Stomatal control as a driver of plant evolution.

Stomata are the pores on a leaf surface through which plants regulate the uptake of carbon dioxide (CO2) for photosynthesis against the loss of water via transpiration. Turgor changes in the guard cells determine the area of stomatal pore through which gaseous diffusion can occur, thus maintaining a constant internal environment within the leaf (Gregory et al., 1950). Stomata first occurred in the fossil record ;400 million years ago (Ma), and are largely identical in form to the stomatal complexes of many extant plants, illustrating their effectiveness and importance to terrestrial plants (Edwards et al., 1998). Stomatal control is critical to a plant’s adaptation to its environment; it is this fundamental importance that has led to a wealth of stomatal research ranging in scale from biomolecular analysis to landscape processes (e.g. Gedney et al., 2006; Hu et al., 2010). The first issue of Journal of Experimental Botany, published 60 years ago, contained four papers relating to stomatal function. These included an analysis by Heath of the effects of atmospheric CO2 concentration ([CO2]) on stomatal aperture and conductance; an area of research that is increasingly relevant to our understanding of the past and prediction of future vegetation responses to atmospheric composition. Heath (1950) was the first to observe that reductions in [CO2] below ambient levels induced stomatal opening, an ecophysiological response of great interest, and that the site of CO2 sensing was most probably in the substomatal cavity and not the guard cells. Stomatal research has become vastly important to crop production, biodiversity responses, and hydrology (particularly in terms of ‘run-off’) with respect to rising atmospheric [CO2], changing water regimes, and growing populations. As our understanding of stomatal physiology develops, the role of stomata in the evolution of terrestrial vegetation and development of the terrestrial landscape and atmospheric composition is becoming increasingly evident, alongside the use of fossil stomata as palaeo-proxies of past atmospheres (e.g. McElwain et al., 2004; Berry et al., 2010; Smith et al., 2010). The stomatal control responses of plants consist of ‘shortterm’ stomatal aperture changes in response to availability of water, light, temperature, wind speed, and carbon dioxide, and also ‘longer term’ changes in stomatal density that set the limits for maximum stomatal conductance in response to atmospheric [CO2], light intensity/quality, and root-to-shoot signals of water availability (Schoch et al., 1980, 1984; Davies et al., 2000; Casson et al., 2009). Stomatal control determines the water use efficiency (WUE) of a plant by optimizing water lost against carbon gained. Additionally, the stomatal control mechanisms employed by a plant species will determine: the risk of xylem embolism by reducing the probability of cavitation through stomatal closure during episodes of high transpirative demand (Brodribb and Jordan, 2008; Meinzer et al., 2009); leaf temperature and resistance to heat stress (Srivastava et al., 1995; Jones et al., 2002); tolerance of toxic atmospheric gases (Mansfield and Majernik, 1970); nutrient uptake via promotion of root mass flow (Van Vuuren et al., 1997); and the maximum rate of photosynthesis (Körner et al., 1979). Those plant species with more effective stomatal control will be expected to be more successful than those with less effective stomatal control. However, not all plant species, or individuals within a species, possess equally effective stomatal control, in the setting of either stomatal numbers or the regulation of stomatal aperture (i.e. speed and ‘tightness’ of closure). Given that any trait that confers a selective advantage is likely to become universal within a population (McNeilly, 1968), it may be reasonable to assume that stomatal control incurs certain ‘costs’, and that these costs have played a significant role in plant evolution over the last 400 million years. The origination of major plant groups, and morphological advances such as the development of planate leaves, coincide with periods of ‘low’ atmospheric [CO2] (Fig. 1) (Woodward, 1998; Beerling et al., 2001). The reduced availability of the substrate for photosynthesis is predicted to be compensated by increases in the carboxylation efficiency of RubisCO and enhanced stomatal conductance to maintain CO2 uptake during periods of low [CO2] (Woodward, 1998; Franks and Beerling, 2009). This elevated stomatal conductance incurs higher rates of water loss and associated risks of desiccation and xylem embolism, in addition to the metabolic costs of enhanced construction of stomatal complexes. It is these costs during periods of low [CO2] that may serve as evolutionary tipping points, where species with more efficient and effective stomata and hydraulic systems are favoured (Robinson, 1994; Brodribb