Epigenetics: a potential mechanism for clonal plant success

Abstract

Clonality in plants is widespread and includes species that span temporally and spatially heterogeneous environments. Yet, theory predicts that clonally reproducing plants evolve at slower rates, risk accumulating more mutations than sexuals, and potentially lack the benefits of DNA repair mechanisms afforded by meiosis. Does the apparent success of clonal plants contradict the severe costs of clonal reproduction suggested by theory? We examine how epigenetics may confer ecological advantages to clonal plants that could outweigh these evolutionary costs. Relying to various degrees on vegetative reproduction, the capacity to conserve or reverse gene regulation changes over cell divisions has clear potential for optimization of plasticity and acclimation in response to environmental variation encountered. Clonal plants may be one of the best examples of organisms taking advantage of epigenetic acclimation as an alternative to the slower mechanisms of adaptation through natural selection. If epigenetic processes are important in matching organismal response to the environment, this may prove to be a mechanism that will buffer plants against the challenges of current and future rapid environmental changes.Theory predicts that clonally reproducing plants evolve at slower rates, risk accumulating more mutations than sexuals, and potentially lack the benefits of DNA repair mechanisms afforded by meiosis mutational meltdown, Lynch et al. 1993; Muller's ratchet, Muller 1964). This suggests they are successful for evolutionarily short periods of time and under stable environments (Silvertown 2008). Yet, clonality in plants is widespread and includes species that span heterogeneous environments, are long-lived and face a range of environmental changes during their lifetime, and have survived major climatic changes such as those of the Pleistocene. Today, clonal plants make up perhaps 40 % of our planet's flora (Tiffney and Niklas 1985) dominate grasslands, deserts, wetlands, and tundras as major primary producers, comprise some of our most important crops, including almost all bioenergy crops, and feature many of the most invasive plants. Some of earth's largest, tallest, oldest, most extensive, and rarest plants are clonal. Being extremely modular organisms, clonal plants, whether large integrated clones, or fragmented into Communicated by C. Holzapfel.

Genetic and epigenetic changes during the invasion of a cosmopolitan species (Phragmites australis)

“…An increasing number of studies have also demonstrated the common existence and significant role of epigenetic variation in plant populations of herbs (Foust et al., 2016; Herrera, Medrano, & Bazaga, 2014; Medrano et al., 2014; Preite et al., 2015; Schulz, Eckstein, & Durka, 2014), shrubs (Avramidou, Ganopoulos, Doulis, Tsaftaris, & Aravanopoulos, 2015; Herrera & Bazaga, 2013, 2016), and trees (Guarino, Cicatelli, Brundu, Heinze, & Castiglione, 2015; Gugger, Fitz‐Gibbon, PellEgrini, & Sork, 2016; Lira‐Medeiros et al., 2010; Platt, Gugger, Pellegrini, & Sork, 2015; Sáez‐Laguna et al., 2014) under natural conditions. Therefore, epigenetic variation can be a very important mechanism for invasive plant success in a broad range of environments (Douhovnikoff & Dodd, 2014; Richards, Schrey, & Pigliucci, 2012). …”

Evolutionary Biology: Biodiversification from Genotype to Phenotype

“…Epigenetic drift refers to the differential acquisition of epigenetic marks in organisms with the same genetic constitution and, naturally, affected by different or even slightly different environmental sceneries and ecological interactions. Thus, epigenetic variation acquired in long-lived asexual organisms may critically influence genotype development and plasticity by differential gene regulation, creating genetic differences among clonemates (e.g., Verhoeven and Preite 2013;Douhovnikoff and Dodd 2015). The age and growth rates of each particular genet/genotype will influence on the relative impact of those gene-based processes on clones' genetic composition.…”

“…Thus, not only genotypic but also epigenetic variations are factors enhancing genotype plasticity and adaptation (e.g., Verhoeven and Preite 2013;Douhovnikoff and Dodd 2015), and hence the capacity of asexual plants to cope better with environmental heterogeneity and niche gradients, promoting the dispersal of fitted genotypes and contributing to the success observed in clonal plants.…”

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

“…Variation in DNA methylation is not completely independent from the genome, and epialleles can have different degrees of autonomy from the genotype (Berbel‐Filho, Rodríguez‐Barreto, Berry, Garcia de Leaniz & Consuegra, ; Richards ; Dubin et al, ; Leung, Breton, & Angers, ). In addition, in some plants and animals, individuals with low levels of heterozygosity display high levels of genome‐wide DNA methylation variation (Liebl, Schrey, Richards, & Martin, ; Richards, Schrey, & Pigliucci, ; Schrey et al, ), suggesting that DNA methylation could contribute to the adaptation of organisms with limited genetic diversity to environmental change (Castonguay & Angers, ; Douhovnikoff & Dodd, ; Liebl et al, ; Schrey et al, ; Verhoeven & Preite, ).…”