Sex-related differences in photosynthesis, energy metabolism, and antioxidant regulation of Neoporphyra haitanensis to ultraviolet-B stress

Abstract

Increased ultraviolet-B (UVB) radiation due to human activities poses a considerable threat to all exposed organisms. While sex-related differences in stress responses have been observed in many plant species, little is known about whether such differences exist in macroalgae. In this study, we investigated the physiological, transcriptomic, and metabolomic responses of male and female Neoporphyra haitanensis under UVB stress and subsequent recovery. The physiological results indicated that UVB stress strongly inhibited the photosynthetic pigment content and activity in females compared to those in males. Consequently, females exhibited higher levels of reactive oxygen species (ROS) and malondialdehyde (MDA) production under UVB stress and recovery. In contrast, males exhibited stronger antioxidant enzyme activity to alleviate the oxidative stress under UVB stress. Transcriptomic analysis revealed that UVB caused a greater downregulation of genes related to pigment synthesis, photosystems, and carbon fixation in females, including genes encoding magnesium protoporphyrin IX methyltransferase (ChlM), phycoerythrin (PE), and glyceraldehyde-3-phosphate dehydrogenase (GAPDH). Furthermore, males possessed a stronger photosynthetic recovery capacity, as a greater number of photosynthesis-related genes were significantly upregulated in males after recovery. Under UVB stress, the expression of genes encoding key enzymes involved in glycolysis, the pentose phosphate pathway, and the tricarboxylic acid cycle was higher in males than in females, indicating a stronger energy metabolism capacity in males. Metabolomic data emphasized the protective role of nonenzymatic antioxidants, particularly flavonoids, with females accumulating more methylated flavonoids and flavonoid glycosides after recovery than males. Overall, these findings highlight sex-related differences in photosynthesis, energy metabolism, and antioxidant regulation in N. haitanensis under UVB stress and recovery. These results contribute to our understanding of how sex differences in macroalgae influence their population survival under increased UVB radiation and provide insights into their potential adaptive responses to ongoing climate change.