Pathogenic fungus 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, identification and characterization of the responsible gall-inducing effectors and corresponding plant signaling pathway(s) are largely elusive. Here we reveal molecular components acting downstream of a group of plant TOPLESS (TPL)- corepressor interacting fungal effectors that are directly involved in gall formation. We classify these effectors into two classes based on distinct phenotypic responses when individually expressed in planta. While class I responses are characterized by leaf chlorosis, transgenic plants expressing class II TPL-interacting protein (Tip) effectors show a derepression of the AtARF7/AtARF19 branch of auxin signaling, resulting in pluripotent calli formation without the external addition of phytohormones. Subsequent comparative transcriptomics in maize also demonstrates a highly significant overlap of genes up-regulated during U. maydis-triggered leaf gall formation and during the developmental initiation of lateral root formation. This suggests that U. maydis can hijack the lateral root initiation pathway to induce galls in maize shoots. We demonstrate that underlying this is the transcriptional upregulation of downstream LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors. Maize mutants in two LBD genes (ra2, rtcs) led to significantly reduced gall formation following U. maydis infection on homozygous mutants. This study reveals a set of dominantly acting cell proliferation-inducing fungal effectors and provides novel insight into plant developmental pathways that can be hijacked by biotrophic pathogens to induce gall formation.