Although not fully understood, molecular communication in the rhizosphere plays an important role regulating traits involved in plant-bacteria association. Burkholderia phytofirmans PsJN is a well-known plant-growth-promoting bacterium, which establishes rhizospheric and endophytic colonization in different plants. A competent colonization is essential for plant-growth-promoting effects produced by bacteria. Using appropriate mutant strains of B. phytofirmans, we obtained evidence for the importance of N-acyl homoserine lactone-mediated (quorum sensing) cell-to-cell communication in efficient colonization of Arabidopsis thaliana plants and the establishment of a beneficial interaction. We also observed that bacterial degradation of the auxin indole-3-acetic acid (IAA) plays a key role in plant-growth-promoting traits and is necessary for efficient rhizosphere colonization. Wildtype B. phytofirmans but not the iacC mutant in IAA mineralization is able to restore promotion effects in roots of A. thaliana in the presence of exogenously added IAA, indicating the importance of this trait for promoting primary root length. Using a transgenic A. thaliana line with suppressed auxin signaling (miR393) and analyzing the expression of auxin receptors in wild-type inoculated plants, we provide evidence that auxin signaling in plants is necessary for the growth promotion effects produced by B. phytofirmans. The interplay between ethylene and auxin signaling was also confirmed by the response of the plant to a 1-aminocyclopropane-1-carboxylate deaminase bacterial mutant strain.