Stomatal closure of tomato under drought is driven by an increase in soil-root hydraulic resistance.

Mohanned Abdalla,Mutez Ali Ahmed,Mathieu Javaux,Andrea Carminati,Gaochao Cai

doi:10.1111/pce.13939

Abstract

The fundamental question as to what triggers stomatal closure during soil drying remains contentious. Thus, we urgently need to improve our understanding of stomatal response to water deficits in soil and atmosphere. Here, we investigated the role of soil-plant hydraulic conductance (Ksp ) on transpiration (E) and stomatal regulation. We used a root pressure chamber to measure the relation between E, leaf xylem water potential (ψleaf-x ) and soil water potential (ψsoil ) in tomato. Additional measurements of ψleaf-x were performed with unpressurized plants. A soil-plant hydraulic model was used to simulate E(ψleaf-x ) for decreasing ψsoil . In wet soils, E(ψleaf-x ) had a constant slope, while in dry soils, the slope decreased, with ψleaf-x rapidly and nonlinearly decreasing for moderate increases in E. The ψleaf-x measured in pressurized and unpressurized plants matched well, which indicates that the shoot hydraulic conductance did not decrease during soil drying and that the decrease in Ksp is caused by a decrease in soil-root conductance. The decrease of E matched well the onset of hydraulic nonlinearity. Our findings demonstrate that stomatal closure prevents the drop in ψleaf-x caused by a decrease in Ksp and elucidate a strong correlation between stomatal regulation and belowground hydraulic limitation.

Highlights

What triggers stomatal closure in plants during soil drying? Water flow across the soil–plant atmosphere continuum is controlled by leaf area, stomatal conductance and atmospheric demand
Transpiration (E [cm3/s]) causes a decrease in the leaf xylem water potential that propagates through the xylem vessels down to the roots and the soil. ψleaf-x depends on the soil water potential, transpiration rate and the hydraulic conductivities of the elements composing the soil–plant system
The linearity is explained by the fact that in wet soils, the plant hydraulic conductance is constant and lower than that of the soil, thereby controlling the water flow

Summary

| INTRODUCTION

What triggers stomatal closure in plants during soil drying? Water flow across the soil–plant atmosphere continuum is controlled by leaf area, stomatal conductance ( gs [mol m−2 s−1]) and atmospheric demand (vapor pressure deficit, VPD [kPa]). Using a meta-analysis across species, they showed that the loss of Ks, more than the xylem, coincides better with the stomatal closure They visualized the relationship between E, ψleaf-x and ψ soil as a surface E(ψ leaf-x,ψsoil) and hypothesized that stomatal regulation prevents plants to cross the onset of hydraulic nonlinearity. Below-ground conductances are not affected by pressurization, including the potential shrinkage of the root cortex and the loss of contact to the soil This method evaluates accurately the changes in below-ground hydraulic conductance occurring at a given E and ψsoil (Carminati et al, 2017; Passioura, 1980). By comparing pressurized and non-pressurized experiments, we tested the hypothesis that stomata close at the onset of hydraulic limitation We applied this method to tomato plants in a sandy-loam soil. The data were interpreted using the conceptual and numerical soil– plant hydraulic model of Carminati and Javaux (2020)

| MATERIALS AND METHODS

| RESULTS

| DISCUSSION