Epigenetic memory and priming in plants

Turgut-Kara, Neslihan; Arıkan, Burcu; Çelik, Haluk

doi:10.1007/s10709-020-00093-4

Cited by 60 publications

(36 citation statements)

References 104 publications

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“…Nowadays, developing methods to improve tolerance to abiotic and biotic stresses is the main goal of breeders to reduce losses associated with climate change [107] in the context of food protection [31]. In this study, we obtained results supporting waterlogging as a priming factor against waterlogging stress in cucumber.…”

Section: Discussionsupporting

confidence: 53%

“…Still, the usage of waterlogging as a priming factor against oxygen deprivation in cucumber is not known. Priming and stress memory, as a consequence, are one of the main approaches developed by breeders for use in resistant plant production [29][30][31], either as an alternative to genetically modified (GM) plants or in beneficial financial terms [32]. Still, many questions remain unanswered, even those concerning the duration of memory in the life of a plant or the application of priming in the field conditions, not only in the laboratory.…”

Section: Introductionmentioning

confidence: 99%

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Long-Term Waterlogging as Factor Contributing to Hypoxia Stress Tolerance Enhancement in Cucumber: Comparative Transcriptome Analysis of Waterlogging Sensitive and Tolerant Accessions

Kęska

Szcześniak

Makałowska

et al. 2021

Genes

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Waterlogging (WL), excess water in the soil, is a phenomenon often occurring during plant cultivation causing low oxygen levels (hypoxia) in the soil. The aim of this study was to identify candidate genes involved in long-term waterlogging tolerance in cucumber using RNA sequencing. Here, we also determined how waterlogging pre-treatment (priming) influenced long-term memory in WL tolerant (WL-T) and WL sensitive (WL-S) i.e., DH2 and DH4 accessions, respectively. This work uncovered various differentially expressed genes (DEGs) activated in the long-term recovery in both accessions. De novo assembly generated 36,712 transcripts with an average length of 2236 bp. The results revealed that long-term waterlogging had divergent impacts on gene expression in WL-T DH2 and WL-S DH4 cucumber accessions: after 7 days of waterlogging, more DEGs in comparison to control conditions were identified in WL-S DH4 (8927) than in WL-T DH2 (5957). Additionally, 11,619 and 5007 DEGs were identified after a second waterlogging treatment in the WL-S and WL-T accessions, respectively. We identified genes associated with WL in cucumber that were especially related to enhanced glycolysis, adventitious roots development, and amino acid metabolism. qRT-PCR assay for hypoxia marker genes i.e., alcohol dehydrogenase (adh), 1-aminocyclopropane-1-carboxylate oxidase (aco) and long chain acyl-CoA synthetase 6 (lacs6) confirmed differences in response to waterlogging stress between sensitive and tolerant cucumbers and effectiveness of priming to enhance stress tolerance.

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Section: Discussionsupporting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

Long-Term Waterlogging as Factor Contributing to Hypoxia Stress Tolerance Enhancement in Cucumber: Comparative Transcriptome Analysis of Waterlogging Sensitive and Tolerant Accessions

Kęska

Szcześniak

Makałowska

et al. 2021

Genes

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“…Plant memory involves multiple physiological, proteomic, transcriptional, and epigenetic changes, with the important role of epigenetic modification in plant memory confirmed by numerous studies (Iwasaki and Paszkowski, 2014;Kinoshita and Seki, 2014;Dean, 2017;Lamke and Baurle, 2017;He and Li, 2018;Turgut-Kara et al, 2020). In this study, the relationship between the effects of repeated environmental low-temperature stimulation (cold priming) and DNA methylation patterns, as well as changes in gene expression and metabolite enrichment after cold memory generation, was investigated, which leads to changes in some agronomic traits in crops (e.g., free lysine content).…”

Section: Discussionmentioning

confidence: 89%

Roles of DNA Methylation in Cold Priming in Tartary Buckwheat

et al. 2020

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Plants experience a wide array of environmental stimuli, some of which are frequent occurrences of cold weather, which have priming effects on agricultural production and agronomic traits. DNA methylation may act as an epigenetic regulator for the cold response of Tartary buckwheat (Fagopyrum tataricum). Combined with long-term field observation and laboratory experiments, comparative phenome, methylome, and transcriptome analyses were performed to investigate the potential epigenetic contributions for the cold priming of Tartary buckwheat variety Dingku1. Tartary buckwheat cv. Dingku1 exhibited low-temperature resistance. Single-base resolution maps of the DNA methylome were generated, and a global loss of DNA methylation was observed during cold responding in Dingku1. These sites with differential methylation levels were predominant in the intergenic regions. Several hundred genes had different DNA methylation patterns and expressions in different cold treatments (cold memory and cold shock), such as CuAO, RPB1, and DHE1. The application of a DNA methylation inhibitor caused a change of the free lysine content, suggesting that DNA methylation can affect metabolite accumulation for Tartary buckwheat cold responses. The results of the present study suggest important roles of DNA methylation in regulating cold response and forming agronomic traits in Tartary buckwheat.

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“…Similar indications of acclimation have been seen in plants in response to salinity and IR (Munns and Gilliham, 2015;Van Hoeck et al, 2017). Although the exact nature of priming is still not fully understood, previous studies have shown that epigenetics, including DNA methylation, and TEs might play a role in this priming mechanism (Espinas et al, 2016;Negin and Moshelion, 2020;Turgut-Kara et al, 2020). Adaptation over one or more generations to stress also remains under debate (Pecinka et al, 2009;Rasmann et al, 2012;Moller and Mousseau, 2016), nonetheless, a number of reports have demonstrated transgenerational adaptive stress responses in plants (Verhoeven and van Gurp, 2012;Suter and Widmer, 2013;Groot et al, 2016).…”

Section: Introductionmentioning

confidence: 75%

Changes in DNA Methylation in Arabidopsis thaliana Plants Exposed Over Multiple Generations to Gamma Radiation

et al. 2021

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Previous studies have found indications that exposure to ionising radiation (IR) results in DNA methylation changes in plants. However, this phenomenon is yet to be studied across multiple generations. Furthermore, the exact role of these changes in the IR-induced plant response is still far from understood. Here, we study the effect of gamma radiation on DNA methylation and its effect across generations in young Arabidopsis plants. A multigenerational set-up was used in which three generations (Parent, generation 1, and generation 2) of 7-day old Arabidopsis thaliana plants were exposed to either of the different radiation treatments (30, 60, 110, or 430 mGy/h) or to natural background radiation (control condition) for 14 days. The parental generation consisted of previously non-exposed plants, whereas generation 1 and generation 2 plants had already received a similar irradiation in the previous one or two generations, respectively. Directly after exposure the entire methylomes were analysed with UPLC-MS/MS to measure whole genome methylation levels. Whole genome bisulfite sequencing was used to identify differentially methylated regions (DMRs), including their methylation context in the three generations and this for three different radiation conditions (control, 30 mGy/h, and 110 mGy/h). Both intra- and intergenerational comparisons of the genes and transposable elements associated with the DMRs were made. Taking the methylation context into account, the highest number of changes were found for cytosines followed directly by guanine (CG methylation), whereas only limited changes in CHG methylation occurred and no changes in CHH methylation were observed. A clear increase in IR-induced DMRs was seen over the three generations that were exposed to the lowest dose rate, where generation 2 had a markedly higher number of DMRs than the previous two generations (Parent and generation 1). Counterintuitively, we did not see significant differences in the plants exposed to the highest dose rate. A large number of DMRs associated with transposable elements were found, the majority of them being hypermethylated, likely leading to more genetic stability. Next to that, a significant number of DMRs were associated with genes (either in their promoter-associated region or gene body). A functional analysis of these genes showed an enrichment for genes related to development as well as various stress responses, including DNA repair, RNA splicing, and (a)biotic stress responses. These observations indicate a role of DNA methylation in the regulation of these genes in response to IR exposure and shows a possible role for epigenetics in plant adaptation to IR over multiple generations.

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Epigenetic memory and priming in plants

Cited by 60 publications

References 104 publications

Long-Term Waterlogging as Factor Contributing to Hypoxia Stress Tolerance Enhancement in Cucumber: Comparative Transcriptome Analysis of Waterlogging Sensitive and Tolerant Accessions

Long-Term Waterlogging as Factor Contributing to Hypoxia Stress Tolerance Enhancement in Cucumber: Comparative Transcriptome Analysis of Waterlogging Sensitive and Tolerant Accessions

Roles of DNA Methylation in Cold Priming in Tartary Buckwheat

Changes in DNA Methylation in Arabidopsis thaliana Plants Exposed Over Multiple Generations to Gamma Radiation

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