Summary
The intricate and interconnecting reactions of C3 photosynthesis are often limited by one of two fundamental processes: the conversion of solar energy into chemical energy, or the diffusion ...of CO2 from the atmosphere through the stomata, and ultimately into the chloroplast. In this review, we explore how the contributions of stomatal morphology and distribution can affect photosynthesis, through changes in gaseous exchange. The factors driving this relationship are considered, and recent results from studies investigating the effects of stomatal shape, size, density and patterning on photosynthesis are discussed. We suggest that the interplay between stomatal gaseous exchange and photosynthesis is complex, and that a disconnect often exists between the rates of CO2 diffusion and photosynthetic carbon fixation. The mechanisms that allow for substantial reductions in maximum stomatal conductance without affecting photosynthesis are highly dependent on environmental factors, such as light intensity, and could be exploited to improve crop performance.
Significance Statement
Plant photosynthesis relies on diffusion of CO2 from the atmosphere to the chloroplasts through the stomatal pores. The distribution and morphological characteristics of stomata influence this and are of particular importance when attempting to understand or improve on rates of carbon fixation. Nonetheless, alterations expected to affect stomatal conductance do not always cause corresponding alterations in photosynthetic carbon assimilation. This review explores the factors that are likely to cause this observed disconnect between maximum stomatal conductance and photosynthesis.
Global warming and associated precipitation changes will negatively impact on many agricultural ecosystems. Major food production areas are expected to experience reduced water availability and ...increased frequency of drought over the coming decades. In affected areas, this is expected to reduce the production of important food crops including wheat, rice, and maize. The development of crop varieties able to sustain or improve yields with less water input is, therefore, a priority for crop research. Almost all water used for plant growth is lost to the atmosphere by transpiration through stomatal pores on the leaf epidermis. By altering stomatal pore apertures, plants are able to optimize their CO
uptake for photosynthesis while minimizing water loss. Over longer periods, stomatal development may also be adjusted, with stomatal size and density being adapted to suit the prevailing conditions. Several approaches to improve drought tolerance and water-use efficiency through the modification of stomatal traits have been tested in the model plant
. However, there is surprisingly little known about the stomata of crop species. Here, we review the current understanding of how stomatal number and morphology are involved in regulating water-use efficiency. Moreover, we discuss the potential and limitations of manipulating stomatal development to increase drought tolerance and to reduce water loss in crops as the climate changes.
Stomata are pores in the plant epidermis that control carbon dioxide uptake and water loss. They are major regulators of global carbon and water cycles
1. Several signaling components that regulate ...stomatal development have been characterized. These include a putative secretory peptide EPF1, LRR receptor components TMM and ER, and a peptidase SDD1
2–4. We have identified EPF2, a peptide related to EPF1 that is expressed in proliferating cells of the stomatal lineage, known as meristemoids, and in guard mother cells, the progenitors of stomata. EPF2 expression during leaf development affects stomatal density on the mature leaf. In the absence of EPF2, excessive numbers of cells enter the stomatal lineage and produce numerous small epidermal cells that express stomatal lineage reporter genes, whereas plants overexpressing EPF2 produce virtually no stomata. Results from genetic experiments indicate that EPF2 regulates a different aspect of stomatal development to EPF1 and are consistent with EPF2 acting in a pathway to regulate stomatal density that involves ER and TMM, but not SDD1. We propose that
EPF2 is expressed earlier in leaf development than
EPF1 and is involved in determining the number of cells that enter, and remain in, the stomatal lineage.
Stomatal pores evolved more than 410 million years ago 1, 2 and allowed vascular plants to regulate transpirational water loss during the uptake of CO2 for photosynthesis 3. Here, we show that ...stomata on the sporophytes of the moss Physcomitrella patens 2 respond to environmental signals in a similar way to those of flowering plants 4 and that a homolog of a key signaling component in the vascular plant drought hormone abscisic acid (ABA) response 5 is involved in stomatal control in mosses. Cross-species complementation experiments reveal that the stomatal ABA response of a flowering plant (Arabidopsis thaliana) mutant, lacking the ABA-regulatory protein kinase OPEN STOMATA 1 (OST1) 6, is rescued by substitution with the moss P. patens homolog, PpOST1-1, which evolved more than 400 million years earlier. We further demonstrate through the targeted knockout of the PpOST1-1 gene in P. patens that its role in guard cell closure is conserved, with stomata of mutant mosses exhibiting a significantly attenuated ABA response. Our analyses indicate that core regulatory components involved in guard cell ABA signaling of flowering plants are operational in mosses and likely originated in the last common ancestor of these lineages more than 400 million years ago 7, prior to the evolution of ferns 8, 9.
► Mosses regulate stomatal apertures in a similar way to later-evolving flowering plants ► Moss stomatal apertures respond to light, CO2 concentration, and stress hormone ABA ► An OST1-like ABA signaling kinase is involved in moss stomatal aperture control ► Stomatal ABA signaling originated in a common ancestor more than 400 million years ago
The epidermal patterning factor (EPF) family of secreted signaling peptides regulate the frequency of stomatal development in model dicot and basal land plant species. Here, we identify and ...manipulate the expression of a barley (Hordeum vulgare) ortholog and demonstrate that when overexpressed HvEPF1 limits entry to, and progression through, the stomatal development pathway. Despite substantial reductions in leaf gas exchange, barley plants with significantly reduced stomatal density show no reductions in grain yield. In addition, HvEPF1OE barley lines exhibit significantly enhanced water use efficiency, drought tolerance, and soil water conservation properties. Our results demonstrate the potential of manipulating stomatal frequency for the protection and optimization of cereal crop yields under future drier environments.
Much of humanity relies on rice (Oryza sativa) as a food source, but cultivation is water intensive and the crop is vulnerable to drought and high temperatures. Under climate change, periods of ...reduced water availability and high temperature are expected to become more frequent, leading to detrimental effects on rice yields.
We engineered the high-yielding rice cultivar ‘IR64’ to produce fewer stomata by manipulating the level of a developmental signal. We overexpressed the rice epidermal patterning factor OsEPF1, creating plants with substantially reduced stomatal density and correspondingly low stomatal conductance.
Low stomatal density rice lines were more able to conserve water, using c. 60% of the normal amount between weeks 4 and 5 post germination. When grown at elevated atmospheric CO2, rice plants with low stomatal density were able to maintain their stomatal conductance and survive drought and high temperature (40°C) for longer than control plants. Low stomatal density rice gave equivalent or even improved yields, despite a reduced rate of photosynthesis in some conditions.
Rice plants with fewer stomata are drought tolerant and more conservative in their water use, and they should perform better in the future when climate change is expected to threaten food security.
Stomata play a pivotal role in the regulation of gas exchange in flowering plants and are distributed throughout the aerial epidermis. In leaves, the pattern of stomatal distribution is highly ...variable between species but is regulated by a mechanism that maintains a minimum of one cell spacing between stomata. In Arabidopsis, a number of the genetic components of this mechanism have been identified and include, SDD1, EPF1 and the putative receptors TMM and the ERECTA-gene family. A mitogen-activated protein (MAP) kinase signalling cascade is believed to act downstream of these putative receptors while a number of transcription factors including SPCH, MUTE and FAMA have been identified that control consecutive steps of stomatal development. The environment also has significant effects on stomatal development. In a number of species both light intensity and CO₂ concentrations have been shown to influence the frequency at which stomata develop on leaves. Long-distance signalling mechanisms have been implicated in these environmental responses with the conditions sensed by mature leaves determining the stomatal frequency in developing leaves. Thus, changes in the environment appear to act by modulating the developmental and patterning pathways to determine stomatal frequency.
Wheat is a staple crop, frequently cultivated in water-restricted environments. Improving crop water-use efficiency would be desirable if grain yield can be maintained. We investigated whether a ...decrease in wheat stomatal density via the manipulation of epidermal patterning factor (EPF) gene expression could improve water-use efficiency. Our results show that severe reductions in stomatal density in EPF-overexpressing wheat plants have a detrimental outcome on yields. However, wheat plants with a more moderate reduction in stomatal density (i.e. <50% reduction in stomatal density on leaves prior to tillering) had yields indistinguishable from controls, coupled with an increase in intrinsic water-use efficiency. Yields of these moderately reduced stomatal density plants were also comparable with those of control plants under conditions of drought and elevated CO2. Our data demonstrate that EPF-mediated control of wheat stomatal development follows that observed in other grasses, and we identify the potential of stomatal density as a tool for breeding wheat plants that are better able to withstand water-restricted environments without yield loss.
Nitric oxide (NO) is an important signaling compound in prokaryotes and eukaryotes. In plants, NO regulates critical developmental transitions and stress responses. Here, we identify a mechanism for ...NO sensing that coordinates responses throughout development based on targeted degradation of plant-specific transcriptional regulators, the group VII ethylene response factors (ERFs). We show that the N-end rule pathway of targeted proteolysis targets these proteins for destruction in the presence of NO, and we establish them as critical regulators of diverse NO-regulated processes, including seed germination, stomatal closure, and hypocotyl elongation. Furthermore, we define the molecular mechanism for NO control of germination and crosstalk with abscisic acid (ABA) signaling through ERF-regulated expression of ABSCISIC ACID INSENSITIVE5 (ABI5). Our work demonstrates how NO sensing is integrated across multiple physiological processes by direct modulation of transcription factor stability and identifies group VII ERFs as central hubs for the perception of gaseous signals in plants.
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•We elucidate a general molecular mechanism for nitric oxide sensing in plants•Group VII ERFs act as nitric oxide sensors via the N-end rule pathway•Group VII ERFs are shown to mediate crosstalk between nitric oxide and abscisic acid•The N-end rule regulates nitric oxide homeostasis through group VII ERFs
Gibbs et al. report that NO-dependent degradation of group VII ERF transcription factors by the N-end rule pathway mediates NO sensing and signal transduction, identifying these transcription factors as central hubs for the perception of gaseous signals in plants.
Stomatal opening and closure depends on changes in turgor pressure acting within guard cells to alter cell shape 1. The extent of these shape changes is limited by the mechanical properties of the ...cells, which will be largely dependent on the structure of the cell walls. Although it has long been observed that guard cells are anisotropic due to differential thickening and the orientation of cellulose microfibrils 2, our understanding of the composition of the cell wall that allows them to undergo repeated swelling and deflation remains surprisingly poor. Here, we show that the walls of guard cells are rich in un-esterified pectins. We identify a pectin methylesterase gene, PME6, which is highly expressed in guard cells and required for stomatal function. pme6-1 mutant guard cells have walls enriched in methyl-esterified pectin and show a decreased dynamic range in response to triggers of stomatal opening/closure, including elevated osmoticum, suggesting that abrogation of stomatal function reflects a mechanical change in the guard cell wall. Altered stomatal function leads to increased conductance and evaporative cooling, as well as decreased plant growth. The growth defect of the pme6-1 mutant is rescued by maintaining the plants in elevated CO2, substantiating gas exchange analyses, indicating that the mutant stomata can bestow an improved assimilation rate. Restoration of PME6 rescues guard cell wall pectin methyl-esterification status, stomatal function, and plant growth. Our results establish a link between gene expression in guard cells and their cell wall properties, with a corresponding effect on stomatal function and plant physiology.
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•The guard cell wall is distinguished by a relatively low level of methylated pectin•Increased methyl pectin leads to stomata with a smaller dynamic range of movement•These plants show increased evaporative cooling and decreased growth under drought•Elevated CO2 restores mutant plant growth to normal
Guard cell wall mechanics must play a role in setting the dynamics of stomatal movement. Amsbury et al. show that the degree of pectin methylation in the wall sets the range of cell swelling, with consequences for plant water use and growth being dependent on CO2 level. Stomatal mechanics are likely to influence plant response to climate change.
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