Stronger transgenerational plasticity in clonal compared to sexual offspring of Fragaria vesca: effects of drought, elevated temperature and CO2

Abstract Background and Aims Climate change threatens plant species, potentially exceeding their adaptive capacities. Plants may adapt to rapid environmental changes through transgenerational plasticity (TGP), where adaptive traits are passed to their offspring via proteins, hormones and epigenetic modifications such as DNA methylation. The extent of TGP and its ecological implications may differ between sexual and clonal reproductive modes due to differences in the inheritance of DNA methylation and provisioning. However, it remains unclear whether TGP differs between these reproductive modes and the role of DNA methylation. Addressing this gap is crucial, as higher TGP in clonal propagation could compensate for low genetic variation and help these plants in adapting to rapid environmental changes. Methods We assessed the adaptive potential of woodland strawberry (Fragaria vesca), a widely distributed herb with both clonal and sexual reproduction, in response to environmental conditions expected by the end of the 21st century: a temperature rise of 4 °C, a 400 ppm rise in atmospheric CO2 and periodic droughts. We quantified ecologically relevant phenotypic traits and examined whole-genome DNA methylation patterns in parents and their clonal and sexual offspring. Key Results We found evidence for TGP induced by the parental environment, with a stronger overall effect observed in clonal compared to sexual offspring. Specifically, parental exposure to current temperature and CO2 conditions prompted adaptive TGP, particularly in clonal offspring. Additionally, adaptive TGP was observed exclusively in clonal offspring in response to a combination of elevated parental temperature and drought conditions. Finally, we found a higher inheritance of DNA methylation marks in clonal than in sexual offspring. Conclusions These results suggest that while TGP via DNA methylation can influence clonal plant adaptation to future conditions, it remains uncertain whether this influence will consistently result in adaptive outcomes. Moreover, TGP would probably be more important in clonal than in sexual reproduction.