Rhizogenic Agrobacterium protein RolB interacts with the TOPLESS repressor proteins to reprogram plant immunity and development br

Rhizogenic Agrobacterium strains comprise biotrophic pathogens that cause hairy root disease (HRD) on hydroponically grown Solanaceae and Cucurbitaceae crops, besides being widely explored agents for the creation of hairy root cultures for the sustainable production of plant-specialized metabolites. Hairy root formation is mediated through the expression of genes encoded on the T-DNA of the root-inducing (Ri) plasmid, of which several, including root oncogenic locus B (rolB), play a major role in hairy root development. Despite decades of research, the exact molecular function of the proteins encoded by the rol genes remains enigmatic. Here, by means of TurboID-mediated prox-imity labeling in tomato (Solanum lycopersicum) hairy roots, we identified the repressor proteins TOPLESS (TPL) and Novel Interactor of JAZ (NINJA) as direct interactors of RolB. Although these interactions allow RolB to act as a transcriptional repressor, our data hint at another in planta function of the RolB oncoprotein. Hence, by a series of plant bioassays, transcriptomic and DNA-binding site enrichment analyses, we conclude that RolB can mitigate the TPL functioning so that it leads to a specific and partial reprogramming of phytohormone signaling, immunity, growth, and developmental pro-cesses. Our data support a model in which RolB manipulates host transcription, at least in part, through interaction with TPL, to facilitate hairy root development. Thereby, we provide important mechanistic insights into this renowned oncoprotein in HRD

Automated summary

Rhizogenic Agrobacterium strains are biotrophic pathogens that infect hydroponically grown Solanaceae and Cucurbitaceae crops, causing hairy root disease (HRD). They are also widely used for hairy root cultures to produce specialized plant metabolites. The development of hairy roots is regulated by genes encoded on the T-DNA of the root-inducing (Ri) plasmid, including the important rolB gene. In this study, through proximity labeling in tomato hairy roots, the repressor proteins TOPLESS (TPL) and Novel Interactor of JAZ (NINJA) were identified as direct interactors of RolB. The interactions between RolB, TPL, and NINJA were found to play a role in the transcriptional regulation and reprogramming of phytohormone signaling, immunity, growth, and developmental processes in the host plants.