Common scab disease: structural basis of elicitor recognition in pathogenicStreptomycesspecies

InStreptomyces scabiei, the main causative agent of common scab disease of root and tuber crops, the interaction between the substrate-binding protein (SBP) CebE (CebEscab) and cellotriose released by the plant host (KDin the nanomolar range) is the first event for the onset of its pathogenic lifestyle. Here we report the structure of CebEscabin complex with cellotriose at a 1.55 Å resolution, adopting a general fold of the B subcluster of SBPs. The interaction between CebEscaband cellotriose involves multiple direct or water-mediated hydrogen bonds and hydrophobic interactions, the glucose monomer at the non-reducing end occupying the most conserved part of the substrate-binding cleft. As main interactions between the two domains of CebE involve cellotriose itself, the closed conformational state of CebE is performed via an induced-fit ligand binding mechanism where cellotriose binding triggers the domain movement. Analysis of regulon predictions revealed that the signaling pathway from the CebE-mediated cellotriose transport to the transcriptional activation of thaxtomin phytotoxin biosynthesis is conserved inStreptomycesspp causing common scab, except forStreptomyces ipomoeaethat specifically colonizes sweet potatoes and responds to other and yet unknown virulence elicitors. Interestingly, strains belonging to pathogenic speciesturgidiscabiesandcaniscabieshave a cellotriose-binding protein orthologous to the CebE protein of the saprophytic speciesStreptomyces reticuliwith lower affinity for its substrate (KDin the micromolar range), suggesting higher cellotriose concentrations for perception of their host. Our work also provides the structural basis for the uptake of cellobiose and cellotriose by non-pathogenic cellulose-decomposingStreptomycesspecies.ImportanceCommon scab is a disease caused by fewStreptomycesspecies that affects important root and tuber crops including potato, beet, radish, and parsnip, resulting in major economic losses worldwide. In this work we unveiled the molecular basis of host recognition by these pathogens by solving the structure of the sugar-binding protein CebE ofS.scabieiin complex with cellotriose, the main elicitor of the pathogenic lifestyle of these bacteria. We further revealed that the signaling pathway from CebE-mediated transport of cellotriose is conserved in all pathogenic species exceptS.ipomoeaethat causes soft rot disease on sweet potatoes. Our work also provides the structural basis of the uptake of cellobiose and cellotriose in saprophyticStreptomycesspecies, the first step activating the expression of the enzymatic system degrading the most abundant polysaccharide on earth, cellulose.Graphical abstractHighlightsCellotriose uptake triggers common scab in tuber/root crops byStreptomyces scabieiCrystal structure of CebE ofS.scabieiinteracting with cellotriose is solvedCellotriose triggers the closed conformational state of CebEThe CebE/cellotriose route to pathogenicity is conserved inStreptomycesspeciesCebE-type background may affect the cellotriose concentration eliciting virulence