Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves

Abstract

Stomatal responsiveness to vapour pressure deficit (VPD) results in continuous regulation of daytime gas-exchange directly influencing leaf water status and carbon gain. Current models can reasonably predict steady-state stomatal conductance (gs ) to changes in VPD but the gs dynamics between steady-states are poorly known. Here, we used a diverse sample of conifers and ferns to show that leaf hydraulic architecture, in particular leaf capacitance, has a major role in determining the gs response time to perturbations in VPD. By using simultaneous measurements of liquid and vapour fluxes into and out of leaves, the in situ fluctuations in leaf water balance were calculated and appeared to be closely tracked by changes in gs thus supporting a passive model of stomatal control. Indeed, good agreement was found between observed and predicted gs when using a hydropassive model based on hydraulic traits. We contend that a simple passive hydraulic control of stomata in response to changes in leaf water status provides for efficient stomatal responses to VPD in ferns and conifers, leading to closure rates as fast or faster than those seen in most angiosperms.

Evolution of the Stomatal Regulation of Plant Water Content

“…Such a linkage means that guard cells lose turgor as leaf water potential declines, passively closing the pore and dramatically reducing evaporation ). This extremely simple means of stomatal closure in response to declining leaf water status requires no metabolic input or complex signaling intermediates and is well described in lycophytes and ferns (Lange et al, 1971;Lösch, 1977Lösch, , 1979Brodribb and McAdam, 2011;Martins et al, 2016). Stomatal responses to changes in vapor pressure deficit (or the humidity of the air) are thus highly predictable in these early vascular plants based on a passive model that links leaf turgor with guard cell turgor Martins et al, 2016).…”

“…This extremely simple means of stomatal closure in response to declining leaf water status requires no metabolic input or complex signaling intermediates and is well described in lycophytes and ferns (Lange et al, 1971;Lösch, 1977Lösch, , 1979Brodribb and McAdam, 2011;Martins et al, 2016). Stomatal responses to changes in vapor pressure deficit (or the humidity of the air) are thus highly predictable in these early vascular plants based on a passive model that links leaf turgor with guard cell turgor Martins et al, 2016). However, there is an important prerequisite for this passive mechanism to function correctly in these basal species: a minimal influence of epidermal cell mechanics on stomatal aperture, meaning that only guard cell turgor influences the aperture of the pore (Franks and Farquhar, 2007).…”

An Integrated Hydraulic-Hormonal Model of Conifer Stomata Predicts Water Stress Dynamics

“…Modeling stomatal movements on the basis of ion fluxes into and out of guard cells will provide the ultimate mechanistic basis for changing aperture, and although Hills et al (2012) developed a model of stomatal movement based on known ion channel behavior from electrophysiological studies, the intention of their model at this stage is not to predict leaf-level stomatal behavior. In light of recent developments, modeling the effect of ABA on stomatal conductance needs re-evaluation.Dynamic stomatal responses to changes in plant water status are well described by a passive hydraulic model in ferns and lycophytes due to ABA insensitivity (Brodribb and McAdam, 2011;Martins et al, 2016), and in gymnosperms over short intervals of water stress due to a limited influence of ABA, which is synthesized slowly in conifers (McAdam and Brodribb, 2014). However, over longer periods of water stress, the synthesis of ABA leads to an uncoupling of stomatal conductance from bulk water potential in gymnosperms (McAdam and Brodribb, 2014).…”

“…Despite apparently similar functional demands on stomatal evolution, not all lineages employ the same mechanism of controlling water loss, but rather show a directional shift from passive hydraulic control in ferns and lycophytes to active metabolic control mediated by the phytohormone abscisic acid (ABA) in angiosperms (Brodribb and McAdam, 2011;McAdam and Brodribb, 2014). Phylogenetically midway between the ferns and angiosperms are the gymnosperms, which appear to employ passive hydraulic control for short-term perturbations in leaf water status, in common with earlier lineages, but are also capable of switching to ABAmediated control following extended water stress (Brodribb and McAdam, 2013;McAdam and Brodribb, 2014;Martins et al, 2016).The proposed evolutionary trajectory from simple to more complex mechanisms of stomatal control of leaf water status may provide a useful framework for the general modeling of stomatal control, starting from passive hydraulic models in ferns and lycophytes, with the end goal of modeling stomatal control in angiosperms where both hydraulics and metabolism are important (Buckley et al, 2003;Brodribb and McAdam, 2011). Of the many hydraulic models proposed (e.g.…”

“…Despite apparently similar functional demands on stomatal evolution, not all lineages employ the same mechanism of controlling water loss, but rather show a directional shift from passive hydraulic control in ferns and lycophytes to active metabolic control mediated by the phytohormone abscisic acid (ABA) in angiosperms (Brodribb and McAdam, 2011;McAdam and Brodribb, 2014). Phylogenetically midway between the ferns and angiosperms are the gymnosperms, which appear to employ passive hydraulic control for short-term perturbations in leaf water status, in common with earlier lineages, but are also capable of switching to ABAmediated control following extended water stress (Brodribb and McAdam, 2013;McAdam and Brodribb, 2014;Martins et al, 2016).…”