Tomato R-gene-mediated resistance against Fusarium wilt originates in roots and extends to shoots via xylem to limit pathogen colonization.

Vascular wilt disease, caused by the soil-borne fungus Fusarium oxysporum (Fo), poses a threat to many crop species. Four different tomato resistance (R) genes (I-1, I-2, I-3, and I-7) have been identified to confer protection against Fo f.sp. lycopersici (Fol). These I genes are root-expressed and mount an immune response upon perception of the invading fungus. Despite immune activation, Fol is still able to colonize the xylem vessels of resistant tomato lines. Yet, the fungus remains localized in the vessels and does not colonize adjacent tissues or cause disease. The molecular mechanism constraining Fol in the vascular system of the stem remains unclear. We here demonstrate that an I-2-resistant rootstock protects a susceptible scion from Fusarium wilt, notwithstanding fungal colonization of the susceptible scion. Proteomic analyses revealed the presence of fungal effectors in the xylem sap of infected plants, showing that the lack of fungal pathogenicity is not due to its inability to express its virulence genes. To identify mobile root-derived proteins, potentially involved in controlling fungal proliferation, comparative xylem sap proteomics was performed. We identified distinct pathogenesis-related (PR) protein profiles in xylem sap from Fol-inoculated I-1, I-2, I-3, and I-7 resistant lines. Despite structural diversity, all four immune receptors trigger the accumulation of a common set of four PR proteins: PR-5x, PR-P2, and two glucan endo-1,3-ß-D-glucosidases. This research provides insights into Fusarium resistance mechanisms and identifies a core set of proteins whose abundance correlates with defense against Fusarium wilt.

The tomato P69 subtilase family is involved in resistance to bacterial wilt.

The intercellular space or apoplast constitutes the main interface in plant-pathogen interactions. Apoplastic subtilisin-like proteases-subtilases-may play an important role in defence and they have been identified as targets of pathogen-secreted effector proteins. Here, we characterise the role of the Solanaceae-specific P69 subtilase family in the interaction between tomato and the vascular bacterial wilt pathogen Ralstonia solanacearum. R. solanacearum infection post-translationally activated several tomato P69s. Among them, P69D was exclusively activated in tomato plants resistant to R. solanacearum. In vitro experiments showed that P69D activation by prodomain removal occurred in an autocatalytic and intramolecular reaction that does not rely on the residue upstream of the processing site. Importantly P69D-deficient tomato plants were more susceptible to bacterial wilt and transient expression of P69B, D and G in Nicotiana benthamiana limited proliferation of R. solanacearum. Our study demonstrates that P69s have conserved features but diverse functions in tomato and that P69D is involved in resistance to R. solanacearum but not to other vascular pathogens like Fusarium oxysporum.

Pattern-triggered immunity restricts host colonization by endophytic fusaria, but does not affect endophyte-mediated resistance.

Fusarium oxysporum (Fo) is best known as a host-specific vascular pathogen causing major crop losses. Most Fo strains, however, are root endophytes potentially conferring endophyte-mediated resistance (EMR). EMR is a mechanistically poorly understood root-specific induced resistance response induced by endophytic or nonhost pathogenic Fo strains. Like other types of induced immunity, such as systemic acquired resistance or induced systemic resistance, EMR has been proposed to rely on the activation of the pattern-triggered immunity (PTI) system of the plant. PTI is activated upon recognition of conserved microbe-associated molecular patterns (MAMPs) of invading microbes. Here, we investigated the role of PTI in controlling host colonization by Fo endophytes and their ability to induce EMR to the tomato pathogen Fo f. sp. lycopersici (Fol). Transgenic tomato and Arabidopsis plants expressing the Fo effector gene Avr2 are hypersusceptible to bacterial and fungal infection. Here we show that these plants are PTI-compromised and are nonresponsive to bacterial- (flg22) and fungal- (chitosan) MAMPs. We challenged the PTI-compromised tomato mutants with the EMR-conferring Fo endophyte Fo47, the nonhost pathogen Fom (a melon pathogen), and with Fol. Compared to wild-type plants, Avr2-tomato plants became hypercolonized by Fo47 and Fom. Surprisingly, however, EMR towards Fol, induced by either Fo47 or Fom, was unaffected in these plants. These data show that EMR-based disease resistance is independent from the conventional defence pathways triggered by PTI, but that PTI is involved in restricting host colonization by nonpathogenic Fo isolates.