Observed and modelled stomatal responses to dynamic light environments in the shade plant Alocasia macrorrhiza

Abstract

Dynamic responses of stomatal conductance to lightflecks (15 s to 5 min) were observed in the tropical understory plant Alocasia macrorrhiza.Brief observations were also made on step changes in light, flashing light and short low-light periods (darkflecks) after stomata had reached steady state conductances in high light. Stotnata opened substantially even in response to very short lightflecks, with maximal opening being reached about 20 min after the end of the lightfleck. These responses are compared to those of a semi-mechanistic stomatal model consisting of three steps in series: a biochemical signal which responds directly to light, producing osmolic changes within the guard cells which, in turn, drive the movement of water into the guard cells. The rate of change of each component was assumed to be given by the difference between the current state of that component and the state of the previous component in the series divided by a characteristic time constant for each step. This model allowed excellent description of observed responses to lightflecks, including the fleck-length dependence of stomatal opening, the lag between the end of the lightfleck and the time of maximal stomatal conductance and the response to tnultiple flecks. However, agreement with predicted responses to flashing light and darkflecks was poor. Good agreement could be restored by using dilTerent titne Abbreviations: A = Net CO, assimilation rate; c, = mole Traction of COj at the leal" surface; g, = stomatal conductance; g,,f,,,,i, = steady-state conductance in flashing light; g».iri»/r ~ Steady-State conductance in high light; g,.i,,w = steadystate contkictancc in low light; h, = relative humidity at the leaf surface; I = photon llux density; L = lightfleck length; S = initial bioehemical signal in the guard eells; S^,, = equilibrium value of S at different photon llux densities; S,,,,,, = extrapolated minimum of S^.j, in darkness; S,,,, = the light dependent variable part of S^^; 1 = time; w = guard cell water content; a = initial slope of S^,, as a function of light; I) = lenn to describe the curvature in the light dependence of S,,,,; n = guard cell osmotic potential; r,,, T,, t^, T^ = time constants for decrease and increase of S, and changes in 71 and w. constants for the initial biochemical step, suggesting that the speed of the initial biochemical response is not constant but dependent on the current physiological state of the stomata. For leaves experiencing predotninantly low light, punctuated by relatively short and infrequent periods of high light, this model allows good description of the dynamic changes in stomatal conductance.

Stomatal Size, Speed, and Responsiveness Impact on Photosynthesis and Water Use Efficiency

“…However, such steady-state situations are rarely observed in nature (Jones, 1994) or in isolation (Lawson and Morison, 2004). Few studies have examined the dynamics of stomatal response and photosynthetic output in the face of environmental perturbations (Grantz and Zeiger, 1986;Knapp and Smith, 1987;Kirschbaum et al, 1988;Tinoco-Ojanguren and Pearcy, 1993;Barradas et al, 1994;Lawson et al, 2010;Wong et al, 2012;McAusland et al, 2013). The majority of these have concentrated on the impact of sun/shade flecks on carbon gain in understory plants, often without reference to stomata, and even fewer have looked at the impact on crop plants.…”

“…Pearcy and coworkers pioneered research on the impact of sun flecks on carbon gain and stomatal dynamics and dissected the photosynthetic response into several different phases, attributing the initial induction phase, periods of up to 10 min, to biochemical limitations (Barradas and Jones, 1996); induction was followed by a period dominated by stomatal limitation to the photosynthetic maximum; a third phase was identified in which g s remained high, effectively exceeding that needed for maximum assimilation rates under the given light conditions (Kirschbaum et al, 1988;TinocoOjanguren and Pearcy, 1993) and, hence, out of synchrony with A (Lawson et al, 2010). Figure 2 shows an example of g s limiting photosynthesis, post induction, when irradiance was increased during a 2-min sun fleck.…”

“…However, research to date suggests that manipulating stomatal number and size is not necessarily the simplest or best approach, and the idea that manipulating the stomatal response to changing environmental conditions could provide a means to both improve the WUE of plants and, at the same time, increase the integrated photosynthetic carbon gain. Most important, they indicate that the rapidity of the stomatal response influences both daily carbon gain and WUE and that it is essential to consider the dynamics both of closing and opening together (Raschke, 1970;Kirschbaum et al, 1988;Knapp, 1993;Tinoco-Ojanguren and Pearcy, 1993;Cardon et al, 1994;Allen and Pearcy, 2000;Noe and Giersch, 2004;Pearcy and Way, 2012;Smith and Berry, 2013). With these points in mind, guard cell ion transport is an obvious target for exploration with the aim of altering stomatal dynamics and the rates of opening and closing.…”

Photosynthetic Induction State of Leaves in a Soybean Canopy in Relation to Light Regulation of Ribulose-1-5-Bisphosphate Carboxylase and Stomatal Conductance

“…This result can be explained by the faster increase than decrease in initial rubisco activities following increases and decreases in PFD, respectively (13,23). Stomatal conductance can also exhibit a hysteretic response, with a faster opening than closing, especially in response to brief lightflicks (9). As a consequence of these hysteretic responses it is unlikely that induction state, and hence the capacity to utilize sunflecks, can be readily predicted from steady-state measurements.…”

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

“…For short-term changes in plant water status, both inward and outward fluxes of solutes, and hence the net balance of solutes, were assumed constant. The flux of solute into the guard cell was assumed to be proportional to the difference between a target solute concentration in the absence of ABA, set by photosynthetic and metabolic conditions, and the current solute concentration (Kirschbaum et al, 1988;Haefner et al, 1997). The flux of solutes out of the guard cell was assumed to be dependent on the level of ABA in the leaf ([ABA], g g 21 fresh weight) and the solute concentration of ions responsive to ABA in the guard cell, by simple mass action.…”