Mucilage facilitates root water uptake under edaphic stress: first evidence at the plant scale

Abstract

Background and aims: Mucilage has been hypothesized to soften the gradients in matric potential at the root-soil interface, thereby facilitating root water uptake in dry soils and maintaining transpiration with a moderate decline in leaf water potential. So far, this hypothesis has been tested only through simplified experiments and numerical simulations. However, the impact of mucilage on the relationship between transpiration rate (E) and leaf water potential (ψleaf) at the plant scale remains speculative.

Methods: We utilized an automated root pressure chamber to measure the E(ψleaf) relationship in two cowpea genotypes with contrasting mucilage production. We then utilized a soil-plant hydraulic model to reproduce the experimental observations and inferred the matric potential at the root-soil interface for both genotypes.

Key results: In wet soil, the relationship between leaf water potential and transpiration rate (E) was linear for both genotypes. However, as the soil progressively dried, the E(ψleaf) relationship exhibited non-linearity. The genotype with low mucilage production exhibited non-linearity earlier during soil drying, i.e. in wetter soil conditions (soil water content <0.36 cm3 cm-3) compared to the genotype with high mucilage production (soil water content <0.30 cm3 cm-3). The incidence of non-linearity was concomitant with the decline in matric potential across the rhizosphere. High mucilage production attenuated water potential diminution at the root-soil interface with increased E. This shows, for the first time at the plant scale, that root mucilage softened the gradients in matric potential and maintained transpiration in drying soils. The model simulations indicate that a plausible explanation for this effect is an enhanced hydraulic conductivity of the rhizosphere in genotypes with higher mucilage production.

Conclusions: Mucilage exudation maintains the hydraulic continuity between soil and roots and decelerates the drop in matric potential near the root surface, thereby postponing the hydraulic limitations to transpiration during soil drying.

Keywords: Drought; leaf water potential; plant hydraulics; rhizosphere; root exudates; soil–root interactions; transpiration.

Fig. 1.

Illustration of the anticipated effects of contrasting root mucilage production on soil–root hydraulics. Without mucilage, the soil matric potential will drop steeply at the root surface, as indicated by the red arrow, which hinders root water uptake (blue arrow). On the other hand, high mucilage concentration at the root surface will maintain the hydraulic conductance between root and soil, and attenuate the decline in matric potential at the root surface (red arrow), hence maintaining root water uptake in drying soils (blue arrow). The figure was made in BioRender: Abdalla, M. (2024) https://BioRender.com/s66t170.

Fig. 2.

Relationship between balancing pressure and transpiration rate in two cowpea genotypes with contrasting mucilage production during soil drying. (A) Genotype with high mucilage production. (C) Genotype with low mucilage production. Open symbols represent direct measurements, while dotted lines indicate linear interpolations based on the slope of the first four data points. The relationship is linear in wet soil and exhibits non-linearity as soil progressively dries. B and D show water potential decrease across the rhizosphere, in response to increasing transpiration rate, for the genotype with high mucilage (B) and for the genotype with low mucilage production (D). Declining soil water content (θ, cm³ cm⁻³) is indicated by the colour map. Asterisks denote linear relationships based on a segmented linear model.

Fig. 3.

Coefficient estimates of segmented linear regression of the relationship between transpiration rate and balancing pressure (P) for the high mucilage genotype (A, C and E) and low mucilage genotype (B, D and F). Both A and B depict the breakpoint (BP) when the relationship changes from linear to non-linear. The slope of the relationship before the BP (Slope1; cm³ s⁻¹ MPa⁻¹) is shown in C and D, while the slope of the relationship after the BP (Slope2; cm³ s⁻¹ MPa⁻¹) is shown in E and F.

Fig. 4.

Relationship between balancing pressure (P) and transpiration rate (E) as reproduced by the soil–plant hydraulic model for the genotype with high mucilage production (A) and genotype with low mucilage production (B). Solid lines stand for modelling simulations and symbols for data measurements.

Fig. 5.

Soil hydraulic conductivity (K_s) curve fitted by the Brooks and Corey model. The soil–plant hydraulic model predicted K_s in the rhizosphere during soil drying. The genotype with high mucilage production has decreased saturated hydraulic conductivity but higher unsaturated conductivity in more negative soil matric potential (ψ_soil) compared to the other genotype and unplanted soil (referred to as no mucilage).