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.