Enrichment of the Conserved RY-Repeat Cis-Element in Maize upon Ustilago maydis Infection and Its Interaction with the Candidate Secreted Protein UMAG_06102

Ustilago maydis causes corn smut diseases by forming tumors on maize. Effectors of U. maydis could regulate host gene transcription. However, there is remaining uncertainty about the mechanisms underlying the regulation of transcription reprogramming of maize genes by U. maydis to facilitate disease progression. Here, we conducted systemic enrichment analysis of cis-elements in maize genes induced by infection with U. maydis. Yeast library screening and gene expression analysis were used to identify candidate proteins that could interact with the RY-repeat-containing promoter regions. Knocking out and genetic variation analysis were also deployed to study the role of fungal protein binding to RY-repeat during U. maydis infection. The conserved plant cis-element RY-repeat in maize was enriched in response to U. maydis. UMAG_06102, a candidate secreted protein of U. maydis, showed a Y1H-detected interaction with the RY-repeat-containing region of ZmSWEET11 promoter in a yeast-one-hybrid system. Knocking out UMAG_06102 was associated with the reduced expression of ZmSWEET11 and a decrease in virulence. Moreover, the genetic variation of the RY-repeat of ZmSWEET11 was likely associated with the disease incidence of U. maydis on maize. Our results suggested that U. maydis could influence the host gene expression through the enrichment of the RY-repeat of ZmSWEET11, thus impacting tumor formation on host tissues.