DNA Methylation Can Mediate Local Adaptation and Response to Climate Change in the Clonal Plant Fragaria vesca: Evidence From a European-Scale Reciprocal Transplant Experiment

Abstract

The ongoing climate crisis represents a growing threat for plants and other organisms. However, how and if plants will be able to adapt to future environmental conditions is still debated. One of the most powerful mechanisms allowing plants to tackle the changing climate is phenotypic plasticity, which can be regulated by epigenetic mechanisms. Environmentally induced epigenetic variation mediating phenotypic plasticity might be heritable across (a)sexual generations, thus potentially enabling rapid adaptation to climate change. Here, we assessed whether epigenetic mechanisms, DNA methylation in particular, enable for local adaptation and response to increased and/or decreased temperature of natural populations of a clonal plant, Fragaria vesca (wild strawberry). We collected ramets from three populations along a temperature gradient in each of three countries covering the southern (Italy), central (Czechia), and northern (Norway) edges of the native European range of F. vesca. After clonal propagation and alteration of DNA methylation status of half of the plants via 5-azacytidine, we reciprocally transplanted clones to their home locality and to the other two climatically distinct localities within the country of their origin. At the end of the growing season, we recorded survival and aboveground biomass as fitness estimates. We found evidence for local adaptation in intermediate and cold populations in Italy and maladaptation of plants of the warmest populations in all countries. Plants treated with 5-azacytidine showed either better or worse performance in their local conditions than untreated plants. Application of 5-azacytidine also affected plant response to changed climatic conditions when transplanted to the colder or warmer locality than was their origin, and the response was, however, country-specific. We conclude that the increasing temperature will probably be the limiting factor determining F. vesca survival and distribution. DNA methylation may contribute to local adaptation and response to climatic change in natural ecosystems; however, its role may depend on the specific environmental conditions. Since adaptation mediated by epigenetic variation may occur faster than via natural selection on genetic variants, epigenetic adaptation might to some degree help plants in keeping up with the ongoing environmental crisis.

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

“…We suggest that the assumption is reasonable as it is generally accepted that the 5-azaC reduces DNA global methylation through the effect on DNA methyltransferases, an enzyme that bonds methyl group on DNA 128 , 129 . We have also provided an evidence in our previous studies that the foliar application of 5-azaC reduces overall DNA methylation level by 4–30% in treated Trifolium repens, Taraxacum brevicorniculatum and Fragaria vesca plants 42 , 54 , 130 . In a grass, Oryza sativa , foliar application of 75 µM 5-azaC solution reduced their overall DNA methylation level by more than 50% 131 .…”

DNA methylation dynamics during stress response in woodland strawberry (Fragaria vesca)

“…In rice, it was show that a high affinity potassium transporter gene is regulated by DNA methylation in its promoter in order to maintain potassium and sodium homeostasis during salinity stress [ 15 ]. A notable example concerning environmental impacts on DNA methylation is the documented loss of methylation at TEs at high altitudes and how it may contribute to local adaptation in natural populations of wild strawberry [ 16 , 17 ]. However, whether stress-induced methylome alterations at individual loci or across the entire genome contribute to heritable changes in DNA methylation patterns and adaptation remains uncertain.…”

Epigenetic variation in the Lombardy poplar along climatic gradients is independent of genetic structure and persists across clonal reproduction

“…One additional cause of phenotypic variation is epigenetic variation (Cubas et al ., 1999; Manning et al ., 2006; Xie et al ., 2015). Several studies have shown that epigenetic variation can be spatially structured among and within plant populations, and that such a structure can be associated with environmental variation and phenotypic differentiation (Lira-Medeiros et al, 2010; Medrano et al, 2014; Avramidou et al, 2015; Kawakatsu et al, 2016; de Kort et al, 2020; Boquete et al, 2021; Galanti et al, 2022, Sammarco et al, 2022). Although causal relationships remain to be studied, such observations suggest that epigenetic variation could contribute to the acclimation of plants to changes in environmental conditions.…”