Do stomata optimize turgor‐driven growth? A new framework for integrating stomata response with whole‐plant hydraulics and carbon balance

Abstract

Summary Every existing optimal stomatal model uses photosynthetic carbon assimilation as a proxy for plant evolutionary fitness. However, assimilation and growth are often decoupled, making assimilation less ideal for representing fitness when optimizing stomatal conductance to water vapor and carbon dioxide. Instead, growth should be considered a closer proxy for fitness. We hypothesize stomata have evolved to maximize turgor‐driven growth, instead of assimilation, over entire plants' lifetimes, improving their abilities to compete and reproduce. We develop a stomata model that dynamically maximizes whole‐stem growth following principles from turgor‐driven growth models. Stomata open to assimilate carbohydrates that supply growth and osmotically generate turgor, while stomata close to prevent losses of turgor and growth due to negative water potentials. In steady state, the growth optimization model captures realistic stomatal, growth, and carbohydrate responses to environmental cues, reconciles conflicting interpretations within existing stomatal optimization theories, and explains patterns of carbohydrate storage and xylem conductance observed during and after drought. Our growth optimization hypothesis introduces a new paradigm for stomatal optimization models, elevates the role of whole‐plant carbon use and carbon storage in stomatal functioning, and has the potential to simultaneously predict gross productivity, net productivity, and plant mortality through a single, consistent modeling framework.

Is carbon, not water, the resource that limits stomatal opening?

“…(a) Predictions from the theory by Cowan & Farquhar (1977) for optimal stomatal conductance ( g s ) can be considered a ‘baseline’, against which (b) temporal variation in the marginal carbon profit of water (∂ A /∂ E ) predicted by the model of Potkay and Feng in this issue of New Phytologist (2023; pp. 506–528) leads to (c) different predictions for stomatal conductance in the Potkay and Feng (PF) model.…”

“…(2020), (c) the least‐cost idea of Prentice et al . (2014), and (d) the growth‐maximization approach of Potkay and Feng as described in this issue of New Phytologist (2023; pp. 506–528) – accounts for a different subset of factors in the network of influences linking physiological state variables and processes.…”

“…Yet, consensus about the true ‘goal’ of stomatal behavior has eluded ecophysiologists, leaving a profusion of divergent models. The most recent model, published by Potkay & Feng in this issue of New Phytologist (2023; pp. 506–528), takes a novel tack that may help resolve a quandary at the heart of stomatal optimization theory.

‘…this model's success in synthesizing many distinct facets of whole plant physiology into a coherent theory’

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Daytime stomatal regulation in mature temperate trees prioritizes stem rehydration at night

“…tree water deficit; Zweifel et al ., 2016) and restore turgor pressure within the stem's cambium tissue at night (Steppe et al ., 2015; Zweifel et al ., 2021; Etzold et al ., 2022). However, depending on both the species‐specific root‐water supply and the sapwood anatomical architecture (Peters et al ., 2021b), increased predawn tree water deficit (TWD pd ) during drought can cause sustained low turgor pressure during the night (Zweifel et al ., 2016; Salomón et al ., 2022) and force stricter stomatal regulation to avoid further dehydration and turgor loss (Potkay & Feng, 2022). Although responses of TWD pd to drought can be utilized to test whether species exhibit weaker predawn rehydration, we lack evidence, showing that mature trees indeed reduce G c to prioritize predawn stem rehydration (Fig.…”

“…1b, H2). As such, it remains unclear whether the species‐specific G c control is tuned to sustain turgor (for growth) or avoid branch embolism formation while maximizing carbon assimilation at the cost of turgor loss in the phloem and cambial zone (McDowell et al ., 2008; Kannenberg et al ., 2019; Mantova et al ., 2021; Potkay & Feng, 2022).…”