Plant pathogenic bacteria possess sophisticated mechanisms to detect the presence of host plants by sensing host-derived compounds. Ralstonia solanacearum, the causative agent of bacterial wilt on solanaceous plants, employs quorum sensing to control the production of the secondary metabolite ralfuranones/ralstonins, which have been suggested to be involved in virulence. Here, we report that D-galactose and D-glucose, plant sugars, activate the production of ralfuranones/ralstonins in R. solanacearum. As a result, two new derivatives, ralfuranone M (1) and ralstonin C (2), were found in the culture extracts, and their structures were elucidated by spectroscopic and chemical methods. Ralstonin C (2) is a cyclic lipopeptide containing a unique fatty acid, (2S,3S,Z)-3-amino-2-hydroxyicos-13-enoic acid, whereas ralfuranone M (1) has a common aryl-furanone structure with other ralfuranones. D-Galactose and D-glucose activated the expression of the biosynthetic ralfuranone/ralstonin genes and in part became the biosynthetic source of ralfuranones/ralstonins. Ralfuranones and ralstonins were detected from the xylem fluid of the infected tomato plants, and their production-deficient mutants exhibited reduced virulence on tomato and tobacco plants. Taken together, these results suggest that activation of ralfuranone/ralstonin production by host sugars functions in R. solanacearum virulence.

Ralstonia solanacearum species complex (RSSC) strains infect both plants and fungi. The phc quorum-sensing (QS) system of RSSC is important for parasitism on plants, because it allows them to invade and proliferate within the hosts by causing appropriate activation of the system at each infection step.

Strains ofRalstonia solanacearumspecies complex (RSSC), though known as the causative agent of bacterial wilt disease in plants, induce the chlamydospores of many fungi species and invade them through the spores. The lipopeptide ralstonins are the chlamydospore inducers produced by RSSC and are essential for this invasion. However, no mechanistic investigation of this interaction has been conducted. In this study, we report that quorum sensing (QS), which is bacterial cell–cell communication, is important for RSSC to invade the fungusFusarium oxysporum(Fo). ∆phcB, a deletion mutant of QS signal synthase, lost the ability to both produce ralstonins and invadeFochlamydospores. The QS signal methyl 3-hydroxymyristate rescued these disabilities. In contrast, exogenous ralstonin A, while inducingFochlamydospores, failed to rescue the invasive ability. Gene-deletion and -complementation experiments revealed that the QS-dependent production of extracellular polysaccharide (EPS I) is essential for this invasion. The RSSC cells adhered toFohyphae and formed biofilms there before inducing chlamydospores. This biofilm formation was not observed in the EPS I- or the ralstonin-deficient mutant. Microscopic analysis showed that RSSC infection resulted in the death ofFochlamydospores. Altogether, we reported that the RSSC QS system is important for this lethal endoparasitism. Among the factors regulated by the QS system, ralstonins, EPS I, and biofilm are important parasitic factors.