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

Abstract

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.We 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.To illustrate the tool’s 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.One-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.Authors 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.

Simulating Root Growth as a Function of Soil Strength and Yield With a Field-Scale Crop Model Coupled With a 3D Architectural Root Model

“…In the future, more extended coupling could make use of CRootbox' ability to compute not only the RLD in each soil layer but also root water uptake sink terms for each soil layer based on root hydraulic architecture.The common variable of both models would be root water uptake per layer, and CRootbox would not only pass the RLD but also the root water uptake to SIMPLACE and get the soil matrix potential in each layer from the SIMPLACE soil component beforehand. This will enable to include further processes not accounted for in the current simulations, i.e., root water uptake compensation and recognition of local root hydraulic properties (Meunier et al, 2019 ). Further field data (more seasons per cultivar, more sites) would allow for more robust model calibration.…”

Combining cross‐section images and modeling tools to create high‐resolution root system hydraulic atlases in Zea mays

“…Meunier et al (2020) showed that modifying hydraulic properties changes the root system hydraulic architecture and thus affects the whole root system conductance ( K rs ). Tuning root hydraulic conductivity functions to match experimental data or test new hypotheses through simulation studies could therefore show the local impact of root anatomy or cell hydraulic properties on the whole root system conductance.…”

“…We posit our approach will allow more realistic parametrizations of functional–structural plant models targeting root water uptake. Such a root hydraulic conductivity atlas can as well be connected to complementary modeling tools (e.g., Meunier et al, 2020) to estimate hydraulic parameters such as the root system conductance or the standard sink fraction for models working at larger scales (e.g., Agee et al, 2021; Cai et al, 2018; Sulis et al, 2019), as envisioned by Passot et al (2019). Future modeling studies could reuse the anatomical networks and the root hydraulic conductivities that we built on their root system architecture.…”

“…Among them, the radial hydraulic conductivity ( k r ) is a key component of the water absorption from the soil to the vasculature of the plant, and the axial hydraulic conductance ( k x ) defines the water transport along the root (Leitner et al, 2014). Changes in the local root hydraulic properties, at the cell and organ‐scale, are known to have overall repercussions on the plant hydraulic behavior (Meunier et al, 2020; Tardieu et al, 2018) and are considered as important breeding targets to create drought resilient varieties (Maurel & Nacry, 2020). Quantitative root hydraulic conductivity data along roots are therefore needed for a thorough understanding of root water uptake dynamics.…”

“…Such estimations are so complex that many studies that simulate water uptake with functional–structural root models still rely on the root hydraulic conductivity profiles estimated more than 20 years ago by Doussan, Page, and Vercambre (1998) (e.g., R‐SWMS, Javaux et al, 2008; OpenSimRoot, Postma et al, 2017; or MARSHAL, Meunier et al, 2020). Today, we need new methods to rapidly quantify root hydraulic conductivities from more easily available data.…”