Soil-plant hydraulics explain the stomatal efficiency-safety tradeoff

Authors: CAI, GAOCHAO - University Of Bayreuth; CARMINATI, ANDREA - Eth Zurich; Gleason, Sean; JAVAUX, MATHIEU - University Of Louvain; AHMED, MUTEZ - University Of California, Davis

Submitted to: Plant, Cell & Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/6/2023
Publication Date: 1/6/2023
Citation: Cai, G., Carminati, A., Gleason, S.M., Javaux, M., Ahmed, M. 2023. Soil-plant hydraulics explain the stomatal efficiency-safety tradeoff. Plant, Cell & Environment. https://doi.org/10.1111/pce.14536.
DOI: https://doi.org/10.1111/pce.14536

Interpretive Summary: It has recently been reported that plants exhibiting high rates of gas exchange (water vapor and CO2) "wind back" their stomatal conductance, and therefore water loss from their leaves, earlier than plants with lower rates of gas exchange. We used a recently developed soil-plant hydraulic model (Carminati-Javaux model) to try and explain this pattern across species. We found that plants with high rates of gas exchange encounter a precipitous decline in soil conductivity, which occurs so rapidly that plant stomata may not have sufficient time to respond. As such, it appears that natural and artificial selection may favor individuals that exhibit high rates of gas exchange but also early stomatal closure to avoid permanent damage to the water-transporting tissues. Our results further demonstrate that water delivery to the sites of evaporation in crop plants depend critically on the conductance of water through soil as well as at the soil-root interface, thus reducing the relative importance of plant xylem conductive capacity at soil water potentials below ca -0.5MPa. This suggests that programs aimed to improve crop performance under limited water should focus on traits maximizing soil-root conductance and conservative stomatal closure (closure at higher water potential), rather than higher xylem conductance.

Technical Abstract: The efficiency-safety tradeoff has been intensively investigated in plants, especially in relation to their capacity to transport water and prevent embolism. Recently, a stomatal efficiency-safety tradeoff was found that plants with higher maximum stomatal conductance showed a greater sensitivity to stomatal closure during soil drying. However, the underlying mechanism of such a tradeoff remains elusive. Here, we utilized a soil-plant hydraulic model, in which stomatal closure is triggered by nonlinearity in soil-plant hydraulics, to explain the stomatal efficiency-safety tradeoff. We found that the tradeoff was impacted by plant hydraulic properties, such as plant hydraulic conductance, active root length, and resistance to xylem embolism (P50). Our analysis of the tradeoff suggested that plants may adjust growth or hydraulic properties to adapt to water limitations.