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

Ann Bot. 2024 Oct 30:mcae193. doi: 10.1093/aob/mcae193. Online ahead of print.

Abstract

Background and aims: Mucilage has been hypothesized to soften the gradients in matric potential at the root-soil interface, hereby 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 leveraged 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 the leaf water potential and transpiration rate (E) was linear for both genotypes. However, as the soil progressively dried, the E(ψleaf) relationship exhibited nonlinearity. Genotype with low mucilage production exhibited nonlinearity earlier during soil drying, i.e. in wetter soil conditions, (soil water content < 0.36 cm3 cm-3) compared to Genotype with high mucilage production (soil water content < 0.30 cm3 cm-3). The incidence of nonlinearity 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 genotype 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, hereby postponing the hydraulic limitations to transpiration during soil drying.

Keywords: Drought; Leaf water potential; Plant hydraulics; Rhizosphere; Root exudates; Soil-root interactions; Transpiration.