Focus on Water

Water covers over 70% of the surface of Earth and is generally recognized as a renewable resource. Yet, however counterintuitive, the availability of fresh water limits plant growth over much of the land mass of the planet and poses major challenges for human society as a whole. For land plants, including crop species, fresh water is a basic requirement for life. Water is a common trigger for seed germination. Its uptake from the soil facilitates inorganic mineral nutrition, and its flux through vascular tissues of the plant circulates minerals and organic nutrients throughout the plant. Water (and solute) retention determines turgor, driving plant cell expansion and contributing to plant form and function, including stomatal movements. Finally, water loss by transpiration from the stomata of leaves is, at once, a by-product of gas exchange and CO₂ uptake for photosynthesis and a driver for water flux and its circulation throughout the plant. In turn, plants exert major controls on the water and carbon cycles of the world. Roughly 32 × 10¹⁵ kg year⁻¹ of water is drawn by land plants and transpired to the atmosphere, while terrestrial photosynthesis annually fixes about 120 × 10¹⁵ g of carbon (Schimel et al., 2001). Stomatal transpiration by plants is speculated to have made a significant contribution to recent changes in continental runoff and freshwater availability associated with the global rise in CO₂ (Gedney et al., 2006), although it must be weighed against the consequences of other human activities, especially land use (Piao et al., 2007).

Agricultural water usage accounts for some 70% of all human water consumption. It should come as no surprise, therefore, that water availability is at the center of a crisis in food production that is expected to unfold over the next 20 to 30 years (UNESCO, 2009). At present, international trade in virtual water (i.e. water associated with the production of commodities of all kinds) is closely tied to the agricultural import and export markets of each regional economy (Hoekstra and Mekonnen, 2012). Such analysis highlights vast, and often counterintuitive, disparities in water use and distribution worldwide, explaining why a relatively water-rich island like the United Kingdom is a net importer of water while the water-poor Australian continent is a net exporter of water. Globally, records and best estimates indicate that agricultural water use has risen more than 6-fold in the past 100 years, primarily as a result of demand for irrigation and twice as fast as the human population. It is projected to double again before 2030. In the Plains states of the United States, irrigation has drawn down the soil water table by 150 m and more in some areas over the past 50 years. Even in the United Kingdom, the use of irrigation has risen almost 10-fold in the past 30 years, and this trend is expected to continue. Clearly, the situation is not sustainable. The economic, political, and social issues are complex, but nonetheless they are inextricably tied to the demand for water by crop plants.

Within this Focus Issue is much thought to the scope for improving water use efficiency and plant productivity through bioengineering, in its simplest formulation addressing the question of how to increase the amount of carbon fixed per unit of water lost via transpiration from a crop. As key gatekeepers of water flux through the plant, stomatal guard cells figure highly here. The opening Topical Review of Lawson and Blatt (2014) explores the rapidity of stomatal responses, its hysteresis in relation to photosynthetic demand for CO₂ under temporal variations in natural light, and the consequences for water use by plants. The authors consider the potential for improvements through the physical as well as physiological characteristics of stomatal guard cells, and they conclude that manipulating transport and metabolism is just as, if not more likely, to yield benefits in water use efficiency. Even so, engineering enhanced stomatal function implies a knowledge of appropriate molecular targets. As Wang et al. (2014) note in the companion article, the complex network of transport and metabolism in guard cells that drives stomatal movements presents a formidable barrier to targeted genetic engineering. Wang et al. (2014) make use of quantitative systems modeling using the OnGuard platform (Chen et al., 2012; Hills et al., 2012) to assess the potential for accelerating stomatal movements by systematically manipulating guard cell transport in silico. Their analysis suggests that altering the populations of individual transporters, such as might be achieved through genetic suppression and overexpression, is likely to have unforeseen consequences. Instead, they highlight channel gating as a promising target for experimental manipulation.

Guard cell physiology has long been inextricably linked with drought and the hormone abscisic acid (ABA), which, under water stress, triggers stomata to close. Although 25 years of research have given us a great depth of knowledge about the mechanics of ABA signaling in isolated guard cells, our understanding of ABA signaling in vivo is far from complete. In this issue, Kuromori et al. (2014) address the origins of ABA within vascular tissue, demonstrating in phloem companion cells the expression of the ABA biosynthetic enzymes ABA2 and AAO3 and a putative ABA efflux transporter, AtABCG25. They also show that enhanced ABA synthesis in this tissue promoted stomatal closure. Seiler et al. (2014) made use of senescent and stay-green lines of barley (Hordeum vulgare) together with drought-induced expression of 9-cis-epoxycarotenoid dioxygenase that leads to ABA synthesis and with silencing of ABA 8′-hydroxylase to the curtail of ABA degradation. Their studies underline the importance of temporal changes in ABA to long-term assimilation in the crop. By contrast, in the conifer Metasequoia glyptostroboides, an evolutionarily intermediate in land plant phylogeny, McAdam and Brodribb (2014) report that hydraulic controls on stomata take precedence within the diurnal cycle. They report that ABA-mediated stomatal closure occurred late under drought stress and was additive with the hydraulic signal. Additionally, two articles focus on reactive oxygen species (ROS), which have attracted much attention as ABA-associated signaling intermediates. The research of Watkins et al. (2014) underlines the effects of secondary metabolism and flavonol accumulation in tempering the stomatal response to ABA by scavenging ROS intermediates. Noctor et al. (2014) review the broader context of ROS and oxidative stress, considering both as signals and, generally, as consequences of drought stress, and they highlight potential drought-responsive, redox-associated genes and metabolite pathways.

Water flux through the plant is subject to other physical and physiological constraints, independent of stomata. The Update review by Rockwell et al. (2014a) focuses on the xylem, the physical processes of cavitation, and how plants recover from embolisms within vascular structures. Chaumont and Tyerman (2014) review the rapidly growing literature on aquaporins, focusing on how these water channels are regulated at the molecular and cellular levels and how they affect water permeability through the sequential layers of tissue from root epidermis through the stele to the xylem and, in the leaf, between the xylem, mesophyll, and epidermal cell layers. The authors highlight the substantial temporal variations in root and leaf hydraulic conductivity imposed by aquaporins, pointing to their roles in coordinating water supply with demand throughout the plant. These themes recur in research articles from Mayr et al. (2014) and Secchi and Zwieniecki (2014). The first of these articles presents correlative studies of embolism in Norway spruce (picea abies) imposed by winter freezing and drought. Mayr et al. (2014) observed embolism refilling in the late winter associated with increased aquaporin expression in the phloem and endodermis at a time when water was still unavailable from the roots. Their results suggest that refilling draws on foliar water uptake and enhanced symplastic water conductance in advance of the start of the growing season. Secchi and Zwieniecki (2014) adopted a genetic strategy to show that embolism and its recovery is connected to the expression of the aquaporin PIP1 in Populus spp. The results also connect genetically the propensity for embolism with stomatal regulation.

Hydraulic conductivity, and its association with aquaporins, almost certainly enters into questions of the site(s) of water evaporation and hydration within the leaf, and it is pertinent on a macroscopic scale to water balance under stress and during expansive growth. In another article, Rockwell et al. (2014b) explore where evaporation occurs, whether close to the leaf xylem or adjacent to the substomatal cavity, developing an analytical model of water flux that incorporates nonisothermal coupling for transport. The model indicates a range of distributions between perivascular and peristomatal evaporation and characteristic to the leaf architecture. Scoffoni et al. (2014) explore the feedback and connection between leaf hydraulic conductance, turgor loss, and leaf shrinkage in different species and show that the process plays a role in hydraulic decline during mild dehydration. Caldeira et al. (2014) close the circle, reporting on model and experimental analysis of leaf growth with diurnal water flux and transpiration. Their studies are consistent with a significant role in leaf expansion of a source-sink balance between aquaporin expression and hydraulic conductance of the root, on the one hand, and of stomatal transpiration from the leaf, on the other. Two other articles will be of interest in these contexts. Wada et al. (2014) revisit water permeation across epidermal cells in Tradescantia virginiana and report a polarity to water transport that is potentially a consequence of aquaporins; Born et al. (2014) offer an advance on the method of terahertz time-domain spectroscopy, more common to materials science, that will enable noninvasive measurements of water status in plant tissues with potential for a semi-high-throughput system.

Aspects of plant development as it relates to plant hydraulic relations and growth under water deficits are featured in two Update reviews. The review by Tardieu et al. (2014) starts with observations that expansive growth under water deficit shows substantial genetic variability, higher than that of photosynthesis, and that quantitative trait loci associated with responses to soil water deficit and to evaporative demand show substantial overlaps. They propose a source-sink relationship between photosynthetic carbon fixation and hydraulically linked expansive growth, discussing its implications for modeling of growth under water deficit and for the design of breeding programs. Lobet et al. (2014) review plant water uptake at the soil interface, with a focus on root architecture and its significance for soil water extraction. In separate articles, Maruyama et al. (2014) report a comparative analysis of metabolites, hormones, and transcripts in rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana) under cold and water stress and Wudick et al. (2014) identify two vacuolar aquaporins specific to Arabidopsis pollen and report on their impact on pollen growth and fertility. Finally, with the review by Amezaga et al. (2014), this Focus Issue examines the potential for future access to new water resources. The review takes a different perspective on questions of hydraulic relations in plant biology, exploring synthetic biological solutions for desalination. Key to these ideas is the use of photosynthetic organisms, such as cyanobacteria, to energize salt transport and sequestration, effectively generating biological ion exchangers to produce fresh water.

We are grateful to all of the authors for their excellent manuscripts and for working under tight deadlines. We also thank the cohort of anonymous reviewers who cheerfully accepted the burden of reviewing a very large number of manuscripts within the short time frame of the call for this issue.

Glossary

ABA

abscisic acid

ROS

reactive oxygen species