Pathogenic fungus Ustilago maydis exploits the lateral root regulators to induce pluripotency in maize shoots

Biotrophic plant-pathogens secrete effector molecules to redirect and exploit endogenous signaling and developmental pathways in their favor. The biotrophic fungus Ustilago maydis causes galls on all aerial parts of maize. However, the responsible gall-inducing effectors and corresponding plant signaling pathway(s) remain largely unknown. Using molecular and genetic approaches, and transcriptomic comparisons in maize, we identify downstream targets and developmental consequences of the plant TOPLESS (TPL)-interacting protein (Tip) effectors in gall formation. We demonstrate that Tip4 derepress AtARF7/AtARF19 branch of auxin signaling, leading to the formation of pluripotent calli without the external addition of phytohormones. Comparative transcriptomics in maize further reveals a significant overlap of genes upregulated during U. maydis-triggered leaf gall formation and the developmental initiation of lateral roots (LRs). Additionally, we show that this process involves the transcriptional upregulation of downstream LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors. Homozygous mutations in two LBD genes (ra2, rtcs) resulted in significantly reduced gall formation in maize. Taken together, our results suggest that U. maydis hijacks the LR initiation pathway to trigger gall formation in maize shoots, revealing key effectors and host pathways exploited by biotrophic pathogens.