Systems analysis of guard cell oscillatory mechanics in stomatal dynamics

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Stomata in the epidermis of plant leaves play a vital role in regulating CO2 exchange for photosynthesis while minimising transpirational water loss between the inner leaf air space and the atmosphere. Guard cells surrounding the stomata take up inorganic solutes and water, increasing in volume to open the stomatal pore when CO2 in the leaf is depleted; and they lose solutes and water, decreasing in volume to close the stomatal pore and conserve leaf water under stress, in the dark and when CO2 is high. We know a great deal about the mechanisms that drive stomatal movements between the extremes in pore aperture. By contrast, our knowledge is remarkably poor of the mechanisms that give rise to the dynamic continuum of apertures normally observed in the field, much less how such fine-tuning is regulated. This gap in knowledge can be seen, for example, in the focus of past efforts in quantitative modelling. Stomatal characteristics underpin models for transpiration and plant water use efficiency that have proven successful in reproducing and predicting transpirational behaviours at the plant and community levels. However all of these models reflect a 'top-down' approach and consider guard cell mechanics as a 'black box', subsuming these processes within a few empirical parameters, hydraulic pathways and conductances. There are very few models that have been developed 'bottom-up' from the properties of the guard cells themselves, despite the wealth of knowledge we have for guard cell transport and signalling, and none that are sufficiently generalised to be widely applicable in predicting stomatal behaviour. A further complication is that much of our knowledge at the cellular level is based on in vitro studies with guard cells in epidermal peels or isolated as protoplasts. We need to bridge these gaps in our knowledge and to understand how stomata compensate dynamically in the face of real environmental challenges. Studies over the past 15 years have yielded several important clues to the mechanisms behind stomatal dynamics. The clues point to oscillations of the guard cell membrane between two quasi-stable states that control and balance osmotic fluxes. This postulate finds support in well-documented observations that stomatal apertures also oscillate and can be driven experimentally under defined conditions. Indeed, such a 'time-averaging' mechanism has already been predicted from a systems analysis of guard cell ion transport, albeit using a mathematical model with significant parameter limitations. These several lines of evidence need now to be drawn together and subject to rigorous experimental testing in order to address a number of key issues. We need to know whether more comprehensive mathematical models for guard cell transport / incorporating, for example, known regulatory properties for the major ion transporters / are able to return the full range of observed behaviours in aperture and voltage, and to predict novel ones. We want to know how these behaviours are underpinned by the dynamics of guard cell ion fluxes and osmotic contents. Finally, we want to test whether experimental manipulations of the relevant guard cell parameters can be shown to yield well-defined and predictable changes in stomatal behaviour. We propose here to develop this line of enquiry jointly through systems kinetic modelling to derive quantitative and testable predictions and through experimental analysis and validation. Our knowledge of guard cell transport and homeostasis is now sufficiently well-developed to make an approach of this kind a readily achievable goal. We fully expect answers to the questions we pose to yield new and exciting insights into the behaviour of stomata and to open entirely new dimensions to practical applications in agriculture and crop development.