Salinity-induced variations in wheat biomass are regulated by the Na⁺:K⁺ ratio, root exudates, and keystone species

Salt stress can limit crop productivity, and there are differences in salt tolerance among plant varieties; however, we lack a comprehensive understanding of how keystone species obtained from different plant varieties under salt stress change plant biomass by driving root exudate secretion and regulating the Na⁺:K⁺ ratio. We conducted a pot experiment for three wheat varieties (JiMai32 (JM32), XiaoYan60 (XY60), and ShanRong3 (SR3)) under saline/nonsaline soil conditions. Salt stress tended to significantly reduce wheat biomass, and the biomass reduction rates of the different varieties decreased in the order JM32 < XY60 < SR3. The compositions of the bacterial and fungal communities in the root endosphere, rhizosphere and bulk soil were measured, and salt-induced microbial taxa were isolated to identify keystone species from the co-occurrence networks and to study their effects on physiological responses to salinity in wheat varieties. We observed that root exudates participated in the regulation of the Na⁺:K⁺ ratio, thereby affecting wheat biomass, and this process was regulated by keystone species. JM32 was enriched in microorganisms that promote plant growth and resistance to salt stress, such as Burkholderiales, Sordariomycetes, Alteromonadaceae, Acremonium, and Dokdonella, and inhibited microorganisms that are sensitive to the environment (salt, nutrients) and plant pathogens, such as Nocardioidaceae, Nitrospira, Cytophagaceae, Syntrophobacteriaceae, and Striaticonidium. XY60 inhibited microorganisms with biological control and disease inhibition potential, such as Agromyces and Kaistobacter. SR3-enriched pathogens, such as Aurantimonadaceae and Pseudogymnoascus, as well as microorganisms with antagonistic pathogen potential and the ability to treat bacterial infections, such as RB41 and Saccharothrix, were inhibited. Our results confirmed the crucial function of salt-induced keystone species in enhancing plant adaptation to salt stress by driving root exudate secretion and regulating the Na⁺:K⁺ ratio, with implications for exploring reasonable measures to improve plant salt tolerance.