Small Pores with a Big Impact.

The guard cells surrounding stomatal pores of leaves are, at once, the best characterized and some of the most intriguing of cells in the plant kingdom. There are, of course, some very basic reasons for our interest in stomatal guard cells. The stomatal pore connects the inner air space of the leaf with the atmosphere, providing a route for gaseous exchange that bypasses the otherwise impermeable cuticle on the outer epidermal surface of land plants. Vascular plants regulate the pore aperture in response to an array of environmental and endogenous stimuli. Stomata thus play a critical role in enabling CO2 entry to the leaf for photosynthesis while protecting the hydrated environment needed by the photosynthetic tissues within. Stomata have a major influence on global water and carbon cycles, and they lie at the center of the crisis in water availability and crop production now expected to unfold over the next 20 to 30 years. Just how big an impact can such small pores have? As an example, we note that incorporating stomatal transpiration was a key factor behind much of the advance in atmospheric modeling of the 1990s, enabling weather prediction with the hour-by-hour precision that we recognize today. This Focus Issue on Stomata is the first dedicated to the evolution, development, and physiology of guard cells, their fundamental relevance to plants and to society. Several reviews and articles in this Focus Issue center around stomata as a target for genetic engineering to improve water use efficiency and their importance for crop survival. The Update reviews of Vialet-Chabrand et al. (2017b) and Matthews et al. (2017) address the potential for improved water use efficiencies by enhancing the kinetics of guard cell responses to environmental cues relevant for photosynthesis. Hughes et al. (2017) demonstrate the efficacy of manipulating stomatal densities to enhance water use efficiency and drought tolerance, while Hochberg et al. (2017) highlight the interplay between stomatal function, water delivery to the leaf, and leaf shedding in the field. Guard cells attract much attention also as models for understanding evolution, development, and cellular physiology. At the heart of all biological research is a quest for understanding how life arises from what is more than the sum of its parts, in other words a search for what emerges from synergistic interactions between the respective components that underpin the biological process. The reviews and articles of this Focus Issue are testament to this, more fundamental interest in the guard cells, and they repeatedly highlight the emergent characteristics of life. The quest for these synergies—the nonlinearities within the biological mechanisms—is a theme that runs through research into stomatal guard cells at many levels. Such nonlinearities are certainly evident in evolution. Stomata first appeared as simple pores on the surfaces of early land plants, evident in fossilized remains. These pores probably served to speed the desiccation of reproductive structures by contrast with the functions of stomata in vascular plants today. When did stomata evolve to moderate water loss? How did they acquire the molecular machinery that drives stomatal movements? And when was the complex network of signal cascades assembled to sensitize stomatal dynamics to environmental, hormonal, and pathogenic stimuli? The Update review by Franks et al. (2017) revisits these questions across temporal and spatial scales. Brodribb and McAdam (2017) highlight a selection of evolutionary boundaries and transitions in relation to signaling by the hormone abscisic acid. These boundaries remain open to debate, as noted by Hõrak et al. (2017) and by Cai et al. (2017). The questions surface again in the context of Crassulacean acid metabolism stomata in the Update review by Males and Griffiths (2017) and in theCorrespondence from Bräutigam et al. (2017). McElwain and Steinthorsdottir (2017) as well as Renzaglia et al. (2017) approach these questions also from the perspective of fossil records. Renewed interest in the topic is certain to throw up new insights in the coming years. Guard cells arise from the surrounding epidermal pavement cells as the leaf expands. Here, too, they present a model for cellular organization and differentiation that incorporates a wealth of nonlinearities, beginning with the asymmetry in cell division that gives rise to the guard mother cell. We dedicate this Focus Issue to the memory of Fred Sack (Bergmann et al., 2017), whose pioneering studies of mutants in stomatal development, as well as his infectious humor and generosity, formed the cornerstone of much research that has followed over the past two decades. The Update review by Chater et al. (2017) touches on some of themost recent developments on this topic. As an example of how this knowledge may be applied, again we point the reader to the research article by Hughes et al. (2017). de Marcos et al. (2017) uncover an unexpected interaction between brassinosteroid signaling and transcriptional control behind cell fates leading to stomatal development. Related articles that bridge the gap between the development of the stomatal cell wall and stomatal function (Huang et al., 2017; Hunt et al., 2017) will also be of interest in this context. Of course, guard cells are widely recognized as the premier plant cell model for studies of membrane transport, signaling, and cellular homeostasis. Ion transport across the plasma membrane and tonoplast of the guard cell, and thewater flux that follows, generates the turgor to drive guard cell volume and, hence, changes in www.plantphysiol.org/cgi/doi/10.1104/pp.17.00642