Mangrove trees exhibit unique adaptations that enable them to tolerate osmotic stress, high temperatures, and nutrient limitations, making them an ideal model for studying rapid molecular responses to environmental stress—an essential factor in keeping pace with climate change. However, the transcriptomic and epigenomic mechanisms underlying their stress responses and local adaptation remain poorly understood.

In Okinawa, Japan, near the northernmost range limit of mangroves, we investigated the roles of genomic, transcriptomic, and epigenetic modifications in stress adaptation along a local salinity gradient. This study focuses on Bruguiera gymnorhiza (Rhizophoraceae), a mangrove species that thrives across varying salinity levels but exhibits stunted growth in high-salinity oceanic environments. We examined two patches of B. gymnorhiza within the same population—one in brackish water (15 psu) and the other in an ocean-facing habitat (34 psu). Despite their proximity, individuals from these patches display striking morphological and physiological differences, which correspond with differentially expressed stress-related genes based on transcriptomic analysis.

Additionally, trees in high-salinity environments exhibited widespread genome-wide DNA hypermethylation, particularly in transposable elements (TEs), despite no significant population genetic differentiation. This epigenetic structuring was accompanied by transcriptional changes in chromatin modifier genes, suggesting a key role for epigenomic regulation in mangroves’ osmotic stress response. To explore whether these epigenetic modifications persist, we conducted a reciprocal transplant experiment by exchanging propagules between the two sites. Whole-genome methylation and transcriptome analysis revealed that DNA methylation and gene expression patterns persist transiently for several weeks post-transplantation, suggesting a form of environmental memory.

Our findings offer new insights into the molecular mechanisms underlying wild trees' ability to adapt to novel stressors, contributing to a broader understanding of their potential resilience to climate change.