Unraveling synergistic and antagonistic effects of simultaneous versus single hypoxia-salt conditions in an evolutionary adapted plant species

Plants frequently encounter simultaneous stressors, requiring complex adaptive responses across regulatory levels. Although morphological and metabolic effects of combined hypoxia-salt stress are known in halophytes, transcriptional impacts remain largely unexplored. This study uses RNA sequencing to analyze Salicornia europaea which is an intertidal salt-marsh plant naturally adapted to these conditions. Combined hypoxia-salt stress induced a distinct gene expression profile in which 16% of genes were exclusively changed. Synergistic, antagonistic, and additive effects were observed across all evaluated functional pathway categories. A data-driven analysis of carbohydrate metabolism, cellular respiration/fermentation, and amino acid pathways revealed that antagonistic effects were more prevalent than synergistic ones in both roots and shoots. Notably higher gene expression levels during hypoxia-salt of sucrose biosynthesis (consistent with salt), sucrose synthase ( SUS ) and trehalose-6-phosphate phosphatase ( TPP , consistent with hypoxia) indicate enhanced sucrose and trehalose metabolism. The parallel down-regulation of invertase genes (consistent with hypoxia) suggests strategic carbon flux redistribution for optimized energy supply. Under hypoxic conditions, lactate dehydrogenase ( LDH ) expression was up-regulated, indicating active lactate fermentation rather than ethanol production via alcohol dehydrogenase ( ADH ). Enhanced proline synthesis under combined stress suggests improved osmoprotection. These insights into transcriptional reprogramming under single and combined hypoxia-salt conditions emphasize the intricate regulatory strategies plants utilize to manage concurrent stressors, showcasing their ability to adapt and develop stress resilience.