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.

A 3D image-based modelling approach for understanding spatiotemporal processes in phosphorus fertiliser dissolution, soil buffering and uptake by plant roots.

Phosphorus (P) is a key yield-limiting nutrient for crops, but the main source of P fertiliser is finite. Therefore, efficient fertilisation is crucial. Optimal P application requires understanding of the dynamic processes affecting P availability to plants, including fertiliser dissolution rate and soil buffer power. However, standard soil testing methods sample at fixed time points, preventing a mechanistic understanding of P uptake variability. We used image-based modelling to investigate the effects of fertiliser dissolution rate and soil buffer power on P uptake by wheat roots imaged using X-ray CT. We modelled uptake based on 1-day, 1-week, and 14-week dissolution of a fixed quantity of total P for two common soil buffer powers. We found rapid fertiliser dissolution increased short-term root uptake, but total uptake from 1-week matched 1-day dissolution. We quantified the large effects root system architecture had on P uptake, finding that there were trade-offs between total P uptake and uptake per unit root length, representing a carbon investment/phosphorus uptake balance. These results provide a starting point for predictive modelling of uptake from different P fertilisers in different soils. With the addition of further X-ray CT image datasets and a wider range of conditions, our simulation approach could be developed further for rapid trialling of fertiliser-soil combinations to inform field-scale trials or management.

Quantifying citrate-enhanced phosphate root uptake using microdialysis.

AIMS: Organic acid exudation by plant roots is thought to promote phosphate (P) solubilisation and bioavailability in soils with poorly available nutrients. Here we describe a new combined experimental (microdialysis) and modelling approach to quantify citrate-enhanced P desorption and its importance for root P uptake. METHODS: To mimic the rhizosphere, microdialysis probes were placed in soil and perfused with citrate solutions (0.1, 1.0 and 10 mM) and the amount of P recovered from soil used to quantify rhizosphere P availability. Parameters in a mathematical model describing probe P uptake, citrate exudation, P movement and citrate-enhanced desorption were fit to the experimental data. These parameters were used in a model of a root which exuded citrate and absorbed P. The importance of soil citrate-P mobilisation for root P uptake was then quantified using this model. RESULTS: A plant needs to exude citrate at a rate of 0.73 µmol cm-1 of root h-1 to see a significant increase in P absorption. Microdialysis probes with citrate in the perfusate were shown to absorb similar quantities of P to an exuding root. CONCLUSION: A single root exuding citrate at a typical rate (4.3 × 10-5 µmol m-1 of root h-1) did not contribute significantly to P uptake. Microdialysis probes show promise for measuring rhizosphere processes when calibration experiments and mathematical modelling are used to decouple microdialysis and rhizosphere mechanisms.

Precipitation-optimised targeting of nitrogen fertilisers in a model maize cropping system.

Typically, half of the nitrogen (N) fertiliser applied to agricultural fields is lost to the wider environment. This inefficiency is driven by soil processes such as denitrification, volatilisation, surface run-off and leaching. Rainfall plays an important role in regulating these processes, ultimately governing when and where N fertiliser moves in soil and its susceptibility to gaseous loss. The interaction between rainfall, plant N uptake and N losses, however, remains poorly understood. In this study we use numerical modelling to predict the optimal N fertilisation strategy with respect to rainfall patterns and offer mechanistic explanations to the resultant differences in optimal times of fertiliser application. We developed a modelling framework that describes water and N transport in soil over a growing season and assesses nitrogen use efficiency (NUE) of split fertilisations within the context of different rainfall patterns. We used ninety rainfall patterns to determine their impact on optimal N fertilisation times. We considered the effects of root growth, root N uptake, microbial transformation of N and the effect of soil water saturation and flow on N movement in the soil profile. On average, we show that weather-optimised fertilisation strategies could improve crop N uptake by 20% compared to the mean uptake. In drier years, weather-optimising N applications improved the efficiency of crop N recovery by 35%. Further analysis shows that maximum plant N uptake is greatest under drier conditions due to reduced leaching, but it is harder to find the maximum due to low N mobility. The model could capture contrasting trends in NUE seen in previous arable cropping field trials. Furthermore, the model predicted that the variability in NUE seen in the field could be associated with precipitation-driven differences in N leaching and mobility. In conclusion, our results show that NUE in cropping systems could be significantly enhanced by synchronising fertiliser timings with both crop N demand and local weather patterns.

Image-based quantification of soil microbial dead zones induced by nitrogen fertilization.

Microbial communities in agricultural soils underpin many ecosystem services including the maintenance of soil structure, food production, water purification and carbon storage. However, the impact of fertilization on the health of microbial communities is not well understood. This study investigates the spatial and temporal dynamics of nitrogen (N) transport away from a fertilizer granule with pore scale resolution. Specifically, we examined how soil structure and moisture content influence fertilizer derived N movement through the soil pore network and the subsequent impact of on soil microbial communities. We develop a mathematical model to describe N transport and reactions in soil at the pore-scale. Using X-ray Computed Tomography scans, we reconstructed a microscale description of a soil-pore geometry as a computational mesh. Solving two-phase water/air model produced pore-scale water distributions at 15, 30 and 70% water-filled pore volume. The N-speciation model considered ammonium (NH4+), nitrate (NO3-) and dissolved organic N (DON), and included N immobilization, ammonification and nitrification processes, as well as diffusion in soil solution. We simulated the dissolution of a fertilizer pellet and a pore scale N cycle at three different water saturations. To aid interpretation of the model results, microbial activity at a range of N concentrations was measured. The model showed that the diffusion and concentration of N in water films is critically dependent upon soil moisture and N species. We predict that the maximum NH4+ and NO3- concentrations in soil solution around the pellet under dry conditions are in the order of 1 × 103 and 1 × 104 mol m-3 respectively, and under wet conditions 2 × 102 and 1 × 103 mol m-3, respectively. Supporting experimental evidence suggests that these concentrations would be sufficient to reduce microbial activity in the short-term in the zone immediately around the fertilizer pellet (ranging from 0.9 to 3.8 mm), causing a major loss of soil biological functioning. This model demonstrates the importance of pore-scale processes in regulating N movement and their interactions with the soil microbiome.

Measurement of micro-scale soil deformation around roots using four-dimensional synchrotron tomography and image correlation.

This study applied time lapse (four-dimensional) synchrotron X-ray computed tomography to observe micro-scale interactions between plant roots and soil. Functionally contrasting maize root tips were repeatedly imaged during ingress into soil columns of varying water content and compaction. This yielded sequences of three-dimensional densiometric data, representing time-resolved geometric soil and root configurations at the micronmetre scale. These data were used as inputs for two full-field kinematic quantification methods, which enabled the analysis of three-dimensional soil deformation around elongating roots. Discrete object tracking was used to track rigid mineral grains, while continuum digital volume correlation was used to track grey-level patterns within local sub-volumes. These techniques both allowed full-field soil displacements to be quantified at an intra-rhizosphere spatial sampling scale of less than 300 µm. Significant differences in deformation mechanisms were identified around different phenotypes under different soil conditions. A uniquely strong contrast was observed between intact and de-capped roots grown in dry, compacted soil. This provides evidence that functional traits of the root cap significantly reduce the amount of soil disturbance per unit of root elongation, with this effect being particularly significant in drier soil.