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.
Highlights
Interest in the evolutionary and ecological significance of epigenetic processes has increased considerably in recent years [1,2,3,4]
In the case of plants, this upsurge of interest has been largely motivated by evidence that epigenetic markers often are not reset across generations [5,6], epigenetic differences can be an important source of heritable phenotypic variation [7,8,9,10], epigenetic variation can greatly exceed genetic differences between individuals or populations [11,12,13,14,15,16], and epigenetic processes can impinge on fitness-related traits and ecological processes at the individual, population and community levels [3], [17,18,19]
Epigenetic characteristics of H. foetidus plants sampled for this study varied significantly across sampling sites, as found by the few investigations that have so far looked for structuring of epigenetic variation in wild plant populations [14], [15], [29], [30]
Summary
Interest in the evolutionary and ecological significance of epigenetic processes has increased considerably in recent years [1,2,3,4]. The current lack of information on the transgenerational constancy of epigenetic characteristics of wild plant populations in natural scenarios has so far hindered interpretations of natural patterns of epigenetic variation in an evolutionary framework [20], [28] This applies to instances of epigenetic differentiation between populations of the same species living in contrasting environments [14], [15], [29], [30], whose evolutionary significance will critically depend on whether such potentially adaptive, epigenetic structuring persist across successive generations [4], [20], [31]. Given the alternation of diploid and haploid generations that characterizes the life cycle of higher plants, and the epigenetic responsiveness of germline to changes in the environment [23] such as those associated with transplants from natural to artificial environments, transplant experiments are prone to produce biased or distorted views of epigenetic inheritance
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