Dual SA-mediated and SA-independent mechanisms drive Sphingomonas paucimobilis -induced cold tolerance in Arabidopsis

Abstract Aim This study aimed to investigate the intrinsic cold tolerance of Sphingomonas paucimobilis ZJSH1 and to evaluate the role of endogenous salicylic acid (SA) in mediating cold adaptation. The research focused on highlighting the influence of microbial SA over plant osmolyte accumulation, antioxidant activity, and broader metabolic responses under low-temperature stress. Methods and results Wild-type S. paucimobilis ZJSH1 and an SA-deficient ΔpchB mutant were subjected to prolonged low-temperature stress. The ΔpchB mutant, which is unable to produce SA, showed impaired growth and lower osmolyte and exopolysaccharide (EPS) accumulation compared to the wild type. Additionally, the mutant exhibited diminished antioxidant enzyme activities (SOD, POD, and CAT) under cold stress but showed partial recovery when supplemented with exogenous SA. In plant inoculation experiments, wild-type ZJSH1 significantly improved rosette diameter (53.1% over control) and fresh weight (approximately 36% over control) in Arabidopsis plants under cold stress, outperforming the ΔpchB mutant (34.67% and 14%, respectively). Transcriptomic analysis revealed that the wild-type strain upregulated genes involved in SA biosynthesis (pchB), redox detoxification (CatA, CatC, sod), membrane stabilization (Omp16), and nutrient cycling (FixK, NifU, PhoU). In contrast, the ΔpchB mutant activated compensatory pathways, including antioxidant enzymes (KatC), nutrient scavenging systems (pstB, cstA), and membrane-modifying proteins (LptF, MreC), suggesting a SA-independent metabolic flexibility. Conclusion S. paucimobilis ZJSH1 exhibits intrinsic cold tolerance with both SA-dependent and SA-independent mechanisms contributing to its adaptation to low temperatures. While SA plays a critical role in enhancing osmolyte accumulation, antioxidant activity, and membrane stabilization, the SA-deficient ΔpchB mutant activates alternative metabolic pathways. These findings suggest that ZJSH1 may be useful in improving plant stress tolerance under cold stress conditions.