Ralstonia solanacearum pandemic lineage strain UW551 overcomes inhibitory xylem chemistry to break tomato bacterial wilt resistance

Plant pathogenic Ralstonia strains cause bacterial wilt disease by colonizing xylem vessels of many crops, including tomato. Host resistance is the best control for bacterial wilt, but resistance mechanisms of the widely used Hawaii7996 tomato breeding line are unknown. Using growth in ex vivo xylem sap as a proxy for host xylem, we found that Ralstonia strain GMI1000 grows in sap from both healthy plants and Ralstonia-infected susceptible plants. However, sap from Ralstonia-infected Hawaii7996 plants inhibited Ralstonia growth, suggesting that in response to Ralstonia infection, resistant plants increase inhibitors in their xylem sap. Consistent with this, reciprocal grafting and defense gene expression experiments indicated that Hawaii7996 wilt resistance acts both above- and belowground. Concerningly, Hawaii7996 resistance is broken by Ralstonia strain UW551 of the pandemic lineage that threatens highland tropical agriculture. Unlike other Ralstonia strains, UW551 grew well in sap from Ralstonia-infected Hawaii7996 plants. Moreover, other Ralstonia strains could grow in sap from Hawaii7996 plants previously infected by UW551. Thus, UW551 overcomes Hawaii7996 resistance in part by detoxifying inhibitors in xylem sap. Testing a panel of xylem sap compounds identified by metabolomics revealed that no single chemical differentially inhibits Ralstonia strains that cannot infect Hawaii7996. However, sap from Ralstonia-infected Hawaii7996 contained more phenolic compounds, which are known plant antimicrobial defenses. Culturing UW551 in this sap reduced total phenolic levels, indicating that the resistance-breaking Ralstonia strain degrades these chemical defenses. Together, these results suggest that Hawaii7996 tomato wilt resistance depends at least in part on inducible phenolic compounds in xylem sap.