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

The virulence of <i>Xanthomonas oryzae</i> pv<i>. oryzae</i>, 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 <i>sux</i> locus of <i>Xoo</i> 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 <i>suxA/suxB</i> genes. Besides a role of sucrose for reproduction, we found that sucrose promotes motility, extracellular polysaccharides production, biofilm formation, and virulence. Notably, the SuxC sucrose H⁺-symporter and the sucrose hydrolase SuxB were required for full virulence of <i>Xoo</i> on <i>indica</i> and <i>japonica</i> rice varieties. Our findings indicate that pathogen-induced sucrose efflux via SWEETs provides sucrose to <i>Xoo</i>, that <i>Xoo</i> uses the <i>sux</i> gene cluster to acquire and utilize sucrose, and that sucrose promotes bacterial fitness and xylem colonization.