The interplay between ScSWEET11 promoters and Paracidovorax avenae effectors regulate resistance in sugarcane

Red stripe, caused by the bacterial pathogen Paracidovorax avenae, poses a significant threat to the sugarcane industry. The Sugar Will Eventually be Exported Transporter (SWEET) gene family participates in plant–pathogen interactions. However, the specific mechanism underlying the interaction between SWEETs and the red stripe pathogen remains unclear. In this study, 17, 21, and 25 members of the SWEET gene family were identified from Saccharum spontaneum, S. officinarum, and Saccharum spp. hybrid, respectively. They were phylogenetically divided into four clades. Four members in clade III, especially ScSWEET11, showed significantly different expression patterns between red stripe-resistant and susceptible sugarcane varieties. Subsequently, the ScSWEET11 gene was isolated and overexpressed in tobacco, resulting in significant lesions when infected with P. avenae (Pa), and there was no substantial difference in lesion area compared to wild-type tobacco. Heterologous expression of ScSWEET11 demonstrated sucrose transport activity in yeast sugar transport mutants. Besides, pScSWEET11_I and pScSWEET11_II, the two types of SWEET11 promoters in Saccharum, were mined and found to originate from S. spontaneum and S. officinarum, respectively. Interestingly, both types of promoters were observed in the susceptible cultivar, while there was only pScSWEET11_II in the resistant one. Notably, the activity of pScSWEET11_I was much higher than that of pScSWEET11_II, particularly under ABA and P. avenae stress conditions. Yeast one-hybrid, dual-luciferase reporter, and transient overexpression assays indicated that the interaction between PaXopQ, PaXopAU, PaXopF2, and pScSWEET11_I led to more susceptibility by promoting the ScSWEET11 expression, while that between PaAvrRxo1, PaXopAU, and pScSWEET11_II resulted in higher resistance through suppressing the ScSWEET11 expression. Collectively, this study provided a good understanding of the regulatory network for the red stripe pathogen invading the host, offering a valuable research basis for molecular breeding of disease-resistant sugarcane.