Abstract
The plant pathogen Ralstonia solanacearum uses plant resources to intensely proliferate in xylem vessels and provoke plant wilting. We combined automatic phenotyping and tissue/xylem quantitative metabolomics of infected tomato plants to decipher the dynamics of bacterial wilt. Daily acquisition of physiological parameters such as transpiration and growth were performed. Measurements allowed us to identify a tipping point in bacterial wilt dynamics. At this tipping point, the reached bacterial density brutally disrupts plant physiology and rapidly induces its death. We compared the metabolic and physiological signatures of the infection with drought stress, and found that similar changes occur. Quantitative dynamics of xylem content enabled us to identify glutamine (and asparagine) as primary resources R. solanacearum consumed during its colonization phase. An abundant production of putrescine was also observed during the infection process and was strongly correlated with in planta bacterial growth. Dynamic profiling of xylem metabolites confirmed that glutamine is the favoured substrate of R. solanacearum. On the other hand, a triple mutant strain unable to metabolize glucose, sucrose and fructose appears to be only weakly reduced for in planta growth and pathogenicity.
Highlights
The Ralstonia solanacearum species complex (RSSC) includes a diverse group of pathogenic strains, causative agents of bacterial wilt on many plants (Álvarez et al, 2010; Hayward, 1991)
To assess which xylem metabolites are affected by infection, we performed a PCA. This multivariate analysis revealed that two principal components (PCs) explained 65% of the variability, on which we focused our analysis
We found that for healthy plants, concentrations are constant between 1 and 8 dpi so we determined a global mean for each plant (Table 1, Table S1)
Summary
The Ralstonia solanacearum species complex (RSSC) includes a diverse group of pathogenic strains, causative agents of bacterial wilt on many plants (Álvarez et al, 2010; Hayward, 1991). The bacterial wilt disease caused by RSSC strains on tomato results from a multi-stage infection process in which, after the root infection stage and colonization of the root cortex tissues, bacteria invade the xylem vessels. This allows their spread to the aerial part of the plant, concomitantly with a strong multiplication (Caldwell et al, 2017; Vasse et al, 1995; Xue et al, 2020). R. solanacearum spp. relies on effectors delivered by the type-three secretion system to circumvent plant immunity (Landry et al, 2020) as well as many other virulence factors which contribute to pathogenic fitness at the different infection steps (Genin & Denny, 2012; Hikichi et al, 2017)
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