Tidal air exposure thresholds in seagrass survival: photodamage-antioxidant imbalance and anthocyanin accumulation associated with Enhalus acoroides zonation limits.

Seagrass meadows are ecologically vital yet increasingly threatened marine ecosystems. Identifying the mechanisms that determine their spatial distribution, particularly in shallow coastal zones, is essential for effective conservation and management. In this study, we investigate the physiological and molecular mechanisms underlying seagrass zonation in Enhalus acoroides using field surveys, controlled experiments, and multi-omics analyses. Our findings demonstrate that seagrass distribution is constrained to areas experiencing ≤4 h of daily air exposure, beyond which plant viability sharply declines. While shoot density remained relatively stable, leaf length was negatively correlated with air exposure. While high-light exposure led to transient photoinhibition, seagrass photosynthetic efficiency (FV/FM) recovered under submersion. Furthermore, laboratory experiments revealed that air exposure beyond 4 h resulted in irreversible physiological damage. Transcriptome and metabolome analyses revealed systemic downregulation of photosynthesis-related genes in shallow populations, along with activation of antioxidant defenses (e.g., APX) and accumulation of stress-related metabolites (e.g., cyanidin-3-O-glucoside increased 5.8-fold via CHS1 upregulation). These results suggest that photodamage-antioxidant imbalance and anthocyanin accumulation may contribute to the zonation limits of E. acoroides. Our study proposes ≤4 h of tidal air exposure as a threshold for seagrass conservation and identifies CHS1 expression and cyanidin accumulation as potential molecular biomarkers for monitoring ecosystem health. By integrating physiological thresholds with molecular diagnostics, this research provides a foundation for adaptive conservation and restoration strategies in seagrass ecosystems under accelerating marine environmental change.