Interannual Covariation of Rhizosphere Microbiomes and Plant Performance in Coastal Saline–Alkali Soils Ameliorated by Nitraria tangutorum

Abstract

Soil salinization severely threatens agricultural productivity and ecosystem sustainability, particularly in coastal regions. Halophyte-based phytoremediation is a promising strategy, yet how rhizosphere soil legacy effects at different restoration ages influence subsequent plant growth and microbial communities remains poorly understood. Here, rhizosphere soils of Nitraria tangutorum at 1- (BC-1), 2- (BC-2), and 3-year (BC-3) restoration stages and non-rhizosphere bulk soil (CK) were sampled, with alfalfa cultivated as a bioindicator to assess soil physicochemical properties, plant growth, stress physiology, and rhizosphere microbiota. With increasing restoration age, rhizosphere soil shifted from a state of salt accumulation and nutrient deficiency to one of salt depletion and nutrient enrichment, with BC-3 exhibiting the highest soil organic matter, total phosphorus, and alkali-hydrolyzable nitrogen and the lowest total salt and soluble Na+. Alfalfa growth was suppressed in BC-1 and BC-2 soils, but significantly promoted in BC-3, accompanied by the lowest malondialdehyde and proline content, indicating effective alleviation of oxidative and osmotic stress. Microbial diversity peaked at BC-2, whereas the total proportion of halotolerant bacteria declined from 0.44 (BC-1) to 0.34 in BC-3 (significantly lower than CK), suggesting a successional shift from a stress-dominated community toward a functionally specialized consortium. Regression analyses identified soluble sodium as the variable most strongly associated with growth inhibition (R2 > 0.80) for plant height and root length. We suggest soluble sodium may represent the principal factor associated with growth inhibition and that a positive-feedback loop among plant Na+ sequestration, microbial carbon sequestration, and soil maturation may sustain long-term saline–alkali soil improvement. These findings suggest a three-stage successional mechanism and highlight the critical role of restoration age in mediating plant–microbe–soil synergistic remediation of coastal saline soils.