Abstract

Stomata, the microvalves on leaf surfaces, exert major influences across scales, from plant growth and productivity to global carbon and water cycling. Stomatal opening enables leaf photosynthesis, and plant growth and water use, whereas plant survival of drought depends on stomatal closure. Here we report that stomatal function is constrained by a safety-efficiency trade-off, such that species with greater stomatal conductance under high water availability (gmax) show greater sensitivity to closure during leaf dehydration, i.e., a higher leaf water potential at which stomatal conductance is reduced by 50% (Ψgs50). The gmax - Ψgs50 trade-off and its mechanistic basis is supported by experiments on leaves of California woody species, and in analyses of previous studies of the responses of diverse flowering plant species around the world. Linking the two fundamental key roles of stomata—the enabling of gas exchange, and the first defense against drought—this trade-off constrains the rates of water use and the drought sensitivity of leaves, with potential impacts on ecosystems.

Highlights

  • Stomata, the microvalves on leaf surfaces, exert major influences across scales, from plant growth and productivity to global carbon and water cycling

  • The decline of gs with decreasing Ψleaf is important among the complex of internal and external factors that determine overall stomatal responses, including root-derived signals, ambient irradiance and CO29–11 and influences the dynamics of gas exchange and productivity and drought tolerance across plant species[1,12,13,14,15]

  • A well-known hypothesis in whole plant physiology is a constraint on internal water transport known as the hydraulic safety-efficiency trade-off: an association across species between high values for the maximum stem or leaf hydraulic conductivity and a greater sensitivity to decline during dehydration[19,20,21]

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Summary

Introduction

The microvalves on leaf surfaces, exert major influences across scales, from plant growth and productivity to global carbon and water cycling. One potentially general constraint on the response of gs to Ψleaf would be a trade-off between high maximum stomatal conductance (gmax) in hydrated leaves and greater sensitivity to closure during dehydration, i.e., a higher Ψleaf at 50% loss of stomatal conductance (Ψgs[50]). Such trade-offs between “safety” and “efficiency”, or, similar in logic, between “stress tolerance” and “potential growth” are common in plant and animal biology[16,17] and industrial systems[18]. Smaller stomata have a greater surface area to volume ratio, facilitating ion exchange and stronger and faster movements in response to changing irradiance and leaf hydration status[26,27,28]

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