Drought-Induced Epigenetic Memory in the cambium of Poplar Trees persists and primes future stress responses

Understanding how perennial plants such as trees perceive, integrate and memorize environmental stresses like water deficit is crucial in the context of climate change.

We investigated short-term and transannual memory of water deficit in cambium derived tissues of poplars ( Populus spp .) using two contrasting genotypes and four genetically modified epitypes with altered DNA methylation machinery.

We found persistent changes in hormone profiles, gene expression and DNA methylation one week after stress relief, consistent with a molecular short-term stress memory. These signatures revealed distinct adaptive strategies between genotypes and marked variability between epitypes, demonstrating that both genetic and epigenetic backgrounds drive stress memory.

Trees already exposed to water deficit in Year 1 showed distinct physiological and molecular responses when subjected to a second water deficit in Year 2, supporting the persistence of a long-term trans-annual memory possibly involved in tree priming. The higher molecular plasticity observed in the intrinsically more sensitive genotype contrasted with the higher stability observed in the intrinsically more tolerant genotype. The number of memory genes was limited, but the results suggested that stable drought-induced DNA methylation changes, particularly in the CG context, contribute to long-term stress imprinting.

Our findings highlight the cambium as a reservoir for stress memory in trees and suggest that DNA methylation dynamics shaped by genetic predisposition, acting through cis- and trans-regulatory routes, may help fine-tuning growth vs. survival strategies across longer time frames. These insights open perspectives for harnessing epigenetic variation in tree breeding and management under increasing drought frequency.