Sex-related osmotic adjustment strategies underpin desiccation tolerance in the intertidal seaweed Neoporphyra haitanensis.

Desiccation stress constitutes a significant environmental challenge for macroalgae inhabiting the intertidal zone, in which recurrent tidal cycles shape their physiological tolerance. However, sex-related responses to desiccation in macroalgae remain largely unexplored. In this study, we integrated physiological measurements with transcriptomic and metabolomic analyses to investigate sex-related responses of Neoporphyra haitanensis to desiccation stress. Physiological results revealed that males possessed a stronger osmotic adjustment capacity than females under desiccation. Consistently, non-invasive micro-test results confirmed that males exhibited superior Na+ and Ca2+ extrusion abilities, while maintaining a higher K+ level. Multi-omics further uncovered sex-based molecular strategies to cope with desiccation stress. Males displayed higher trehalose levels with up-regulated expression of trehalose-6-phosphate synthase, the key enzyme in trehalose synthesis. In contrast, females displayed higher proteasome gene expression and greater amino acid accumulation levels, suggesting a reliance on amino acid accumulation driven by protein degradation for osmotic protection. Moreover, males displayed higher transcript levels of ion transport-related genes, including genes encoding sodium/hydrogen exchangers (NHXs) and K+-stimulated pyrophosphate-energized sodium pumps (HppAs), which facilitated toxic ion exclusion and stable K+ retention. Overall, these findings revealed the critical role of sex-specific osmotic adjustment strategies in desiccation tolerance of N. haitanensis, driven by osmotic adjustment strategies integrating organic osmolyte synthesis and inorganic ion transport. This study provides new insights into the sex-related adaptive mechanisms of macroalgae and has valuable implications for understanding population dynamics under environmental stresses and for guiding strain selection in mariculture.