Transcriptional memory of gene expression across generations participates in transgenerational plasticity of field pennycress in response to cadmium stress.

Transgenerational plasticity (TGP) occurs when maternal environments influence the expression of traits in offspring, and in some cases may increase fitness of offspring and have evolutionary significance. However, little is known about the extent of maternal environment influence on gene expression of offspring, and its relationship with trait variations across generations. In this study, we examined TGP in the traits and gene expression of field pennycress (Thlaspi arvense) in response to cadmium (Cd) stress. In the first generation, along with the increase of soil Cd concentration, the total biomass, individual height, and number of seeds significantly decreased, whereas time to flowering, superoxide dismutase (SOD) activity, and content of reduced glutathione significantly increased. Among these traits, only SOD activity showed a significant effect of TGP; the offspring of Cd-treated individuals maintained high SOD activity in the absence of Cd stress. According to the results of RNA sequencing and bioinformatic analysis, 10,028 transcripts were identified as Cd-responsive genes. Among them, only 401 were identified as transcriptional memory genes (TMGs) that maintained the same expression pattern under normal conditions in the second generation as in Cd-treated parents in the first generation. These genes mainly participated in Cd tolerance-related processes such as response to oxidative stress, cell wall biogenesis, and the abscisic acid signaling pathways. The results of weighted correlation network analysis showed that modules correlated with SOD activity recruited more TMGs than modules correlated with other traits. The SOD-coding gene CSD2 was found in one of the modules correlated with SOD activity. Furthermore, several TMGs co-expressed with CSD2 were hub genes that were highly connected to other nodes and critical to the network's topology; therefore, recruitment of TMGs in offspring was potentially related to TGP. These findings indicated that, across generations, transcriptional memory of gene expression played an important role in TGP. Moreover, these results provided new insights into the trait evolution processes mediated by phenotypic plasticity.

Increased epigenetic diversity and transient epigenetic memory in response to salinity stress in Thlaspi arvense.

Epigenetic diversity could play an important role in adaptive evolution of organisms, especially for plant species occurring in new and stressful environments. Thlaspi arvense (field pennycress), a valuable oilseed crop, is widespread in temperate regions of the northern hemisphere. In this study, we investigated the effect of salinity stress on the epigenetic variation of DNA methylation and epigenetic stress memory in pennycress using methylation-sensitive amplification polymorphism (MSAP) markers. We examined how the status of DNA methylation changes across individuals in response to salinity stress and whether such an effect of maternal stress could be transferred to offspring for one or two generations in nonstressed environments. Our results based on 306 epiloci indicated no consistent change of DNA methylation status in specific epiloci across individuals within the same conditions. In contrast, we found that the epigenetic diversity at population level increased significantly in response to the stimulation of salinity stress; and this "stimulation effect" could be transferred partially in the form of stress memory to at least two generations of offspring in nonstressed environments. In addition, we observed a parallel change in functionally important traits, that is, phenotypic variation was significantly higher in plants grown under salinity stress compared with those of control groups. Taken together, our results provide novel clues for the increased spontaneous epimutation rate in response to stress in plants, of potential adaptive significance.