Epigenetic and transcriptional landscape of heat-stress memory in woodland strawberry (Fragaria vesca)

We have previously reported that different stresses can lead to substantial DNA methylation changes in strawberry. Here, we wanted to assess the heritability of heat-stress induced DNA methylation and transcriptional changes following asexual and sexual reproduction in a plant. Woodland strawberry (Fragaria vesca) is an ideal model to study epigenetic inheritance in plants because it presents two modes of reproduction: sexual and asexual. Here we wanted to assess if heat-stress induced DNA methylation changes can be transmitted via asexual reproduction and whether past stresses can also affect sexually propagated progenies. Our genome-wide study provides evidence for a memory acquisition and maintenance in F. vesca. We found that certain DNA methylation changes can stably be transmitted over at least three asexual generations. Finally, the first sexual generation by selfing from stressed maternal and their respective non-stressed asexual daughter plants showed both shared and unique stress responses. This suggests that an acquired molecular memory from the previous heat-stress event was transmitted. This molecular memory might be involved in functional plasticity and stress adaption, an important aspects that will have to be investigated in future studies. Finally, these findings may contribute to novel approaches that may contribute to the breeding of climate-ready plants. IN A NUTSHELLO_ST_ABSBackgroundC_ST_ABSWith ongoing climate change, natural plant populations and crops are facing stress situations more frequently and at higher intensity. These unfavorable growing conditions force plants to develop strategies to adapt to persist. One of these strategies involves epigenetic mechanisms which can affect the activity of genes without altering the actual DNA sequence. These molecular modifications can be retained by plants as a molecular "memory" which might be used later to better respond to a stressful event. QuestionIs there multi-generational persistence of heat-stress induced epigenetic patterns in strawberry and are heritable epigenetic changes associated with stress adaptation? FindingsWe found that the strawberry methylome and transcriptome respond with a high level of flexibility to heat-stress. In addition, we took advantage of the two reproductive modes of strawberry (asexual and sexual) to evaluate the acquisition and maintenance of molecular stress memory. We showed how specific DNA methylation and gene expression changes can persist for a long time in progeny plants. We found that the asexual, and seemingly also sexual progenies can retain information in the genome of a past stressful condition that was encountered by its progenitor. Next stepsOur work presents valuable epigenetic and transcriptional screening data to understand plant memory maintenance and transmission over generations. The most important next step will be to assess if heritable stress-induced epigenetic changes can contribute to stress adaptation through a plant competition experiment in natural environments. One sentence summaryStrawberry can transmit molecular stress-memory at the DNA methylation and transcriptional level over multiple generations which may play an important role in stress adaptation.