Unraveling the effects of Caulerpa metabolites on Posidonia oceanica apical and vertical shoots at physiological and molecular level

Invasive Caulerpa species produce bioactive metabolites that can disrupt seagrass physiology, yet their specific effects on different shoot types remain poorly understood. This study examines the physiological and molecular responses of Posidonia oceanica apical and vertical shoots to two major Caulerp a-derived metabolites: caulerpenyne (CYN) from C. taxifolia and caulerpin (CAU) from C. cylindracea . Exposure to 25 μM CYN led to a 90 % mortality in adult leaves of apical shoots and significantly inhibited juvenile leaf formation in vertical shoots, despite no effect on chlorophyll content. Conversely, 25 μM CAU stimulated juvenile leaf emergence but reduced adult leaf elongation by 93% and impaired chlorophyll content in both shoot types. Proteomic analysis revealed significant protein downregulation in CYN-exposed apical shoots, particularly those involved in photosynthesis, stress response, brassinosteroid signaling, and fatty acid metabolism. CYN also upregulated lactate dehydrogenase and glyoxalase while disrupting Ca²⁺/calmodulin signaling. CAU exposure led to a decrease in histone H4 but increased the abundance of protective proteins, including catalase, phenylalanine ammonia-lyase, and Hsp70, mitigating oxidative damage. In vertical shoots, CYN enhanced fatty acid biosynthesis, lipoxygenase activity, phosphorylation pathways, and sulfur metabolism, while CAU suppressed methylation and increased histone H3. Apical shoots exhibited greater susceptibility to the phytotoxic effects of CYN than vertical shoots, while both showed great resilience to CAU. Given the critical role of apical shoots in clonal propagation, their heightened vulnerability to CYN may contribute to the decline of P. oceanica meadows in C. taxifolia -invaded regions. These findings reveal the molecular and physiological mechanisms of seagrass responses to invasive macroalgal toxins. • Apical shoots are highly vulnerable to caulerpenyne than vertical shoots. • Caulerpenyne disrupts photosynthesis and induces stress pathways. • Vertical shoots exhibited lower tolerance to caulerpin than apical shoots. • Caulerpin induces protective proteins against oxidative stress in apical shoots. • Apical shoot vulnerability drives the decline of C. taxifolia invaded meadow.