Towards a unified theory of plant photosynthesis and hydraulics

Abstract

<p>Increasing frequencies and intensities of droughts are projected for many regions of the Earth. Water stress leads to a decline in the gross primary productivity (GPP) of plants. Plant responses to water stress vary with timescale, and plants adapted to different environments differ in their responses. Here, we present a unified theory of plant photosynthesis and plant hydraulics, which explains a wide range of observed plant responses to developing water stress.</p><p>Our theory is based on the least-cost hypothesis of Prentice et al. (2014). By integrating plant hydraulics into the least-cost framework, we attempt to improve upon the model of GPP by Wang et al. (2017), which accurately predicts the responses of global GPP to temperature, elevation, and vapour pressure deficit, but overestimates GPP under water-stressed conditions. Our model has three key ingredients. (1) The aforementioned least-cost framework, in which optimal stomatal conductance minimizes the summed costs of maintaining transpiration, the photosynthetic machinery, and the hydraulic pathways, including the potential costs of repairing embolized xylem. We also test a closely related maximum-benefit framework, in which optimal stomatal conductance maximizes the net benefit from assimilation while accounting for these summed costs, and obtain comparable results. (2) A trait-dependent model of water flow through the plant stem, in which water flow is limited by the conductivity (K<sub>s</sub>) and embolism resistance (P<sub>50</sub>) of the hydraulic pathway. At the shortest timescale, water stress causes stomatal closure to an extent that the transpiration demand determined by the vapour pressure deficit at the leaf surface is matched by the water supply through the stem. (3) A short-term response of photosynthetic capacity (V<sub>cmax</sub>) to soil moisture, through which the potential V<sub>cmax</sub> acclimates to prevailing daytime conditions to equalize carboxylation-limited and electron-transport-limited photosynthesis rates (A<sub>c</sub> and A<sub>j</sub>), while the realized values of V<sub>cmax</sub>, A<sub>c</sub>, and A<sub>j</sub> are reduced from their potential values by a factor dependent on the leaf water potential and the leaf embolism resistance.</p><p>We estimate the parameters of our model using published data from short-term and long-term dry-down experiments. The key predictions of our model are as follows: (1) GPP declines with decreasing soil water potential and drops to zero soon after the soil water potential crosses P<sub>50</sub>; (2) soil-to-leaf water potential difference remains relatively constant under developing water stress; (3) functional forms describing the declines in stomatal conductance, V<sub>cmax</sub>, and GPP with soil water potential are consistent with observations; and (4) decreased photosynthetic capacity (V<sub>cmax</sub>) recovers (in the long term) if the plant increases its Huber value (e.g., by shedding leaves), increases its conductivity (e.g., by growing wider new vessels), or decreases its height growth (e.g., by reducing allocation to growth). Our theory provides a potential way of integrating trait-based responses of plants to water stress into global vegetation models, and should therefore help to improve predictions of the global carbon and water cycles in a changing environment.</p><p>