Plant growth-promoting bacteria (PGPR) improve plant growth and biotic or/and abiotic stress tolerance. In nature plants are challenged by multiple stressors simultaneously and plants under abiotic stress are more susceptible to disease. Therefore, it is imperative to understand how PGPR modulate plant stress response to achieve overall plant health. However, the underlying mechanisms are not fully understood. Our objective was to investigate how the PGPR Bradyrhizobium japonicum IRAT FA3 modulates plant responses to individual and multiple stresses. Using the model plant Arabidopsis thaliana (Col-0) and an auxin receptor mutant, tir1afb2, the effects of heat stress, salt stress, or a combination of both in the presence of B. japonicum were investigated. After 8 d of cocultivation with B. japonicum, shoot and root fresh weight increased. B. japonicum drove developmental plasticity in roots by inhibiting primary root elongation and promoting lateral root and root hair formation. Compared to Col-0, tir1afb2 displayed fewer lateral roots, indicating that functional auxin perception is required for B. japonicum-stimulated root architectural changes in Arabidopsis. Stress induced a reduction in photosynthetic pigments and an increase in lipid peroxidation. B. japonicum rescued plants exposed to moderate stresses. Transcription of key antioxidant enzymes increased significantly in treated plants. These results suggest that B. japonicum improves plant performance under moderate salt and heat stress through increasing root phenotypic plasticity and priming of antioxidant responses.