Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages

Abstract

DNA methylation is one of the mechanisms underlying epigenetic modifications. DNA methylations can be environmentally induced and such induced modifications can at times be transmitted to successive generations. However, it remains speculative how common such environmentally induced transgenerational DNA methylation changes are and if they persist for more than one offspring generation. We exposed multiple accessions of two different apomictic dandelion lineages of the Taraxacum officinale group (Taraxacum alatum and T. hemicyclum) to drought and salicylic acid (SA) treatment. Using methylation‐sensitive amplified fragment length polymorphism markers (MS‐AFLPs) we screened anonymous methylation changes at CCGG restriction sites throughout the genome after stress treatments and assessed the heritability of induced changes for two subsequent unexposed offspring generations. Irrespective of the initial stress treatment, a clear buildup of heritable DNA methylation variation was observed across three generations, indicating a considerable background rate of heritable epimutations. Less evidence was detected for environmental effects. Drought stress showed some evidence for accession‐specific methylation changes, but only in the exposed generation and not in their offspring. By contrast, SA treatment caused an increased rate of methylation change in offspring of treated plants. These changes were seemingly undirected resulting in increased transgenerational epigenetic variation between offspring individuals, but not in predictable epigenetic variants. While the functional consequences of these MS‐AFLP‐detected DNA methylation changes remain to be demonstrated, our study shows that (1) stress‐induced transgenerational DNA methylation modification in dandelions is genotype and context‐specific; and (2) inherited environmental DNA methylation effects are mostly undirected and not targeted to specific loci.

Transgenerational Effects and Epigenetic Memory in the Clonal Plant Trifolium repens

“…For instance, Herman and Sultan (2016) observed drought-triggered TGE in Polygonum persicaria that were removed after demethylation treatment with zebularine, thus indicating that DNA methylation was likely involved in the expression of the offspring phenotypes. On the other hand, Preite et al (2018) observed a build-up of DNA methylation variation after three generations in two lineages of the apomictic dandelion concluding that these changes were inherited in a genotype and context-specific manner. Another study reported heritable DNA hypomethylation and enhance tolerance to heavy metal stress in the unstressed offspring of rice ( Ou et al, 2012 ).…”

“…One of the first evidences provided Verhoeven et al (2010) who showed that environmental stress in parental generation can trigger changes in DNA methylation that can be passed to next apomictic (clonal) generation of dandelions ( Taraxacum officinale ) with high fidelity. The environmental induction of DNA methylation changes was genotype-specific and represents, at least partly, a stress-induced increase of seemingly untargeted DNA methylation variation ( Preite et al, 2018 ). In another study, they pointed out that the epigenetic differentiation (DNA methylation variation) of natural populations of apomictic dandelions can be environmentally determined ( Preite et al, 2015 ).…”

Increased epigenetic diversity and transient epigenetic memory in response to salinity stress in Thlaspi arvense

“…Recent studies have demonstrated that epigenetic variation was affected by environmental stimulus, genetic variation, and geographic origin together (Artemov et al., 2017; Herman & Sultan, 2016; Kawakatsu et al., 2016; Preite et al., 2018). Thus, it was a good choice to use nearly isogenic plants to study the effects of environmental stimulus on epigenetic variation.…”

Epigenetic Mechanisms of Plant Adaptation to Biotic and Abiotic Stresses

“…Hence, epigenetic variation may cause heritable phenotypic differences in ecologically relevant traits in natural plant populations. Commonality and heritability of environmentally induced changes in DNA methylation were studied by subjecting multiple accessions of two different apomictic dandelion lineages ( T. alatum and T. hemicyclum ) to drought and SA [ 102 ]. In both stress treatments, heritable variations of DNA methylation were accumulated across three successive plant generations, indicating a high frequency of spontaneous epimutations.…”