XX et al. Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol. 2011; 168: 1685-93.

[60] Verhoeven KJF, Jansen JJ, van Dijk PJ et al. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010; 185: 1108-18.

[61] Slotkin RK, Martienssen R . Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007; 8: 272-85.

[62] Deniz Ö, Frost JM, Branco MR . Regulation of transposable elements by DNA modifications. Nat Rev Genet. 2019; 20: 417-31.

[63] Naito K, Zhang F, Tsukiyama T et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature. 2009; 461: 1130-4.

[64] Noshay JM, Anderson SN, Zhou P et al. Monitoring the interplay between transposable element families and DNA methylation in maize. PLoS Genet. 2019; 15: 1-25.

[65] Secco D, Wang C, Shou H et al. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. elife. 2015; 4: 1-26.

[66] Xin Y, Ma B, Xiang Z et al. Amplification of miniature inverted-repeat transposable elements and the associated impact on gene regulation and alternative splicing in mulberry (Morus notabilis). Mob DNA. 2019; 10: 1-13.

[67] Nunn A, Rodríguez-Arévalo I, Tandukar Z et al. Chromosome-level Thlaspi arvense genome provides new tools for translational research and for a newly domesticated cash cover crop of the cooler climates. Plant Biotechnol J. 2022; 20: 944-63.

[68] Naish M, Alonge M, Wlodzimierz P et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021; 374: eabi7489.

[69] Comai L, Maheshwari S, Marimuthu MPA . Plant centromeres. Curr Opin Plant Biol. 2017; 36: 158-67.

[70] Janni M, Gullì M, Maestri E et al. Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity. J Exp Bot. 2020; 71: 3780-802.

[71] dos Santos TB, Ribas AF, de Souza SGH et al. Physiological responses to drought, salinity, and heat stress in plants: a review. Stress. 2022; 2: 113-35.

[72] Nahar L, Aycan M, Hanamata S et al. Impact of single and combined salinity and high-temperature stresses on agro-physiological, biochemical, and transcriptional responses in rice and stress-release. Plants. 2022; 11: 501.

[73] Ohama N, Kusakabe K, Mizoi J et al. The transcriptional cascade in the heat stress response of arabidopsis is strictly regulated at the level of transcription factor expression. Plant Cell. 2016; 28: 181-201.

[74] Ohama N, Sato H, Shinozaki K et al. Transcriptional regulatory network of plant heat stress response. Trends Plant Sci. 2017; 22: 53-65.

[75] Zhang CL, Wang YX, Hu X et al. An apple AP2/EREBP-type transcription factor, MdWRI4, enhances plant resistance to abiotic stress by increasing cuticular wax load. Environ Exp Bot. 2020; 180: 104206.

[76] Liang D, Zhang Z, Wu H et al. Single-base-resolution methylomes of populus trichocarpa reveal the association between DNA methylation and drought stress. BMC Genet. 2014; 15: 1-11.

[77] Liu HC, Liao HT, Charng YY . The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 2011; 34: 738-51.

[78] Klay I, Gouia S, Liu M et al. Ethylene response factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Sci. 2018; 274: 137-45.

[79] Huang J, Zhao X, Bürger M et al. Two interacting ethylene response factors regulate heat stress response. Plant Cell. 2021; 33: 338-57.

[80] Centomani I, Sgobba A, D’Addabbo P et al. Involvement of DNA methylation in the control of cell growth during heat stress in tobacco BY-2 cells. Protoplasma. 2015; 252: 1451-9.

[81] Liao WY, Lin LF, Jheng JL et al. Identification of heat shock transcription factor genes involved in thermotolerance of octoploid cultivated strawberry. Int J Mol Sci. 2016; 17: 1-21.

[82] Song H, Wang P, Hou L et al. Global analysis of WRKY genes and their response to dehydration and salt stress in soybean. Front Plant Sci. 2016; 7: 1-15.