The transcription factor TaWRKY27 confers enhanced stripe rust susceptibility by facilitating auxin accumulation in wheat.

Many pathogens exploit host susceptibility genes to facilitate their colonization. The disruption of these susceptibility genes holds the potential to confer broad-spectrum and robust disease resistance, offering a promising crop improvement strategy. However, little is known about the molecular mechanisms by which susceptibility genes suppress host immunity. In this study, we identified a transcription factor in wheat (Triticum aestivum L.), TaWRKY27, that was substantially induced during Puccinia striiformis f. sp. tritici (Pst) infection. TaWRKY27 is a nucleus-localized transcriptional activator. TaWRKY27 downregulation in wheat conferred increased Pst resistance, while TaWRKY27 overexpression substantially decreased Pst resistance and increased auxin accumulation. Notably, auxin application to wheat leaves suppressed the expression of defense-related genes. Additionally, integrated DNA affinity purification sequencing (DAP-seq) and RNA-seq analyses demonstrated that TaWRKY27 directly activates the transcription of two 2-oxoglutarate-dependent dioxygenase superfamily members, aminocyclopropane carboxylate oxidase protein TaACO3 and senescence-related protein TaSRG1, a finding confirmed through yeast 1-hybrid and dual-luciferase reporter assays. Notably, both TaACO3 and TaSRG1 negatively regulated wheat resistance to Pst. Taken together, our findings reveal that TaWRKY27 responds to Pst infection and contributes to wheat stripe rust susceptibility by facilitating TaACO3/TaSRG1-mediated auxin accumulation. These results highlight TaWRKY27 as a potential target for engineering enhanced stripe rust resistance in wheat.