Towards a unified theory of plant photosynthesis and hydraulics

Abstract

The global carbon and water cycles are strongly governed by the simultaneous diffusion of CO2 and water vapour through the leaves of terrestrial plants. These diffusive fluxes are controlled by plants’ adaptations to balance carbon gains and hydraulic risks. We introduce a trait-based optimality theory that unifies the treatment of stomatal responses and biochemical acclimation of plants to changing environments. Tested with experimental data from eighteen species, our model successfully predicts the simultaneous decline in carbon assimilation rate, stomatal conductance, and photosynthetic capacity during progressive soil drought. It also correctly predicts the dependencies of gas exchange on atmospheric vapour pressure deficit, temperature, and CO2. Consistent with widely observed patterns, inferred trait values for the analysed species display a spectrum of stomatal strategies, a safety-efficiency trade-off, and a convergence towards low hydraulic safety margins. Our unifying theory opens new avenues for reliably modelling the interactive effects of drying soil and air and rising atmospheric CO2 on global photosynthesis and transpiration.

Coordination of plant hydraulic and photosynthetic traits: confronting optimality theory with field measurements

“…Leaves with low LMA tend to display a larger leaf area to fix carbon within a relatively short leaf life span. In addition, high hydraulic conductivity at both leaf and stem levels ensures that large amounts of water can be transported to leaves for transpiration, to maintain open stomata and a high rate of CO 2 uptake (Mencuccini et al ., 2019b ; Joshi et al ., 2020 ). This relationship between hydraulics and LMA may also be associated with physiological characteristics.…”

“…Ó 2021 The Authors New Phytologist Ó 2021 New Phytologist Foundation New Phytologist (2021) 232: 1286-1296 www.newphytologist.com the weak trade-off between Ψ tlp and K S in deciduous species and the apparent absence of these trade-offs in evergreen species imply that low hydraulic safety does not accompany high K S . Although the xylem tension at which 50% of the maximum conductivity is lost (P 50 ) is the most commonly used index of hydraulic safety, we used Ψ tlp for this purpose, noting that the two measures are significantly correlated (Zhu et al, 2018;Joshi et al, 2020). Globally, a weak trade-off between hydraulic safety and efficiency has been reported (Gleason et al, 2016), and new work suggests a tight trade-off between efficiency and safety may be a feature of climates with highly seasonal precipitation (Liu et al, 2021).…”

Eco‐evolutionary optimality as a means to improve vegetation and land‐surface models

“…However, further research is needed to determine how soil influences might best be included in models. Solutions are likely to include EEO approaches to explain the coordination of hydraulic and photosynthetic traits (Brodribb, 2009; Deans et al ., 2020; Joshi et al ., 2020), and the influence of soil fertility factors on water and nutrient acquisition costs (Paillassa et al ., 2020).…”

Plant hydraulics coordinated with photosynthetic traits and climate

“…However, the weak trade-off between π tlp and K S implies that low hydraulic safety does not always accompany high K S . Although the xylem tension at which 50% of the maximum conductivity is lost ( P 50 ) is the most commonly used index of hydraulic safety, we used π tlp for this purpose, noting that the two measures are strongly correlated 6,30 . Globally, a weak trade-off between hydraulic safety and efficiency has been reported 31 , although new work suggests a tight trade-off between efficiency and safety may be a feature of climates with highly seasonal precipitation 32 .…”

“…Leaves with low LMA tend to display a larger leaf area to fix carbon within a relatively short leaf life span. Meanwhile, high hydraulic conductance at both leaf and stem levels ensures that large amount of water can be transported to leaves for transpiration, in order to maintain open stomata and a high rate of CO 2 uptake 8,30 . This relationship between hydraulics and LMA may also be associated with physiological characteristics.…”