Rhizobia, which enter into symbiosis with legumes, can also interact with non-legumes and promote plant growth. In this paper, we explored the effects of nickel (Ni, 200 µM) on Arabidopsis thaliana (Col-0) inoculated with plant growth-promoting (PGP) rhizobia nodulating ultramafic Anthyllis vulneraria. The isolated PGP strains tolerant to Ni were identified as Rhizobium sp. and Bradyrhizobium sp. The isolates highly differed in their PGP abilities and Ni resistance. Without Ni-stress, the plants inoculated with most isolates grew better and had higher photosynthetic efficiency than non-inoculated controls. Nickel treatment increased Ni concentration in inoculated plants. Plant growth, leaf anatomy, chloroplast ultrastructure, efficiency of photosynthesis, and antioxidant defense system activity were significantly impaired by Ni, however, the majority of these effects were diminished in plants inoculated with the most effective PGP rhizobia. Real-time PCR revealed an increased expression level of genes involved in auxin and gibberellin biosynthesis in the inoculated, Ni-treated plants, and this may have improved shoot and root growth after inoculation with effective isolates. Our results also suggest a positive correlation between Ni-stress parameters and antioxidant defense system activity, and also between the effectiveness of photosynthesis and plant growth parameters. We showed that the selected rhizobia, naturally nodulating Anthyllis on Ni-rich ultramafic soils can promote Arabidopsis growth and increase plant tolerance to Ni by improving different physiological and biochemical mechanisms.