Sucrose-dependence of sugar uptake, quorum sensing and virulence of the rice blight pathogen Xanthomonas oryzae pv. oryzae

Abstract

AbstractVirulence of Xanthomonas oryzae pv. oryzae (Xoo), which causes bacterial leaf blight of rice, depends on induction of host SWEET sucrose efflux transporters. It remained unknown whether secreted sucrose serves bacterial nutrition or host defense. Here we identified the sux sucrose uptake/utilization locus of Xoo and demonstrate that it is necessary and sufficient for sucrose acquisition. Induction of sux genes during infection closely tracked induction of rice SWEET11a. sux mutants were defective in swimming, swarming, extracellular polysaccharide (EPS) production and biofilm formation. EPS synthesis in mutants was restored by the quorum-sensing factor DSF. Notably, transcripts for rate limiting steps in DSF production were unaffected by sucrose, transcripts of the DSF receptor were sucrose-inducible and increased during infection, indicating sensitization to DSF in response to sucrose supply. Sucrose induced the sigma factors transcripts for RpoN1 and RpoN2 that regulate swimming, EPS and virulence. Furthermore, in contrast to Xanthomonas axonopodis pv. manihotis, virulence of Xoo depended critically on sux gene function. Together, pathogen-induced sucrose efflux from host cells likely induces bacterial sigma factors and sensitizes quorum signaling necessary for biofilm formation and colonization of the xylem, serves as energy source for swimming against the xylem stream, and as nutrient for growth.Lay AbstractIf we want to efficiently protect plants against infections, we need to understand the disease mechanisms. Bacterial leaf blight is a major scourge for rice production in Asia and Africa. We had found that disease-causing bacteria use a set of keys, so-called TAL effectors, to switch on sugar transporter genes in rice leaves causing sucrose to be released around the bacteria. A key question was whether the sugars act primarily in activation of host defense, or serve as nutrients and signals for bacterial infection. Here we provide evidence that both the ability to attack as well as the growth of bacteria depend on sucrose uptake. We unravel a regulatory network including transcriptional regulators, quorum sensing, swimming, biofilm production and virulence that all depend on sucrose uptake. These discoveries may prove to be crucial for the development of strategies for protecting rice against this disease.