Investigating physiological host resistance mechanisms to Xylella fastidiosa diseases using XCT imaging and mathematical modelling

Abstract

Xylella fastidiosa (X. fastidiosa) is a global bacterial plant pathogen, devastating important crops including grapes, coffee and olives. X. fastidiosa infects host xylem, the tissue responsible for plant water and nutrient transport. It is understood that disease symptoms arise due to blockages to xylem flow caused both directly by the presence of the pathogen (biofilms) and by plant associated structures formed in the host immune response (e.g. tyloses). However, specifics of these within-host dynamics are poorly characterised. As such, there remains no cure for X. fastidiosa diseases in the open field. Despite this, even among susceptible taxa, some hosts are resistant to disease, and are considered a critical resource for rebuilding lost agriculture. Xylem structure has been correlated with resistance for a small number of hosts comparing one susceptible and one resistant variety within the same taxonomic group. However, identified morphological traits have not been generalised or compared more broadly. Furthermore, mechanisms by which these traits could be facilitating resistance are rarely considered. 

In this thesis, a mathematical model is developed describing bulk X. fastidiosa biofilm dynamics within xylem vessels. Model simulations are compared with microfluidic experiments, showing good qualitative agreement. Importantly, simulations suggest that even small amounts of biofilm induce significant reductions in hydraulic conductivity on infected vessels, with developed structures having the potential to fully bridge vessel lumen. This indicates that biofilm occlusions have significant direct influence on symptom development. The remaining work in this thesis uses X-ray Computed Tomography to obtain xylem morphological metrics among resistant and susceptible olive and citrus cultivars. Trends in the measurements are then related to biofilm spread, air embolism susceptibility and hydraulic conductivity using mathematical models. Measurements indicate that resistant olive cultivar Leccino has both narrower vessels, and a lack of the widest vessels, compared to considered susceptible olive (Koroneiki, Ogliarola) and citrus (Pera sweet orange) cultivars. Results show that not only does this make the vasculature of Leccino particularly resistant to air embolisms, but it also greatly reduces biofilm spread in the vessels compared to the considered susceptible plants. Interestingly this trend is not found in resistant olive cultivar FS17, for which it is hypothesised xylem morphology plays a limited role in its resistance. Furthermore, the distinguishing morphological trait found in the resistant citrus (Tangor Murcott) plants is distinct from that found in Leccino. In particular, results suggest that though they do not have narrow vessels, the vasculature is significantly more connected than the other considered plants. It is hypothesised that these connections provide critical flow paths for bypassing vessel occlusions. Finally, both susceptible olive and citrus plants are found to have significantly more vessels than the resistant types. This represents a potentially important broader reaching trend for identifying candidate resistant plant varieties in relation to both recent and novel outbreaks.

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