Among abiotic stresses, salinity is considered the main limiting stress that negatively affects plant growth and reduces productivity worldwide. To overcome this challenge, a sustainable solution such as plant growth-promoting bacteria (PGPB) can be used to meet the increasing demand for food. The desert microbe Enterobacter sp SA187, an endophytic PGPB, induces salt tolerance in both model plant and crops. The interaction between SA187 and the host plant triggers the sulfur pathway in the bacteria which then provides multiple sulfur-containing compounds to its host plant. However, the molecular sensor of these compounds in the host plant is not known. Here, we show that SA187 activates the plant target of rapamycin (TOR) pathway. The beneficial effect of SA187 was lost in TOR mutants like raptor, and by the application of TOR inhibitor AZD8055. Next, we show that SA187 modulates the one- carbon (1C) metabolism of the host plant consisting of methionine and folate cycles. The beneficial effect of SA187 was compromised by using chemical inhibitors of folate cycle like Methotrexate (MTX) and Sulfadiazine (SDZ). The intermediates of the 1C metabolism like Homocysteine and S-adenosyl methionine (SAM) showed similar beneficial effects as SA187 colonized plants. Finally, we showed that SA187 enhances 1C metabolism activity by increasing methylation index (SAM/SAH ratio) in the plants. Taken together, we could show that host TOR-1C axis is essential for plant salt tolerance by SA187.