Time dynamics of stress legacy in clonal transgenerational effects: A case study on Trifolium repens

Abstract

Stress can be remembered by plants in a form of stress legacy that can alter future phenotypes of previously stressed plants and even phenotypes of their offspring. DNA methylation belongs among the mechanisms mediating the stress legacy. It is however not known for how long the stress legacy is carried by plants. If the legacy is long‐lasting, it can become maladaptive in situations when parental–offspring environment do not match. We investigated for how long after the last exposure of a parental plant to drought can the phenotype of its clonal offspring be altered. We grew parental plants of three genotypes of Trifolium repens for five months either in control conditions or in control conditions that were interrupted with intense drought periods applied for two months in four different time slots. We also treated half of the parental plants with a demethylating agent (5‐azacytidine, 5‐azaC) to test for the potential role of DNA methylation in the stress memory. Then, we transplanted parental cuttings (ramets) individually to control environment and allowed them to produce offspring ramets for two months. The drought stress experienced by parents affected phenotypes of offspring ramets. The stress legacy resulted in enhanced number of offspring ramets originating from plants that experienced drought stress even 56 days before their transplantation to the control environment. 5‐azaC altered transgenerational effects on offspring ramets. We confirmed that drought stress can trigger transgenerational effects in T . repens that is very likely mediated by DNA methylation. Most importantly, the stress legacy in parental plants persisted for at least 8 weeks suggesting that the stress legacy can persist in a clonal plant Trifolium repens for relatively long period. We suggest that the stress legacy should be considered in future ecological studies on clonal plants.

Effect of DNA methylation, modified by 5-azaC, on ecophysiological responses of a clonal plant to changing climate

“…Hence, it is plausible that the plants already lost their epigenetic memory on the field conditions and became epigenetically adjusted to the new experimental conditions 7 . This is in line with other studies indicating that epigenetic memory can be gradually lost over several asexual generations 89 , 90 . Epigenetic adjustments of the plants to our common garden and greenhouse could be however maladaptive when plants were moved to the growth chambers simulating their original environments.…”

DNA methylation dynamics in response to stress : An insight into stress-induced and stably inherited DNA methylation variants in asexual and sexual plants

“…Although our results did not allow us to conclude that intergenerational effects are more common in asexually reproducing plant species compared to sexually reproducing species, it remains interesting, however, that the only species to show intergenerational effect on phenotypes in G3 (when the stress was removed) was in the clonal T. repens. Such inter-and trans-generational effects have been reported in previous studies in the specific case of T. repens (González et al, 2017;Quan et al, 2022;Rendina González et al, 2016. In one of these studies the generality of transgenerational effects of different stresses on biomass was tested across five T. repens genotypes (Rendina González et al, 2018).…”

DNA methylation variation and growth in the clonal Duchesnea indica is regulated by both past and present lead environments

“…Phenotypic variation driven by environmental change is associated with DNA methylation [ 16 ]. It has been shown that the parents methylation level and status of clonal plants can be stably transmitted to their offspring, thus affecting the methylation status and growth of their offspring (e.g., [ 12 , 15 , 24 , 59 ]). In this study, we investigated whether DNA methylation changes in the progeny of the clonal plant D. indica were regulated by both past and present environments and whether the stress legacy induced by DNA methylation in parental plants played a role in its offspring growth.…”

“…The transgenerational effect of phenotypic plasticity has also been confirmed by other studies on clonal plants, such as dandelion under salt stress, where transgenerational DNA methylation changes cause transgenerational phenotypic changes, and the leaf morphology and R/S of its offspring are different from the control [ 59 ]. Drought stress can also affect the DNA methylation level of Trifolium repens parental strains, inducing their offspring to form the legacy of drought stress, which changes the offspring phenotype [ 12 ]. Besides, for clonal plants, the biggest defect is the lack of genetic diversity, which can be remedied by stress legacy induced by epigenetics [ 23 ].…”