The Arabidopsis DNA Methylome Is Stable under Transgenerational Drought Stress

Abstract

Improving the responsiveness, acclimation, and memory of plants to abiotic stress holds substantive potential for improving agriculture. An unresolved question is the involvement of chromatin marks in the memory of agriculturally relevant stresses. Such potential has spurred numerous investigations yielding both promising and conflicting results. Consequently, it remains unclear to what extent robust stress-induced DNA methylation variation can underpin stress memory. Using a slow-onset water deprivation treatment in Arabidopsis (Arabidopsis thaliana), we investigated the malleability of the DNA methylome to drought stress within a generation and under repeated drought stress over five successive generations. While drought-associated epialleles in the methylome were detected within a generation, they did not correlate with drought-responsive gene expression. Six traits were analyzed for transgenerational stress memory, and the descendants of drought-stressed lineages showed one case of memory in the form of increased seed dormancy, and that persisted one generation removed from stress. With respect to transgenerational drought stress, there were negligible conserved differentially methylated regions in drought-exposed lineages compared with unstressed lineages. Instead, the majority of observed variation was tied to stochastic or preexisting differences in the epigenome occurring at repetitive regions of the Arabidopsis genome. Furthermore, the experience of repeated drought stress was not observed to influence transgenerational epi-allele accumulation. Our findings demonstrate that, while transgenerational memory is observed in one of six traits examined, they are not associated with causative changes in the DNA methylome, which appears relatively impervious to drought stress.

Maintenance of pre‐existing DNA methylation states through recurring excess‐light stress

“…The potential for DNA methylation to contribute towards plant acclimatory responses, as an “epigenetic” layer regulating the expression of a genotype, remains an enigmatic phenomenon. In contrast to studies that have reported DNA methylation changes associated with abiotic stress (Jiang et al, ; Tricker, Gibbings, Rodríguez López, Hadley, & Wilkinson, ; Wibowo et al, ; Zheng et al, ), we recently reported a lack of drought‐induced methylome variation, persisting in a transgenerational manner, in Arabidopsis (Ganguly, Crisp, Eichten, & Pogson, ). These results of a robust methylome impervious to drought stress raised multiple questions: (a) is robustness a general principle of the methylome or was it specific of drought stress and (b) did the lack of variation in the methylome reflect a lack of physiological memory.…”

“…All Arabidopsis plants used in this study were in the Columbia (Col‐0) background and derived from a common inbred parent, to minimize genetic variation and stochastic DNA methylation variation (Crisp et al, ; Ganguly et al, ; Schmitz et al, ). Prior to light, seeds were sown onto moist soil and kept at 4 °C for three nights to allow for seed stratification.…”

“…Using an experimental design to minimize genetic variation and pre‐existing methylation differences in Arabidopsis, by comparing siblings from an inbred parent (Ganguly et al, ), physiological measurements were coupled to in‐depth methylome profiling to establish the contribution of stable methylome changes towards photo‐acclimatory reprogramming, in the context of SAA priming or memory. We determined that SAA phenotypes are evident in whole rosette treatments and tested whether they can be propagated from exposed tissue to new tissue, developed in the absence of stress.…”

Inhibition of DNA demethylation enhances plant tolerance to cadmium toxicity by improving iron nutrition

“…In the present study, we detected an apparent increase in global DNA methylation in the roots of Arabidopsis plants upon Cd exposure (Figures a,b and S1), which is in accordance with the findings of Wang et al (). Several other abiotic stresses, such as salt stress, phosphorus deficiency, and drought stress have also been reported to upregulate DNA methylation in plants (Ganguly, Crisp, Eichten, & Pogson, ; Secco et al, ; Wibowo et al, ). In mammals, the genes involved in the DNA methylation machinery have been linked to Cd‐induced DNA methylation alterations (Benbrahim‐Tallaa, Waterland, Dill, Webber, & Waalkes, ; Jiang et al, ).…”

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

“…Such inherited environmental effects can be transmitted from parent to offspring (and to additional generations in some cases) by diverse and nonmutually exclusive mechanisms, including (a) heritable epigenetic modifications (i.e., DNA methylation marks, histone modifications, and small RNAs) and (b) the allocation of nutritive resources, hormones, mRNAs, and regulatory proteins to seeds or eggs (Herman & Sultan, ; Jablonka, ). As more research has focused on transgenerational plasticity, it has become clear that these effects are highly variable (Colicchio, ; Groot et al., ; Herman & Sultan, ) and nearly absent in some cases (Ganguly, Crisp, Eichten, & Pogson, ). Empirical investigations in diverse plant and animal systems have confirmed that transgenerational environmental effects can be adaptive when parent and progeny environments match (i.e., under positive intergenerational environmental autocorrelations; see, e.g., Bilichak, Ilnystkyy, Hollunder, & Kovalchuk, ; Dantzer et al, ; Herman, Sultan, Horgan‐Kobelski, & Riggs, ; Lopez Sanchez, Stassen, Furci, Smith, & Ton, ; Rasmann et al, ; Slaughter et al, ; Verhoeven & van Gurp, ; Walsh et al, ; Wibowo et al, ).…”