Contrasting thermal histories modulate Posidonia oceanica ecotypes responses to simulated present-day and future acute warming events

Marine heatwaves (MHWs), intensified by climate change, severely threaten Mediterranean seagrasses such as Posidonia oceanica . We investigated how local thermal history along the Tyrrhenian and Ionian coasts shapes resilience to MHWs. In a controlled mesocosm experiment, plants from two genetically distinct populations originating from a warmer Tyrrhenian site and a colder Ionian site were exposed for 10 days to three thermal scenarios: PAST (26 ± 0.5 °C), TODAY (29 ± 0.5 °C), and FUTURE (31 ± 0.5 °C), followed by a 10-day recovery at 26 ± 0.5 °C. Plants from the colder Ionian site showed vulnerability under FUTURE conditions, with 50% mortality, chlorophyll reorganization and loss, reduced growth, and impaired recovery. In contrast, plants from the warmer Tyrrhenian site displayed resilience, maintaining photosynthetic performance and regrowth capacity. These contrasting responses were associated with population-specific leaf meristematic reprogramming, revealed by label-free quantitative proteomics of apical and vertical meristems. In vulnerable plants from the colder Ionian site, meristems exhibited metabolic imbalance and disrupted proteostasis, including upregulation of heat-shock proteins and translation factors such as eIF-5B, together with reduced abundance of key metabolic enzymes. Conversely, resilient plants from the warmer Tyrrhenian site showed coordinated proteomic shifts enhancing photosynthesis through RuBisCO activase, energy metabolism, antioxidant defence, protein turnover, and recovery capacity. Our results confirmed that local thermal history drives divergent stress responses and population-specific vulnerability to warming. These findings identify intraspecific adaptive variation as a key determinant of seagrass persistence under climate change and support region-specific conservation strategies, particularly for vulnerable meadows.