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ABSTRACT Stomata control plant water loss and photosynthetic carbon gain. Developing more generalized and accurate stomatal models is essential for earth system models and predicting responses under novel environmental conditions associated with global change. Plant optimality theories offer one promising approach, but most such theories assume that stomatal conductance maximizes photosynthetic net carbon assimilation subject to some cost orconstraintof water. We move beyond this approach by developing a new, generalized optimality theory of stomatal conductance, optimizing any non‐foliar proxy that requires water and carbon reserves, like growth, survival, and reproduction. We overcome two prior limitations. First, we reconcile the computational efficiency ofinstantaneousoptimization with a more biologically meaningfuldynamic feedbackoptimization over plant lifespans. Second, we incorporatenon‐steady‐statephysics in the optimization to account for the temporal changes in the water, carbon, and energy storage within a plant and its environment that occur over the timescales that stomata act, contrary to previous theories. Our optimal stomatal conductance compares well to observations from seedlings, saplings, and mature trees from field and greenhouse experiments. Our model predicts predispositions to mortality during the 2018 European drought and captures realistic responses to environmental cues, including the partial alleviation of heat stress by evaporative cooling and the negative effect of accumulating foliar soluble carbohydrates, promoting closure under elevated CO2. We advance stomatal optimality theory by incorporating generalized evolutionary fitness proxies and enhance its utility without compromising its realism, offering promise for future models to more realistically and accurately predict global carbon and water fluxes.
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Dynamically optimizing stomatal conductance for maximum turgor-driven growth over diel and seasonal cycles
Abstract Stomata have recently been theorized to have evolved strategies that maximize turgor-driven growth over plants’ lifetimes, finding support through steady-state solutions in which gas exchange, carbohydrate storage and growth have all reached equilibrium. However, plants do not operate near steady state as plant responses and environmental forcings vary diurnally and seasonally. It remains unclear how gas exchange, carbohydrate storage and growth should be dynamically coordinated for stomata to maximize growth. We simulated the gas exchange, carbohydrate storage and growth that dynamically maximize growth diurnally and annually. Additionally, we test whether the growth-optimization hypothesis explains nocturnal stomatal opening, particularly through diel changes in temperature, carbohydrate storage and demand. Year-long dynamic simulations captured realistic diurnal and seasonal patterns in gas exchange as well as realistic seasonal patterns in carbohydrate storage and growth, improving upon unrealistic carbohydrate responses in steady-state simulations. Diurnal patterns of carbohydrate storage and growth in day-long simulations were hindered by faulty modelling assumptions of cyclic carbohydrate storage over an individual day and synchronization of the expansive and hardening phases of growth, respectively. The growth-optimization hypothesis cannot currently explain nocturnal stomatal opening unless employing corrective ‘fitness factors’ or reframing the theory in a probabilistic manner, in which stomata adopt an inaccurate statistical ‘memory’ of night-time temperature. The growth-optimization hypothesis suggests that diurnal and seasonal patterns of stomatal conductance are driven by a dynamic carbon-use strategy that seeks to maintain homeostasis of carbohydrate reserves.
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- Award ID(s):
- 2045610
- PAR ID:
- 10465663
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- AoB PLANTS
- Volume:
- 15
- Issue:
- 5
- ISSN:
- 2041-2851
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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