A critical role of sux cistron-mediated sucrose uptake for virulence of the rice blight pathogen Xanthomonas oryzae pv. oryzae

Abstract

The virulence of Xanthomonas oryzae pv. oryzae, the causal agent of bacterial blight (BB) of rice, critically depends on the activation of SWEET sucrose uniporters of the host. To date, the role of SWEET-released sucrose for virulence remains unclear. We here identified the sux locus of Xoo, consisting of a LacI-type repressor (SuxR), an outer membrane TonB-like porin (SuxA), an inner membrane MFS H+-symporter (SuxC), and a cytosolic sucrose hydrolase (SuxB). Structural and functional analyses demonstrate that SuxB has exclusive sucrose hydrolase activity. Mutant analyses show that the transporter SuxC and the sucrose hydrolase are necessary for growth of bacteria on sucrose, while SuxA is not essential, likely due to the ability of other porins to transport sucrose across the outer membrane. Consistent with a role of SuxR as a sucrose repressor, transcriptome studies show sucrose-dependent regulation of the suxA/suxB genes. Besides a role of sucrose for reproduction, we found that sucrose promotes motility, EPS production, biofilm formation, and virulence. Notably, the SuxC sucrose H+-symporter and the sucrose hydrolase SuxB were required for full virulence of Xoo on indica and japonica rice varieties. Our findings indicate that pathogen-induced sucrose efflux via SWEETs provides sucrose to Xoo, that Xoo uses the sux gene cluster to acquire and utilize sucrose, and that sucrose promotes bacterial fitness and xylem colonization. Significance StatementUnderstanding disease mechanisms is critical for developing strategies to protect plants against infections. Bacterial blight, a major threat to global rice production, is caused by Xanthomonas oryzae pv. oryzae strains that hijack rice SWEET sucrose uniporters. Xanthomonas oryzae pv. oryzae deploys a set of molecular "keys", TAL effectors, to trigger host sucrose release. Sugars could serve as nutrients for the bacteria or prime host defense. Here, we provide evidence that the pathogens ability to attack and grow depends on sucrose uptake. We explore how crucial virulence functions, such as motility, EPS production, and biofilm formation, depend on the activity of the sucrose utilization system, supporting a key role of sucrose for the nutrition of the bacteria in the xylem.