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Couvreur, V.

Publications and source records attributed to Couvreur, V..

9 recordsLinked to original sources

Secondary Growth and Exodermal Barriers Shape Local Root Hydraulics: Modeling Insights in Tomato

Root water uptake efficiency depends on root system architecture and anatomical features of individual root segments. Beyond cell wall, membrane, and plasmodesmata hydraulic properties, root anatomy critically influences profiles of radial conductivity and axial conductance. While these structural factors have been well-characterized in monocotyledons, their role in dicotyledons--where developmental anatomy, secondary growth, and hydrophobic barrier dynamics differ--remains poorly understood. Here, we integrate structural and functional models to assess how dicotyledon-specific anatomy, hydrophobic depositions (suberin/lignin in exo-/endodermis), and aquaporin contribution influence root hydraulics. Using tomato (Solanum lycopersicum L., cv. Moneymaker) as a dicotyledon model, our simulations show that: - Exodermal suberin has negligible effects on radial conductivity when a lignin cap is present, and exodermal barriers are less effective than endodermal ones. - Secondary growth and dicotyledon-specific anatomy are essential for sustaining high axial conductance, ensuring efficient water uptake across soil profiles and maintaining root system hydraulic conductance.

plant biology↗

Root hydraulic properties: an exploration of their variability across scales

Root hydraulic properties are key physiological traits that determine the capacity of root systems to take up water, at a specific evaporative demand. They can strongly vary among species, cultivars or even within the same genotype, but a systematic analysis of their variation across plant functional types (PFTs) is still missing. Here, we reviewed published empirical studies on root hydraulic properties at the segment-, individual root-, or root system scale and determined its variability and the main factors contributing to it. We observed an extremely large range of variation (of orders of magnitude) in root hydraulic properties, but this was not caused by systematic differences among PFTs. Rather, the (combined) effect of factors such as root system age, driving force used for measurement, or stress treatments shaped the results. We found a significant decrease in root hydraulic properties under stress conditions (drought and aquaporin inhibition) and a significant effect of the driving force used for measurement (hydrostatic or osmotic gradients). Furthermore, whole root system conductance increased significantly with root system age across several crop species, causing very large variation in the data (> 2 orders of magnitude). Interestingly, this relationship showed an asymptotic shape, with a steep increase during the first days of growth and a flattening out at later stages of development. This behaviour was also observed in simulations with computational plant models, suggesting common patterns across studies and species. These findings provide better understanding of the main causes of root hydraulic properties variations observed across empirical studies. They also open the door to better representation of hydraulic processes across multiple plant functional types and at large scales. All data collected in our analysis has been aggregated into an open access database (https://roothydraulic-properties.shinyapps.io/database/), fostering scientific exchange.

plant biology↗

Evidence for a multicellular symplasmic water pumping mechanism across vascular plant roots

With global warming, climate zones are projected to shift poleward, and the frequency and intensity of droughts to increase, driving threats to crop production and ecosystems. Plant hydraulic traits play major roles in coping with such droughts, and process-based plant hydraulics (water flowing along decreasing pressure {Psi}p or total water potential {Psi}tot gradients) has newly been implemented in land surface models. An enigma reported for the past 35 years is the observation of water flowing along increasing water potential gradients across roots. By combining the most advanced modelling tool from the emerging field of plant micro-hydrology with pioneering cell solute mapping data, we found that the current paradigm of water flow across roots of all vascular plants is incomplete: it lacks the impact of solute concentration (and thus negative osmotic potential {Psi}o) gradients across living cells. This gradient acts as a water pump as it reduces water tension without loading solutes in plant vasculature (xylem). Importantly, water tension adjustments in roots may have large impacts in leaves due to the tension-cavitation feedback along stems. Here, we mathematically demonstrate the water pumping mechanism by solving water flow equations analytically on a triple-cell system. Then we show that the simplistic upscaled equations hold in 2- and 3-D maize, grapevine and Arabidopsis complex hydraulic anatomies, and that water may flow "uphill" of water potential gradients toward xylem as observed experimentally. Besides its contribution to the fundamental understanding of plant water relations, this study lays new foundations for future multidisciplinary research encompassing plant physiology and ecohydrology, and has the ambition to mathematically capture a keystone process for the accurate forecasting of plant water status in crop models and LSMs. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=141 SRC="FIGDIR/small/439789v1_ufig1.gif" ALT="Figure 1"> View larger version (85K): org.highwire.dtl.DTLVardef@a7db9borg.highwire.dtl.DTLVardef@42bb32org.highwire.dtl.DTLVardef@1100204org.highwire.dtl.DTLVardef@1f45a48_HPS_FORMAT_FIGEXP M_FIG C_FIG Highlights- We provide a scale-consistent solution of water flow equations across root tissues - Symplasmic osmotic potential gradients are missing in the current theory of root water uptake - The model solves the empirical enigma of root water uptake uphill of water potential gradients

physiology↗

Connecting the dots between root cross-section images and modelling tools to create a high resolution root system hydraulic maps in Zea mays.

Root hydraulic properties play a central role in the global water cycle, agricultural systems productivity, and ecosystem survival as they impact the global canopy water supply. However, the available experimental methods to quantify root hydraulic conductivities, such as the root pressure probing, are particularly challenging and their applicability on thin roots and small root segments is limited. There is a gap in methods enabling easy estimations of root hydraulic conductivities across a diversity of root types and at high resolution along root axes. In this case study, we analysed Zea mays (maize) plants of the var. B73 that were grown in pots for 14 days. Root cross-section data were used to extract anatomical measurements. We used the Generator of Root Anatomy in R (GRANAR) model to generate root anatomical networks from anatomical features. Then we used the Model of Explicit Cross-section Hydraulic Anatomy (MECHA) to compute an estimation of the root axial and radial hydraulic conductivities (kx and kr, respectively), based on the generated anatomical networks and cell hydraulic properties from the literature. The root hydraulic conductivity maps obtained from the root cross-sections suggest significant functional variations along and between different root types. Predicted variations of kr along the root axis were strongly dependent on the maturation stage of hydrophobic barriers. The same was also true for the maturation rates of the metaxylem. The different anatomical features, as well as their evolution along the root type add significant variation to the kr estimation in between root type and along the root axe. Under the prism of root types, anatomy, and hydrophobic barriers, our results highlight the diversity of root radial and axial hydraulic conductivities, which may be veiled under low-resolution measurements of the root system hydraulic conductivity. While predictions of our root hydraulic maps match the range and trend of measurements reported in the literature, future studies could focus on the quantitative validation of hydraulic maps. From now on, a novel method, which turns root cross-section images into hydraulic maps will offer an inexpensive and easily applicable investigation tool for root hydraulics, in parallel to root pressure probing experiments. One-Sentence summaryThe use of cross-section images and modelling tools to generate a map the axial and radial hydraulic conductivity along different root types for the maize cultivar B73.

plant biology↗

Call for participation: Collaborative benchmarking of functional-structural root architecture models. The case of root water uptake.

Three-dimensional models of root growth, architecture and function are becoming important tools that aid the design of agricultural management schemes and the selection of beneficial root traits. However, while benchmarking is common in many disciplines that use numerical models such as natural and engineering sciences, functional-structural root architecture models have never been systematically compared. The following reasons might induce disagreement between the simulation results of different models: different representation of root growth, sink term of root water and solute uptake and representation of the rhizosphere. Presently, the extent of discrepancies is unknown, and a framework for quantitatively comparing functional-structural root architecture models is required. We propose, in a first step, to define benchmarking scenarios that test individual components of complex models: root architecture, water flow in soil and water flow in roots. While the latter two will focus mainly on comparing numerical aspects, the root architectural models have to be compared at a conceptual level as they generally differ in process representation. Therefore defining common inputs that allow recreating reference root systems in all models will be a key challenge. In a second step, benchmarking scenarios for the coupled problems are defined. We expect that the results of step 1 will enable us to better interpret differences found in step 2. This benchmarking will result in a better understanding of the different models and contribute towards improving them. Improved models will allow us to simulate various scenarios with greater confidence and avoid bugs, numerical errors or conceptual misunderstandings. This work will set a standard for future model development.

plant biology↗

MARSHAL, a novel tool for virtual phenotyping of maize root system hydraulic architectures

Functional-structural root system models combine functional and structural root traits to represent the growth and development of root systems. In general, they are characterized by a large number of growth, architectural and functional root parameters, generating contrasted root systems evolving in a highly nonlinear environment (soil, atmosphere), which makes unclear what impact of each single root system on root system functioning actually is. On the other end of the root system modelling continuum, macroscopic root system models associate to each root system instance a set of plant-scale, easily interpretable parameters. However, as of today, it is unclear how these macroscopic parameters relate to root-scale traits and whether the upscaling of local root traits are compatible with macroscopic parameter measurements. The aim of this study was to bridge the gap between these two modelling approaches by providing a fast and reliable tool, which eventually can help performing plant virtual breeding.\n\nWe describe here the MAize Root System Hydraulic Architecture soLver (MARSHAL), a new efficient and user-friendly computational tool that couples a root architecture model (CRootBox) with fast and accurate algorithms of water flow through hydraulic architectures and plant-scale parameter calculations, and a review of architectural and hydraulic parameters of maize.\n\nTo illustrate the tools potential, we generated contrasted maize hydraulic architectures that we compared with architectural (root length density) and hydraulic (root system conductance) observations. Observed variability of these traits was well captured by model ensemble runs We also analyzed the multivariate sensitivity of mature root system conductance, mean depth of uptake, root system volume and convex hull to the input parameters to highlight the key parameters to vary for efficient virtual root system breeding. MARSHAL enables inverse optimisations, sensitivity analyses and virtual breeding of maize hydraulic root architecture. It is available as an R package, an RMarkdown pipeline, and a web application.\n\nOne-sentence summaryWe developed a dynamic hydraulic-architectural model of the root system, parameterized for maize, to generate contrasted hydraulic architectures, compatible with field and lab observations and that can be further analyzed in soil-root system models for virtual breeding.\n\nAuthors contributionsF.M., X.D., M.J. and G.L. designed the study and defined its scope; F.M. and G.L. developed the model while associated tools were created by A.H. and G.L.; F.M. ran the model simulations and analyzed the results together with M.J and G.L.; F.M. and M.J. wrote the first version of this manuscript; all co-authors critically revised it.

plant biology↗

GRANAR, a new computational tool to better understand the functional importance of root anatomy

Root hydraulic conductivity is an important determinant of plant water uptake capacity. In particular, the root radial conductivity is often thought to be a limiting factor along the water pathways between the soil and the leaf. The root radial conductivity is itself defined by cell scale hydraulic properties and anatomical features. However, quantifying the influence of anatomical features on the radial conductivity remains challenging due to complex, and time-consuming, experimental procedures.\n\nWe present a new computation tool, the Generator of Root ANAtomy in R (GRANAR) that can be used to rapidly generate digital versions of root anatomical networks. GRANAR uses a limited set of root anatomical parameters, easily acquired with existing image analysis tools. The generated anatomical network can then be used in combination with hydraulic models to estimate the corresponding hydraulic properties.\n\nWe used GRANAR to re-analyse large maize (Zea mays) anatomical datasets from the literature. Our model was successful at creating virtual anatomies for each experimental observation. We also used GRANAR to generate anatomies not observed experimentally, over wider ranges of anatomical parameters. The generated anatomies were then used to estimate the corresponding radial conductivities with the hydraulic model MECHA. This enabled us to quantify the effect of individual anatomical features on the root radial conductivity. In particular, our simulations highlight the large importance of the width of the stele and the cortex.\n\nGRANAR is an open-source project available here: http://granar.github.io\n\nOne-Sentence summaryGenerator of Root ANAtomy in R (GRANAR) is a new open-source computational tool that can be used to rapidly generate digital versions of root anatomical networks.

plant biology↗

Connecting the dots between computational tools to analyse soil-root water relations

In the recent years, many computational tools, such as image analysis, data management, process-based simulation and upscaling tools, were developed to help quantify and understand water flow in the soil-root system, at multiple scales (tissue, organ, plant and population). Several of these tools work together or, at least, are compatible. However, for the un-informed researcher, they might seem disconnected, forming a unclear and disorganised succession of tools.\n\nIn this article, we present how different pieces of work can be further developed by connecting them to analyse soil-root-water relations in a comprehensive and structured network. This \"explicit network of soil-root computational tools\" informs the reader about existing tools and help them understand how their data (past and future) might fit within the network. We also demonstrate the novel possibilities of scale-consistent parameterizations made possible by the network with a set of case studies from the literature. Finally, we discuss existing gaps in the network and how we can move forward to fill them.\n\nHighlightsMany computational tools exist to quantify water flow in the soil-root system. These tools can be arranged in a comprehensive network that can be leveraged to better interpret experimental data.

plant biology↗

Novel multiscale insights into the composite nature of water transport in roots

- MECHA is a novel mathematical model that computes the flow of water through the walls, membranes and plasmodesmata of each individual cell throughout complete root cross-sections, from a minimal set of cell level hydraulic properties and detailed root anatomical descriptions.\n- Using the hydraulic anatomical framework of the Zea mays root reveals that hydraulic principles at the cell and root segment scales, derived independently by Katchalsky and Curran [1967] and Fiscus and Kramer [1975], are fully compatible, irrespective of apoplastic barriers leakiness.\n- The hydraulic anatomy model accurately predicts empirical root radial permeability (kr) from relatively high cell wall hydraulic conductivity and low plasmodesmatal conductance reported in the literature.\n- MECHA brings novel insights into contradictory interpretations of experiments from the literature by quantifying the impact of intercellular spaces, cortical cell permeability and plasmodesmata among others on root kr, and suggests new experiments efficiently addressing questions of root water relations.\n\n\nSymbols

plant biology↗