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A mathematical model of biofilm growth and spread within plant xylem: case study of Xylella fastidiosa in olive trees

A mathematical model of biofilm growth and spread within plant xylem: case study of Xylella fastidiosa in olive trees
A mathematical model of biofilm growth and spread within plant xylem: case study of Xylella fastidiosa in olive trees
Xylem-limited bacterial pathogens cause some of the most destructive plant diseases. Though imposed measures to control these pathogens are generally ineffective, even among susceptible taxa, some hosts can limit bacterial loads and symptom expression. Mechanisms by which this resistance is achieved are poorly understood. In particular, it is still unknown how differences in vascular structure may influence biofilm growth and spread within a host. To address this, we developed a novel theoretical framework to describe biofilm behaviour within xylem vessels, adopting a polymer-based modelling approach. We then parameterised the model to investigate the relevance of xylem vessel diameters on Xylella fastidiosa resistance among olive cultivars. The functionality of all vessels was severely reduced under infection, with hydraulic flow reductions of 2–3 orders of magnitude. However, results suggest wider vessels act as biofilm incubators; allowing biofilms to develop over a long time while still transporting them through the vasculature. By contrast, thinner vessels become blocked much earlier, limiting biofilm spread. Using experimental data on vessel diameter distributions, we were able to determine that a mechanism of resistance in the olive cultivar Leccino is a relatively low abundance of the widest vessels, limiting X. fastidiosa spread.
Biofilm formation, Multiphase model, Olive, Xylella fastidiosa, Xylem-limited bacterial pathogen
0022-5193
111737
Walker, N.C.
0b539663-b1db-4e93-a513-2580c3229df4
White, S.M.
4506a4e0-8812-4abb-88ef-0c8d0ce921ce
Ruiz, S.M.
d79b3b82-7c0d-47cc-9616-11d29e6a41bd
Mckay fletcher, D.
db06e7e0-69af-4fa2-89b3-26f6599e43d4
Saponari, M.
89d2e04b-1e6d-4c87-a73e-29f8d3138d56
Roose, T.
3581ab5b-71e1-4897-8d88-59f13f3bccfe
Walker, N.C.
0b539663-b1db-4e93-a513-2580c3229df4
White, S.M.
4506a4e0-8812-4abb-88ef-0c8d0ce921ce
Ruiz, S.M.
d79b3b82-7c0d-47cc-9616-11d29e6a41bd
Mckay fletcher, D.
db06e7e0-69af-4fa2-89b3-26f6599e43d4
Saponari, M.
89d2e04b-1e6d-4c87-a73e-29f8d3138d56
Roose, T.
3581ab5b-71e1-4897-8d88-59f13f3bccfe

Walker, N.C., White, S.M., Ruiz, S.M., Mckay fletcher, D., Saponari, M. and Roose, T. (2024) A mathematical model of biofilm growth and spread within plant xylem: case study of Xylella fastidiosa in olive trees. Journal of Theoretical Biology, 581, 111737, [111737]. (doi:10.1016/j.jtbi.2024.111737).

Record type: Article

Abstract

Xylem-limited bacterial pathogens cause some of the most destructive plant diseases. Though imposed measures to control these pathogens are generally ineffective, even among susceptible taxa, some hosts can limit bacterial loads and symptom expression. Mechanisms by which this resistance is achieved are poorly understood. In particular, it is still unknown how differences in vascular structure may influence biofilm growth and spread within a host. To address this, we developed a novel theoretical framework to describe biofilm behaviour within xylem vessels, adopting a polymer-based modelling approach. We then parameterised the model to investigate the relevance of xylem vessel diameters on Xylella fastidiosa resistance among olive cultivars. The functionality of all vessels was severely reduced under infection, with hydraulic flow reductions of 2–3 orders of magnitude. However, results suggest wider vessels act as biofilm incubators; allowing biofilms to develop over a long time while still transporting them through the vasculature. By contrast, thinner vessels become blocked much earlier, limiting biofilm spread. Using experimental data on vessel diameter distributions, we were able to determine that a mechanism of resistance in the olive cultivar Leccino is a relatively low abundance of the widest vessels, limiting X. fastidiosa spread.

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Accepted/In Press date: 10 January 2024
e-pub ahead of print date: 25 January 2024
Published date: 21 March 2024
Additional Information: Publisher Copyright: © 2024 The Author(s)
Keywords: Biofilm formation, Multiphase model, Olive, Xylella fastidiosa, Xylem-limited bacterial pathogen

Identifiers

Local EPrints ID: 490090
URI: http://eprints.soton.ac.uk/id/eprint/490090
ISSN: 0022-5193
PURE UUID: bd00c68a-1f34-40f5-b413-8829b228bdc3
ORCID for N.C. Walker: ORCID iD orcid.org/0000-0003-2297-1046
ORCID for D. Mckay fletcher: ORCID iD orcid.org/0000-0001-6569-2931
ORCID for T. Roose: ORCID iD orcid.org/0000-0001-8710-1063

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Date deposited: 14 May 2024 16:47
Last modified: 06 Jun 2024 02:08

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Contributors

Author: N.C. Walker ORCID iD
Author: S.M. White
Author: S.M. Ruiz
Author: D. Mckay fletcher ORCID iD
Author: M. Saponari
Author: T. Roose ORCID iD

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