Dynamically optimizing stomatal conductance for maximum turgor-driven growth over diel and seasonal cycles

Aaron Potkay; Xue Feng

doi:10.1093/aobpla/plad044

Dynamically optimizing stomatal conductance for maximum turgor-driven growth over diel and seasonal cycles

AoB Plants. 2023 Jul 6;15(5):plad044. doi: 10.1093/aobpla/plad044. eCollection 2023 Oct.

Authors

Aaron Potkay^{1

2}, Xue Feng^{1

2}

Affiliations

¹ Department of Civil, Environmental, and Geo-Engineering, University of Minnesota, Twin Cities, 500 Pillsbury Drive S.E., Minneapolis, MN 55455, USA.
² Saint Anthony Falls Laboratory, University of Minnesota, Twin Cities, 23rd Ave SE, Minneapolis, MN 55414, USA.

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.

Keywords: Dynamic optimality; non-structural carbohydrates; source-sink dynamics; stomatal optimization; tree growth; tree hydraulics; turgor-driven expansion.

Publication types

Review