ScWRKY2: a key regulator for smut resistance in sugarcane

Sugarcane smut is a worldwide fungal disease caused by Sporisorium scitamineum, which seriously jeopardizes the healthy and sustainable development of the sugarcane industry. WRKY transcription factors are actively involved in plant responses to pathogen infection; however, the mechanisms by which WRKY mediates resistance to sugarcane smut remain elusive. Here, we obtained a nucleus-localized transcription factor ScWRKY2, which was down-regulated in smut-resistant but up-regulated in smut-susceptible sugarcane cultivars. Overexpression of the ScWRKY2 gene in sugarcane enhanced its sensitivity to smut disease. Besides, an immune-related gene ScLRR-RLK, directly regulated by ScWRKY2, was identified through a combination of transcriptome and DNA affinity purification sequencing. Interestingly, ScWRKY2 suppressed the expression of the ScLRR-RLK gene by binding to the W-box element in its promoter region. Furthermore, protein-protein interaction assays demonstrated that ScWRKY2 interacted with the ScPsbP protein in the nucleus. Notably, co-overexpression of ScWRKY2 and ScPsbP enhanced the sensitivity of plants to pathogens by inducing the expression of reactive oxygen species (ROS) scavenging-related genes. Collectively, our study revealed that ScWRKY2 negatively regulated sugarcane resistance to smut disease by repressing the expression of the ScLRR-RLK gene, followed by interacting with the chloroplast protein ScPsbP, and thus inducing the expression of ROS scavenging-related genes to maintain ROS homeostasis. These findings provided a theoretical basis and gene resources for sugarcane disease resistance breeding.