Field plants strategically regulate water uptake from different soil depths by spatiotemporally adjusting their radial root hydraulic conductivity

Introduction

With drought occurrences projected to increase due to climate change, breeding crops tolerant to water stress has become crucial to sustaining crop yields and meeting the growing demand for food (Davies & Bennett, 2015). Among various techniques, developing cultivars with deep roots and improved rhizosphere has been proposed as a potential solution to address this challenge (Lynch, 2013, 2019; Gao et al., 2016; Rabbi et al., 2018; Hallett et al., 2022). However, root water uptake depends not only on root architecture and its rhizosphere (Zhu et al., 2024), but also on other abiotic and biotic factors (Vadez, 2014; Q. Sun et al., 2021). Phenotyping root morphology and analysing the rhizosphere alone is thus insufficient to determine the water use efficiency of plants, and understanding the response of other root traits to environmental changes is also important (Vadez, 2014). In fact, experimental observations have shown that not all plants with deep roots increased their water uptake from the deep soil when the topsoil dried (Prechsl et al., 2015; Rasmussen et al., 2020; Gessler et al., 2022; Deseano Diaz et al., 2023), and a recent meta-analysis showed that root depth does not necessarily equate to root water uptake depth (Bachofen et al., 2024). These suggest the existence of additional mechanisms that regulate root water uptake from different soil layers (Kulmatiski & Beard, 2013).

Water ascent in plants is driven by a water potential gradient between soil and leaves. Plants regulate this process by modifying their hydraulic conductance in different organs (Bartlett et al., 2016). In the aboveground, plants cope with water stress by stomatal closure (Hopmans & Bristow, 2002; Carminati & Javaux, 2020; Corso et al., 2020), and xylem embolisation (Loepfe et al., 2007; Bartlett et al., 2016; Scoffoni et al., 2017; Gao et al., 2020), while the strategies plants use to extract water from different soil layers in the field remain elusive (Kühnhammer et al., 2020). Root water uptake involves two distinct yet interconnected processes: radial water flow from the rhizosphere into root xylem vessels, and axial water flow through the xylem vessels (Vadez, 2014). Compared to axial water flow, the pathways through which water moves from the rhizosphere into the xylem are multiple and complicated (Steudle & Peterson, 1998; Johnson et al., 2014; Domec et al., 2021). Recent research indicated that the resistances of these pathways control not only water flow in the soil–plant–atmosphere system but also stomatal closure when the soil dried (Carminati & Javaux, 2020; Abdalla et al., 2021; Cai et al., 2022; Yang et al., 2023).

The molecular and biophysical mechanisms regulating the response of radial root hydraulic conductivity to water stress are fairly understood for a single root segment (Maurel & Nacry, 2020). The difficulty is in extrapolating these findings to the field where soil water varies spatiotemporally (Tardieu et al., 1992). Unlike controlled pots and hydroponic experiments that intentionally dehydrated part of a root system and kept the other part adequately hydrated for a limited period (Zhang & Davies, 1987; Dodd et al., 2010; Kreszies et al., 2020; Suresh et al., 2024), roots at different depths in the field represent different parts or branches of the same root system, where the shallow roots experience periodic wetting–drying cycles due to irregular precipitation and irrigation, while the deep roots generally stay in a relatively stable and moist condition. It has been found that roots in the subsoil could increase their water uptake as a compensation when the topsoil dried, indicating the presence of signals that coordinate root water uptake from different soil depths (Simunek & Hopmans, 2009; Couvreur et al., 2012; Thomas et al., 2020). Theoretical modelling indicates plants can increase subsoil water uptake by either decreasing (more negative) its root water potential or increasing the ratio of the axial root conductance to the radial root hydraulic conductance (Draye et al., 2010). However, experimental studies on compensatory root water uptake have produced mixed results, with some finding compensatory uptake (Johnson et al., 2014; Thomas et al., 2020; Müllers et al., 2023), while others showed no or limited increase in subsoil water uptake when shallow roots experienced water stress (Gessler et al., 2022; Müllers et al., 2023).

Plants under water stress tend to maintain their water status by modifying their root hydraulic network to regulate water uptake (Clarkson et al., 2000; Maurel et al., 2010). For example, column experiments have shown that in the absence of water stress, shallow roots of some plants were more effective in taking up water than their roots in the subsoil (Müllers et al., 2022), while under water stress, the plants reduced the hydraulic conductance of their shallow roots, accompanied by an increase in hydraulic conductivity of their roots in the subsoil to sustain transpiration (Müllers et al., 2023). Most experimental studies on root response to water stress have focused on changes in root hydraulic conductance of plants grown in pots or hydroponic systems by imposing a water stress for a limited period (Hu et al., 2011; Müllers et al., 2023). In the field, plants experience periodic water stress, and their roots penetrate much deeper. The strategies plants use to cope with such periodic water stress in the field are poorly understood because of the difficulties associated with in situ measurements. This paper aims to bridge this knowledge gap.

We developed a method to continuously measure and calculate daily root water uptake, root water potential, and radial root water permeability at different depths in a wheat (Triticum aestivum L.) field and a permanent grassland dominated by perennial ryegrass (Lolium perenne L.) from 1 April to 30 June 2022. During this period, there were two significant rainfall events. These allow us to elucidate the strategies the two plant systems used to cope with periodic water stress and the differences in their use of these strategies.