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Data Intensive Modelling of the Rhizosphere Processes

Periodic Reporting for period 4 - DIMR (Data Intensive Modelling of the Rhizosphere Processes)

Reporting period: 2020-03-01 to 2021-08-31

We rely on soil to support the crops on which we depend. Less obviously we also rely on soil for a host of 'free services' from
which we benefit. For example, soil buffers the hydrological system greatly reducing the risk of flooding after heavy rain; soil
contains very large quantities of carbon, which would otherwise be released into the atmosphere where it would contribute to
climate change. Given its importance it is not surprising that soil, especially its interaction with plant roots, has been a focus
of many researchers. However the complex and opaque nature of soil has always made it a difficult medium to study.
In this ERC research program I will develop a state of the art image based model of the physical and chemical properties of
soil and soil-root interactions, i.e. a quantitative, model of the rhizosphere based on fundamental scientific laws.
This will be realised by a combination of innovative, data rich fusion of structural and chemical imaging methods, integration
of experimental efforts to both support and challenge modelling capabilities at the scale of underpinning bio-physical
processes, and application of mathematically sound homogenisation/scale-up techniques to translate knowledge from
rhizosphere to field scale. The specific science questions I will address with these techniques are: (1) how does the soil
around the root, the rhizosphere, function and influence the soil ecosystems at multiple scales, (2) what is the role of rootsoil
interface micro morphology and mycorrhizae on plant nutrient uptake, (3) what is the effect of plant exuded mucilage on
the soil morphology, mechanics and resulting field and ecosystem scale soil function and (4) how to translate this knowledge
from the single root scale to root system, field and ecosystem scale in order to predict how the climate change, different soil
management strategies and plant breeding will influence the soil fertility.
This project focuses on investigating how plants and soil interact in order to gain a better understanding of the fundamental processes which control this system. With this improved understanding scientist will then able to provide advice to agronomists, farmers, managers etc. how to better manage crops, soils and natural ecosystems. In particular, we are using correlative structural imaging and chemical elemental mapping to build new models of plant-soil interaction. These new models will enable in silico scenario testing of different soil and crop management scenarios.

As an indication of the prestige and the visibility the ERC award brought to our group within the soil and rhizosphere science community the PI was invited to write the 2016 annual Marschner Review (Roose et al 2016) for the journal Plant and Soil; these reviews are commissioned by the journal to highlight a new trend within the journals field. We believe our review is the first co-authored by an interdisciplinary group that includes mathematicians, engineers, soil scientists and geochemists.

There have been 3 main strands within our research during our project thus far.

The first strand has developed a technique for imaging how plant roots interact with mycorrhizal fungi in the soil using X-ray Computed Tomography for the first time. We developed a microscale assay to enable imaging at synchrotron beamlines by a combination of microfabrication and 3D printing. Following successful imaging at the Diamond Light Source and at Swiss Light Source using both phase contrast and adsorption modalities we have finished the image analysis and quantified the morphological parameters associated with plant-mycorrhizae-soil interaction (total 198 scans of 66 samples resulted in 8.43 TB of structural data). These findings have been confirmed by conventional methods developed by Iver Jakobsen (Denmark) under his guidance and training. Following the morphological imaging the samples were frozen and transported back to Southampton where they were resin fixed for XRF elemental mapping which was completed at the Swiss Light Source (Switzerland) and Diamond Light Source (UK). Following this we were able to correlate elemental mapping with structural mapping and integrate both experimental outputs into the predictive mathematical model describing plant-mycorrhizae-soil interaction.

The second strand of the project is focusing on applying imaging to the micromechanics of root-soil interaction with particular emphasis on understanding how roots move through soil. We used X-ray CT and image analysis techniques to address this problem and published two papers on this work (Keyes et al 2016, 2017). In addition we have published a paper that first time shows how it is possible to image root exudates, that are thought to aid root movement through soil, using a combination of NMR and X-ray CT (Van Veelen et al 2019). In this stream we have also investigated the mechanics and drying behaviour of the root exuded mucilage using a combination of optical and NMR imaging (Williams et al 2021).

The third strand is imaged based modelling of soil solute and water dynamics and solid mechanics. We have published three fundamental papers on this work (Daly et al 2016, Cooper et al 2017, Daly&Roose 2017) and have one more pending minor corrections (Daly et al 2018). In addition, we are now starting to consolidate these theoretical developments with full structural and chemical imaging and the first paper in this stream has already been submitted in Dec 2017 (McKay-Fletcher et al 2017 Plant Soil).

The fourth strand deals with imaging and monitoring soil chemistry in large mesocosms using the combination of in house X-ray CT and microdialysis soil solution sampling. By combinging structural imaging and ICPMS with microdialysis allows us to monitor and then predict plant P uptake from soil and calibrate the mathematical models so they are with strong predictive power. This has resulted in one paper being published already (Petroselli et al 2020) with the second one being currently completed. Note the paper Petroselli et al 2020 also won a major international prize (see below) by the International Fertilizer Society.

This project combines these techniques, which in themselves are novel and unconventional, in synergistic and novel ways. Thus we are applying X-ray CT structural scanning of soil and plants in real soils in 4D (3D+time) in combination with XRF and SEMEDX elemental mapping of the same samples (live or resin fixed) in combination with pore scale modelling. We have already published a number of papers in this area (Daly et al 2017, Cooper et al 2017, Keyes et al 2016ab,2017, Daly et al 2016). In addition, we have included NMRI in our imaging arsenal since we believe this technique has considerable potential for measuring root exudate dynamics in 4D (3D+time) in real soil (Van Veelen et al 2019). Whilst each of these techniques are being applied to soil-plant science in a novel way as part of our project, we are in addition combining these techniques leading to insights which cannot be gained any other way.

I would also like to bring to you attention the following international major awards that my team and I have been awarded in 2020/21 reporting period:
1. Dr Chiara Petroselli was awarded the Brian Chambers Award for Early Career Researchers in Crop Nutrition by the International Fertiliser Society. See the new nugget at this link:
2. Dr. Dan McKay Fletcher was awarded the runner up prize in the Brian Chambers Award for the Early Career Researchers.
3. Professor Tiina Roose received the Rien Van Genuchten Award for Outstanding Contributions and Advanced Modelling of Flow and Transport Processes in Soils awarded by the International Soil Modelling Consortium.
The progress beyond the state of the art can be summarised by the following 3 statements related to the recently published papers.

1. Cooper et al (2017) “Fluid flow in porous media using image based modelling to parametrise Richards’ equation” in Proceedings of The Royal Society A. This is the first paper in the world to show how Richards’ equation could be parameterised from the soil underlying observed geometry. This is important for the two reasons: (a) the conventional experimental measurements to properly parameterise Richards’ equation are very time consuming (3+ months), however our computational image based approach is much faster (couple of weeks depending on soil and availability of the imaging equipment) thus enabling the possibility of high throughput comparison of different soils and guiding of soil amendments based on in silico computations. (b) conventional measurements cannot be conducted on the rhizosphere (ie region of soil influenced by roots) scale since this region is very small (<=1mm) and traditional methods could not be used since stable structural and biological sampling is not possible, and hence the non-invasive image based modelling is the only way to address this. As an evidence of the importance of this paper one reviewer wrote that “… this is the biggest breakthrough since 1953 when Lorenzo Richards published his thesis” and whilst the paper was published on Nov 22nd 2017, during the month of Nov 2017 (ie in 9 days) it was read by 200+ times and as of March 1st 2018 it had been read by over 700 times.
2. As the second “paper” I want to name two interlinked papers, Keyes et al (2017) and (2016) that dealt with imaging plant root growth in the soil. The paper published in 2016 dealt with single entire root scale imaging of root growth in 4D (3D+time) and estimating how the soil strains using the image analysis tools. The paper published in 2017 did the same at the high resolution near the individual root tip thus for the first time showing how to observe the micromechanics of root growth in real soil. The reason why these papers are important is that they set up for the first time an experimental and image analysis protocol to enable the time-lapse observation of root architecture. Most of the previous imaging has not been able to image root growth at the timescales where one could observe grain movement, soil pore water movement etc. However, this is important if one wants to (a) have fundamental understanding of how plant roots grow in soil and (b) how to modify the roots or soil amendments to enhance, or in impede, root growth and function in the soil. This knowledge will be useful for situations where we would like to use plants or grow crops in soils which are prone to instability, landsildes, and flooding.
3. As the third paper I would like to discusse Van Veelen et al (2019) which combines correlatively structural observations of soil mechanics using X-ray CT and elemental mapping using XRF and XANES. As part of this paper we introduce the concpt of root microbial incubator as we show for the first time that all/most microbially mediated soil chemcial transformations are primarily constrained to the zone around the root that is phyiscally sealed off from the bulk soil. This zone seems to also be influenced by the presence of root hairs and thus potentially offers a way for manipulating it if needed.
3. As the final paper I am naming is the invited Marschner Review Roose et al “Challenges in imaging and predictive modelling of rhizosphere processes” published in Plant and Soil in 2016. It was a huge honour to be a first mathematician to write this one a year commissioned review and with the help of the team of co-authors we did a great job and as a result paper has been downloaded over 4400 times and already cited 12 times.

Going onwards, after having completed most/all of the soil microscale imaging and modelling work we will move forwards to integrate these microscale findings into the larger, soil pot, scale studies. This will necessarily include introduction of new chemical sensing methodologies since the microscale techniques, such as XRF and SEM-EDX, are not necessarily suitable in the larger samples without introducing major observational artefacts. In the next year we will endeavour to use micro dialysis probe soil solution sampling in combination with X-ray CT and analyse the chemical time resolved samples using high precision ICPMS. We will integrate all these findings into an a pot scale model of the plant P uptake. The experimental aspects of the study were clearly impeded by COVID-19 induced societal and lab lockdowns, but we believe our project tis now well on track to be completed in time. Most notably, our work on mentoring and modelling P release from fertiliser pellet (Petroselli et al 2021) won Chiara Petroselli a first/top prize in the International Fertiliser Society 2020 Brian Chambers Award for Early Career Achievements in Crop Nutrition. It was an international competition with 10 finalists from across all continents. Not only did my ERC postdoc Chiara Petroselli win the top award, but another postdoc Dan McKay Fletcher shared one of the two runner up prizes.
Image of SXRCT of fungi in the soil.
Root scavenging P pellet, root — yellow, P — green and S — blue
Citrate concentrations on 2D planes for a young wheat root system. Citrate solution concentration at
Visual comparison of sub-regions of the aligned XCT slice, BSEI and P EDS map for each thin-sec
Comparison of 3D morphological features during drying from a modelled liquid bridge representing pla
Visulization of root P uptake evolution for high/low buffering soils and 3 fertiliser dissolution ra