Transpiration response to atmospheric drying vs. to soil drying: underlying physical and physiological mechanisms and related plant traits

Plant water use during drought depends on atmospheric demand and soil water supply. Typically, transpiration response to drought is evaluated in two types of experiments: either exposure to a stepwise increase in vapor pressure deficit (VPD), or exposure to soil drying over the course of weeks. Surprisingly however, the extent of similarities and differences of the underlying mechanisms remains poorly documented. This hampers progress towards breeding for well-adapted crops targeting environments with high VPD, high risk of soil moisture deficit, or both. We present an extensive review of the two experimental approaches and use a soil-plant hydraulic model to simulate transpiration responses to both environmental drivers. Existing experimental results lead to contradicting results regarding the role of the plant hydraulic conductance for the transpiration response to atmospheric drying vs. to soil drying: a high plant hydraulic conductance triggers an earlier transpiration decline (i.e. in wetter soil conditions) during soil drying; but enables plants to sustain transpiration at high VPD. A hydraulic framework hypothesizing that transpiration responds to a decline in soil-plant conductance helps to explain the contradiction. At high VPD, water potential gradients mainly develop within the plant, and thus it is the plant hydraulic conductance that limits the water flow during atmospheric drying. During soil drying, the gradients develop in the soil, and thus the soil hydraulic conductivity controls the flow. The plant hydraulic conductance is expected to impact the plant’s sensitivity to the development of water potential gradients around the roots that occurs during soil drying. Thus, stomatal closure and hence transpiration response is related to a drop in hydraulic conductivities in both scenarios but the relevant hydraulic traits differ between the two environmental changes in a predictable way. Such a finding could better guide breeding efforts targeting adaptation to specific drought regimes.