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Abstract
<title>Abstract</title> <p> Background Global soil salinization is intensifying, yet the mechanisms determining whether beneficial plant–microbe symbioses remain functional under extreme ionic stress remain poorly understood. Methods Using the halophyte <italic>Suaeda salsa</italic> and two ecologically distinct dark septate endophytes (DSEs), we evaluated symbiotic performance across a Na <sub>2</sub> SO <sub>4</sub> gradient (0-0.4 M) by integrating physiological, ionomic, rhizosphere, and untargeted metabolomic analyses. Symbiotic outcomes were strongly dependent on fungal habitat adaptation. Results The halophytic isolate <italic>Alternaria chlamydospora</italic> SC11 maintained stable colonization and consistently enhanced plant survival and growth under increasing salinity, whereas the non-adapted isolate As17463 progressively lost functionality. SC11 sustained K, N, and P homeostasis despite high Na <sup>+</sup> accumulation, preserved root structural integrity and rhizosphere enzymatic activity, and promoted persistent activation of pyrimidine and nucleotide-sugar metabolism. Integrative analyses revealed strong coupling between rhizosphere properties and host metabolic responses, indicating coordinated regulation across the soil-root-plant continuum. Conclusion Persistent colonization by habitat-adapted DSEs strengthens the osmoregulatory capacity, nutrient homeostasis, and functional stability of <italic>S. salsa</italic> under severe sulfate salinity. This study provides mechanistic criteria for selecting effective fungal inoculants and offers theoretical guidance and practical support for microbial-assisted restoration and sustainable management of saline-alkali environments. </p>