Phenotyping and modeling of root hydraulic architecture reveal critical determinants of axial water transport

Abstract

Water uptake by roots is a key adaptation of plants to aerial life. Water uptake depends on root system architecture (RSA) and tissue hydraulic properties that, together, shape the root hydraulic architecture. This work investigates how the interplay between conductivities along radial (e.g. aquaporins) and axial (e.g. xylem vessels) pathways determines the water transport properties of highly branched RSAs as found in adult Arabidopsis (Arabidopsis thaliana) plants. A hydraulic model named HydroRoot was developed, based on multi-scale tree graph representations of RSAs. Root water flow was measured by the pressure chamber technique after successive cuts of a same root system from the tip towards the base. HydroRoot model inversion in corresponding RSAs allowed us to concomitantly determine radial and axial conductivities, providing evidence that the latter is often overestimated by classical evaluation based on the Hagen-Poiseuille law. Organizing principles of Arabidopsis primary and lateral root growth and branching were determined and used to apply the HydroRoot model to an extended set of simulated RSAs. Sensitivity analyses revealed that water transport can be co-limited by radial and axial conductances throughout the whole RSA. The number of roots that can be sectioned (intercepted) at a given distance from the base was defined as an accessible and informative indicator of RSA. The overall set of experimental and theoretical procedures was applied to plants mutated in ESKIMO1 and previously shown to have xylem collapse. This approach will be instrumental to dissect the root water transport phenotype of plants with intricate alterations in root growth or transport functions.

High-throughput and automatic structural and developmental root phenotyping on Arabidopsis seedlings

“…Root system shape, structure, and plasticity impact its efficiency and condition the plant fitness in fluctuating environments [ 1 ]. The root system architecture (RSA) is dramatically affected by spatial and temporal changes in the soil environment that, in turn, will modify its water and nutrients capture efficiency [ 3 ]. These adaptive responses, including branching angles and frequencies of lateral roots, rely on growth rate modifications of the different root classes (e.g., primary, seminal, lateral, or adventitious roots).…”

High-throughput and automatic structural and developmental root phenotyping on Arabidopsis seedlings

“…Root system shape, structure, and plasticity impact its efficiency and condition the plant fitness in fluctuating environments (Balduzzi et al, 2017). The root system architecture (RSA) is dramatically affected by spatial and temporal changes in the soil environment that, in turn, will modify its water and nutrients capture efficiency (Boursiac et al, 2022). These adaptive responses, including branching angles and frequencies of lateral roots, rely on growth rate modifications of the different root classes (e.g., primary, seminal, lateral, or adventitious roots).…”

The flow of water: Critical factors of root axial water transport determined

“…Using this method, and in combination with HydroRoot, both axial and radial conductances were obtained in a single experiment and for the same plant. With this approach, Boursiac et al (2022a ) showed that axial conductance in particular increases less with distance to the root tip than expected from classical models. They found that, in highly branched root systems, axial hydraulic conductance can be as strongly limiting as radial hydraulic conductance for water transport to shoots ( Figure 1 ).…”

“…In this issue of Plant Physiology , Boursiac et al (2022a ) developed the hydraulic mathematical model “HydroRoot” and used it in combination with a cut-and-flow experimental procedure to investigate root hydraulic conductance of complex and highly branched root systems. In cut-and-flow experiments, entire root systems were placed into a pressure chamber, and the shoots were removed to measure pressure-induced sap flow.…”

“…They found that, in highly branched root systems, axial hydraulic conductance can be as strongly limiting as radial hydraulic conductance for water transport to shoots ( Figure 1 ). While Boursiac et al (2022a ) used the model plant Arabidopsis ( Arabidopsis thaliana , Brassicaceae ), similar highly branched roots systems are present in many of our noncereal crops, ranging from potatoes ( Solanum tuberosum, Solanaceae ) and common beans ( Phaseolus vulgaris , Fabaceae ) to lettuce ( Lactuca sativa , Asteraceae ) and cotton ( Gossypium hirsutum , Malvaceae ).…”