Microbial Melatonin Production Improves Plant Metabolic Function in Short-Term Climate-Induced Stresses

Climate change, specifically high temperatures, can reduce soil moisture and cause hypersaline conditions, which creates an unsustainable agro-production system. Microbial symbionts associated with plants relinquish stressful conditions by producing stress-protecting substances. Melatonin is a signaling and stress-protecting molecule for plants, but is least known for microbial symbionts and their function in stress protection. Here, our study shows that the melatonin-synthesizing Bacillus velezensis EH151 (27.9 ng/mL at 96 h) significantly improved host plant (Glycine max L.) growth, biomass, photosynthesis, and reduced oxidative stress during heat and salinity stress conditions than the non-inculcated control. The EH151 symbiosis enhanced the macronutrient (P, Ca, and K) and reduced Na uptake in shoots during stress conditions. The microbial inoculation significantly expressed the high-affinity K⁺ transporter, MYB transcription factor, Salt Overly Sensitive 1, Na⁺/H⁺ antiporter 2, and heat shock transcription factors in spatio-temporal orders during heat and salinity stress (H&S 1, 3, 10, and 14 h). We observed that microbial strain significantly increased the plant's endogenous abscisic acid (49.5% in H&S 10 h), jasmonic acid (71% in H&S 10 h), and melatonin biosynthesis (418% in H&S 14 h). Metabolome map of plant defense response showed that EH151 enhanced activation of amino acid metabolism pathways (e.g., glutamate (34%) L-aspartate (82%), glycine (18.5%), and serine (58%) under H&S 14 h compared to non-inoculation). Conversely, the free sugars and organic acids within the central carbon metabolism were significantly activated in non-inoculated combined heat and salinity stress compared to inoculated plants-suggesting lesser defense energy activated for stress tolerance. In conclusion, the current results show promising effects of the microbial abilities of melatonin that can regulate host growth and defense responses. Utilization of beneficial strains like B. velezensis EH151 could be the ideal strategy to improve stress tolerance and overcome the adverse impact of climate-induced abrupt changes.