Ameliorating salt stress in tomato by a top-down approach of acclimatizing the rhizosphere microbiome

Soil salinization adversely impacts plant and soil health. While amendment with chemicals is not sustainable, the application of bioinoculants suffers from competition with indigenous microbes. Hence, microbiome-based rhizosphere engineering, focussing on acclimatization of rhizosphere microbiome under selection pressure to facilitate plant growth, exhibits promise. This study aimed to acclimatize a salt-susceptible tomato cultivar to high salt concentration through a microbiome-based top-down approach of rhizosphere engineering. Multiple passaging of the rhizosphere microbiome of the cultivar was performed for twelve plant growth cycles in the presence of increasing salt stress. The rhizosphere microbiome of the phenotypically best-grown plant under stress was transferred as inoculum to the next plant growth cycle. Plant growth attributes and stress marker levels were assessed, expression levels of plant salt stress-responsive genes were examined, and the bacterial community composition in the initial and final plant growth cycles was analysed. Rhizosphere microbiome inoculation promoted plant growth under increasing salt concentrations. Stress markers were reduced in plants inoculated with an acclimatized microbiome, while the root architecture was enhanced, indicating salt tolerance. The salt stress-responsive genes were downregulated in salt-treated plants, whereas upregulation of these genes was observed upon microbiome inoculation. The relative abundance of Exiguobacterium, Arthrobacter, and Lysobacter was higher in microbiome-treated plants under salt stress compared to the salt-treated plants without microbiome inoculation. The strategy of acclimatizing the rhizosphere microbiome of a salt-susceptible tomato cultivar was successfully implemented for stress amelioration and plant growth promotion, thereby offering a sustainable means with immense potential for application in other crops.