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Plant growth-promoting rhizobacteria are involved in altering secondary root (SR) formation, but hitherto there has been no distinction between the different types of SRs upon induction of soil biota, and the genetic pathways involved. By using plate and soil systems, we studied the effects of the Pseudomonas strains CM11 and WCS417 on plant performance with a focus on root development. Through a combination of cellular, molecular and genetic analyses, we investigated the type of SRs induced upon CM11 and WCS417 root inoculation using genetic pathways associated with specific SR types. CM11 was shown to affect the root architecture differently from WCS417. CM11 inoculation leads to primary root arrest, whereas WCS417 reveals a longer primary root. Both CM11 and WCS417 activate the PLETHORA 3,5,7-controlled lateral root pathway, rather than the WUSCHEL-RELATED HOMEOBOX 11,12-controlled adventitious (lateral) root pathway. In addition, CM11 promotes plant growth in model and various crop species. It improves plant fitness traits, such as bigger shoots, faster bolting and higher yield in terms of seeds. Our results indicate that the root system architecture can be promoted by activation of PLETHORA 3,5,7 dependent primed lateral pre-branch sites upon inoculation with CM11, which creates great potential to gain a better understanding of root plasticity.