Plants must quickly adapt to a changing environment in order to maintain their fitness. One rapid adaptation mechanism that promotes plasticity is epigenetic memory, which may provide long-lived organisms the precious time needed to adapt to climate change. In this study, we used the perennial plant Fragaria vesca as a model to determine how the methylome and transcriptome adapt to elevated temperatures (28 vs. 18 ˚C) over three asexual generations. Changes in flowering time, stolon number, and petiole length were induced in responses to temperature treatment in one or more ecotypes after three asexual generations in a manner indicative of an epigenetic memory. Induced methylome changes differed between four different ecotypes from Norway, Iceland, Italy, and Spain, but there were also some shared responses. Elevated temperature conditions induced significant phenotypic and methylation changes, particularly in the Norwegian ecotype. Most of the differentially methylated regions (DMRs) were in the CHG context, and most CHG and CHH DMRs were hypermethylated. Notably, the four ecotypes shared only eight CHG DMR peaks. Several differentially methylated genes (DMGs) also showed a change in gene expression. Ecotype-specific methylation and expression patterns were observed for genes related to gibberellin metabolism, flowering time, epigenetics. Furthermore, when repetitive elements (REs) were found near (2 kb) or inside a gene, they showed a negative correlation with gene expression. In conclusion, phenotypic changes induced by elevated temperatures during asexual reproduction were accompanied by changes in DNA methylation patterns. Also, positional influences of REs impacted gene expression, indicating that DNA methylation may be involved in both general and ecotype-specific phenotypic plasticity in F. vesca.
Temperature conditions experienced during embryogenesis and seed development may induce epigenetic changes that increase phenotypic variation in plants. Here we investigate if embryogenesis and seed development at two different temperatures (28 vs. 18°C) result in lasting phenotypic effects and DNA methylation changes in woodland strawberry (Fragaria vesca). Using five European ecotypes from Spain (ES12), Iceland (ICE2), Italy (IT4), and Norway (NOR2 and NOR29), we found statistically significant differences between plants from seeds produced at 18 or 28°C in three of four phenotypic features investigated under common garden conditions. This indicates the establishment of a temperature‐induced epigenetic memory‐like response during embryogenesis and seed development. The memory effect was significant in two ecotypes: in NOR2 flowering time, number of growth points and petiole length were affected, and in ES12 number of growth points was affected. This indicates that genetic differences between ecotypes in their epigenetic machinery, or other allelic differences, impact this type of plasticity. We observed statistically significant differences between ecotypes in DNA methylation marks in repetitive elements, pseudogenes, and genic elements. Leaf transcriptomes were also affected by embryonic temperature in an ecotype‐specific manner. Although we observed significant and lasting phenotypic change in at least some ecotypes, there was considerable variation in DNA methylation between individual plants within each temperature treatment. This within‐treatment variability in DNA methylation marks in F. vesca progeny may partly be a result of allelic redistribution from recombination during meiosis and subsequent epigenetic reprogramming during embryogenesis.
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