Salt-sensitive glycophytes and salt-tolerant halophytes employ common mechanisms to cope with salinity, and it is hypothesized that differences in salt tolerance arise because of changes in the regulation of a basic set of salt tolerance genes. We explored the expression of genes involved in two key salt tolerance mechanisms in Arabidopsis thaliana and the halophytic A. thaliana relative model system (ARMS), Thellungiella halophila. Salt overly sensitive 1 (SOS1) is a plasma membrane Na+/H+ antiporter that retrieves and loads Na+ ions from and into the xylem. Shoot SOS1 transcript was more strongly induced by salt in T. halophila while root SOS1 was constitutively higher in unstressed T. halophila. This is consistent with a lower salt-induced rise in T. halophila xylem sap Na+ concentration than in A. thaliana. Thellungiella halophila contained higher unstressed levels of the compatible osmolyte proline than A. thaliana, while under salt stress, T. halophila accumulated more proline mainly in shoots. Expression of the A. thaliana ortholog of proline dehydrogenase (PDH), involved in proline catabolism, was undetectable in T. halophila shoots. The PDH enzyme activity was lower and T. halophila seedlings were hypersensitive to exogenous proline, indicating repression of proline catabolism in T. halophila. Our results suggest that differential gene expression between glycophytes and halophytes contributes to the salt tolerance of halophytes.