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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., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Sammarco, Münzbergová and Latzel.)

Clonal plants in heterogeneous environments can benefit from their habitat selection behavior, which enables them to utilize patchily distributed resources efficiently. It has been shown that such behavior can be strongly influenced by their memories on past environmental interactions. Epigenetic variation such as DNA methylation was proposed to be one of the mechanisms involved in the memory. Here, we explored whether the experience with Ultraviolet B (UV-B) radiation triggers epigenetic memory and affects clonal plants' foraging behavior in an UV-B heterogeneous environment. Parental ramets of Glechoma longituba were exposed to UV-B radiation for 15 days or not (controls), and their offspring ramets were allowed to choose light environment enriched with UV-B or not (the species is monopodial and can only choose one environment). Sizes and epigenetic profiles (based on methylation-sensitive amplification polymorphism analysis) of parental and offspring plants from different environments were also analyzed. Parental ramets that have been exposed to UV-B radiation were smaller than ramets from control environment and produced less and smaller offspring ramets. Offspring ramets were placed more often into the control light environment (88.46% ramets) than to the UV-B light environment (11.54% ramets) when parental ramets were exposed to UV-B radiation, which is a manifestation of "escape strategy." Offspring of control parental ramets show similar preference to the two light environments. Parental ramets exposed to UV-B had lower levels of overall DNA methylation and had different epigenetic profiles than control parental ramets. The methylation of UV-B-stressed parental ramets was maintained among their offspring ramets, although the epigenetic differentiation was reduced after several asexual generations. The parental experience with the UV-B radiation strongly influenced foraging behavior. The memory on the previous environmental interaction enables clonal plants to better interact with a heterogeneous environment and the memory is at least partly based on heritable epigenetic variation., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2021 Quan, Latzel, Tie, Zhang, Münzbergová, Chai, Liu and Yue.)

Active foraging for patchy resources is a crucial feature of many clonal plant species. It has been recently shown that plants' foraging for resources can be facilitated by anticipatory behavior via association of resource position with other environmental cues. We therefore tested whether clones of Fragaria vesca are able to associate and memorize positions of soil nutrients with particular light intensity, which will consequently enable them anticipating nutrients in new environment. We trained clones of F. vesca for nutrients to occur either in shade or in light. Consequently, we tested their growth response to differing light intensity in the absence of soil nutrients. We also manipulated epigenetic status of a subset of the clones to test the role of DNA methylation in the anticipatory behavior. Clones of F. vesca were able to associate presence of nutrients with particular light intensity, which enabled them to anticipate nutrient positions in the new environment based on its light intensity. Clones that had been trained for nutrients to occur in shade increased placement of ramets to shade whereas clones trained for nutrients to occur in light increased biomass of ramets in light. Our study clearly shows that the clonal plant F. vesca is able to relate two environmental factors, light and soil nutrients, and use this connection in anticipatory behavior. We conclude that anticipatory behavior can substantially improve the ability of clonal plants to utilize scarce and unevenly distributed resources.

Transgenerational effects (TGE) can modify phenotypes of offspring generations playing thus a potentially important role in ecology and evolution of many plant species. These effects have been studied mostly across generations of sexually reproducing species. A substantial proportion of plant species are however reproducing asexually, for instance via clonal growth. TGE are thought to be enabled by heritable epigenetic modification of DNA, although unambiguous evidence is still scarce. On the clonal herb white clover ( Trifolium repens ), we tested the generality of clonal TGE across five genotypes and five parental environments including soil contamination and above-ground competition. Moreover, by genome wide-methylation variation analysis we explored the role of drought, one of the parental environments that triggered the strongest TGE. We tested the induction of epigenetic changes in offspring generations using several intensities and durations of drought stress. We found that TGE of different environments were highly genotype specific and all tested environments triggered TGE at least in some genotypes. In addition, parental drought stresses triggered epigenetic change in T. repens and most of the induced epigenetic change was maintained across several clonal offspring generations. We conclude that TGE are common and genotype specific in clonal plant T. repens and potentially under epigenetic control.

Environmentally induced epigenetic change enables plants to remember past environmental interactions. If this memory capability is exploited to prepare plants for future challenges, it can provide a basis for highly sophisticated behavior, considered intelligent by some. Against the backdrop of an overview of plant intelligence, we hypothesize: (1) that the capability of plants to engage in such intelligent behavior increases with the additional level of complexity afforded by clonality, and; (2) that more faithful inheritance of epigenetic information in clonal plants, in conjunction with information exchange and coordination between connected ramets, is likely to enable especially advanced intelligent behavior in this group. We therefore further hypothesize that this behavior provides ecological and evolutionary advantages to clonal plants, possibly explaining, at least in part, their widespread success. Finally, we suggest avenues of inquiry to enable assessing intelligent behavior and the role of epigenetic memory in clonal species.