The plant pathogen Agrobacterium tumefaciensC58 harbours three independent type IV secretion (T4SS) machineries. T4SS(T-DNA) promotes the transfer of the T-DNA to host plant cells, provoking tumour development and accumulation of opines such as nopaline and agrocinopines. T4SS(pTi) and T4SS(pAt) control the bacterial conjugation of the Ti and At plasmids respectively. Expression of T4SS(pTi) is controlled by the agrocinopine-responsive transcriptional repressor AccR. In this work, we compared the genome-wide transcriptional profile of the wild-type A.tumefaciens strain C58 with that of its accR KO-mutant to delineate the AccR regulon. In addition to the genes that encode agrocinopine catabolism and T4SS(pTi), we found that AccR also regulated genes coding for nopaline catabolism and T4SS(pAt). Further opine detection and conjugation assays confirmed the enhancement of nopaline consumption and At plasmid conjugation frequency in accR. Moreover, co-regulation of the T4SS(pTi) and T4SS(pAt) correlated with the co-transfer of the At and Ti plasmids both in vitro and in plant tumours. Finally, unlike T4SS(pTi), T4SS(pAt) activation does not require quorum-sensing. Overall this study highlights the regulatory interplays between opines, At and Ti plasmids that contribute to a concerted dissemination of the two replicons in bacterial populations colonizing the plant tumour.