DNA methylation mediates the clonal transmission of a primed epigenetic state in a marine plant

Rapid environmental change poses severe threats to plant survival, requiring rapid and effective adaptive responses. The capacity to retain a molecular memory of past stress via epigenetic mechanisms has emerged as a key strategy to buffer climate variability. Clonality may facilitate such inheritance by preventing the epigenetic reprogramming typically associated with meiosis. Using the fast-growing pioneer seagrass Cymodocea nodosa as a model, we conducted a controlled thermal priming experiment to test whether heat-induced epigenetic modifications persist through clonal propagation and contribute to resilience under ocean warming. Following acute heat stress (35°C), high-resolution reduced representation bisulfite sequencing (RRBS-seq) revealed divergent epigenomic reprogramming despite comparable photophysiological buffering. Not-primed shoots exhibited a broad, reactive methylome reconfiguration consistent with stress-induced epigenetic resetting. In contrast, primed plants showed a constrained and energetically efficient response, characterized by targeted modulation and selective regulation of key regulatory hubs. Importantly, these stress-induced DNA methylation signatures persisted through clonal propagation into newly formed shoots, indicating stable vegetative transmission of epigenetic states. Our findings demonstrate that thermal priming establishes a preparatory, vegetatively transmitted epigenetic state, providing a critical proof-of-concept for assisted evolution strategies to actively mitigate climate impacts and sustain marine ecosystems.