Epigenetic Differentiation Persists after Male Gametogenesis in Natural Populations of the Perennial Herb Helleborus foetidus (Ranunculaceae)

Abstract

Despite the importance of assessing the stability of epigenetic variation in non-model organisms living in real-world scenarios, no studies have been conducted on the transgenerational persistence of epigenetic structure in wild plant populations. This gap in knowledge is hindering progress in the interpretation of natural epigenetic variation. By applying the methylation-sensitive amplified fragment length polymorphism (MSAP) technique to paired plant-pollen (i.e., sporophyte-male gametophyte) DNA samples, and then comparing methylation patterns and epigenetic population differentiation in sporophytes and their descendant gametophytes, we investigated transgenerational constancy of epigenetic structure in three populations of the perennial herb Helleborus foetidus (Ranunculaceae). Single-locus and multilocus analyses revealed extensive epigenetic differentiation between sporophyte populations. Locus-by-locus comparisons of methylation status in individual sporophytes and descendant gametophytes showed that ∼75% of epigenetic markers persisted unchanged through gametogenesis. In spite of some epigenetic reorganization taking place during gametogenesis, multilocus epigenetic differentiation between sporophyte populations was preserved in the subsequent gametophyte stage. In addition to illustrating the efficacy of applying the MSAP technique to paired plant-pollen DNA samples to investigate epigenetic gametic inheritance in wild plants, this paper suggests that epigenetic differentiation between adult plant populations of H. foetidus is likely to persist across generations.

Genetic and epigenetic divergence between disturbed and undisturbed subpopulations of a Mediterranean shrub: a 20‐year field experiment

“…New epigenetic variants could have arisen spontaneously (e.g., via unfaithful meiotic transmission, leading to parent‐offspring differences; Herrera et al. 2013; Lauria et al. 2014) and/or in response to the environmental changes brought about by disturbance (e.g., somatic modifications between the seed and adult plant stages; Boyko and Kovalchuk 2008; Feng et al.…”

When is incomplete epigenetic resetting in germ cells favoured by natural selection?

“…Recent data from both animals and plants indicate that epigenetic resetting is not always complete and hence that acquired epigenetic states may be transmitted from parents to offspring ('germ-line epigenetic inheritance' or 'incomplete epigenetic resetting' or 'incomplete epigenetic reprogramming'; e.g. [6][7][8][9][10][11][12][13][14] reviewed in [4,5,[15][16][17][18][19]). …”

Population Epigenetics

“…In some cases, these epigenetic responses provide an adaptive advantage to offspring that are subjected to those same environmental conditions [46]. To fully address these questions, laboratory-based studies on model organisms should be coupled with natural and manipulative studies on natural populations and nonmodel organisms to obtain a clearer picture of how epigenetics affects organisms [38].…”

“…Both facilitated and pure tend to exhibit non-Mendelian segregation and both can be affected by stochasticity in addition to environmental conditions. Researchers have begun designing elegant studies that control for genetic differences among individuals [14,[37][38][39][40]. These studies have suggested that some epigenetic variation is correlated with environment and some environmentally induced epigenetic variation is passed on to the next generation.…”

“…Epigenetic inheritance also occurs in the perennial herbs, Helleborus foetidus [38] and T. officinale [14]. In both studies, MS-AFLP was used to identify patterns of epigenetic variation in parent plants and the next generation.…”