The control of stomata by water balance

It is clear that stomata play a critical role in regulating water loss from terrestrial vegetation. What is not clear is how this regulation is achieved. Stomata appear to respond to perturbations of many aspects of the soil-plant-atmosphere hydraulic continuum, but there is little agreement regarding the mechanism (or mechanisms) by which stomata sense such perturbations. This review discusses feedback and feedforward mechanisms by which hydraulic perturbations are putatively transduced into stomatal movements, in relation to generic empirical features of those responses. It is argued that a metabolically mediated feedback response of stomatal guard cells to the water status in their immediate vicinity ('hydro-active local feedback') remains the best explanation for many well-known features of hydraulically related stomatal behaviour, such as transient 'wrong-way' responses and the equivalence of hydraulic supply and demand as stomatal effectors. Furthermore, many curious phenomena that appear inconsistent with feedback, such as 'apparent feedforward' humidity responses and 'isohydric' behaviour (water potential homeostasis), are in fact expected to emerge from the juxtaposition of hydro-active local feedback and the well-known hysteretic and threshold-like effect of water potential on xylem hydraulic resistance.     

Control of the Co2 Responses of Stomata by Indol-3ylacetic Acid and Abscisic Acid

Previous studies of stomatal behaviour on detached epidermisof Commelina communis L. have suggested that abscisic acid (ABA)and C02 act independently to cause stomatal closure. Evidenceis presented here that if indol-3ylacetic acid (IAA) is addedto the medium used for incubating the epidermis, an interactionbetween ABA and Co₂ becomes apparent. Increasing concentrationsof IAA reduce the ability of the stomata to respond to CO₂,and ABA appears to antagonize this effect. Recognition of therole of IAA enables us to reconcile earlier conflicting reportsconcerning the interdependence of effects of ABA and Co₂on stomata.     

Hydraulic and chemical signalling in the control of stomatal conductance and transpiration.

Abscisic acid (ABA) transported in the xylem from root to shoot and perceived at the guard cell is now widely studied as an essential regulating factor in stomatal closure under drought stress. This provides the plant with a stomatal response mechanism in which water potential is perceived in the root as an indication of soil water status and available water resources. There is also ample evidence that stomata respond directly to some component of leaf water status. This provides additional information about water potential gradients developing between root and shoot as the result of water transport, allowing for a more stable regulation of shoot water status and better protection of the transport system itself. The precise location at which leaf water status is sensed, however, and the molecular events transducing this signal into a guard cell response are not yet known. Major questions therefore remain unanswered on how water stress signals perceived at root and leaf locations are integrated at the guard cell to control stomatal behaviour.     

Opinion: The red-light response of stomatal movement is sensed by the redox state of the photosynthetic electron transport chain

Guard cells regulate CO₂ uptake and water loss of a leaf by controlling stomatal movement in response to environmental factors such as CO₂, humidity, and light. The mechanisms by which stomata respond to red light are actively debated in the literature, and even after decades of research it is still controversial whether stomatal movement is related to photosynthesis or not. This review summarizes the current knowledge of the red-light response of stomata. A comparison of published evidence suggests that stomatal movement is controlled by the redox state of photosynthetic electron transport chain components, in particular the redox state of plastoquinone. Potential consequences for the modeling of stomatal conductance are discussed.     

Stomatal responses to non-local changes in PFD: evidence for long-distance hydraulic interactions

Interactions among stomata within a single areole have recently been reported, and evidence suggests that hydraulic mechanisms may be responsible for these interactions. Such interactions may play a role in patchy stomatal behaviour by coordinating stomatal behaviour within areoles. However, models suggest that longer‐distance interactions may be required to produce the large‐scale discoordination that is characteristic of stomatal patchiness. This study was undertaken to characterize long‐distance interactions between ‘artificial patches’ of stomata under varying conditions of evaporative demand and soil water stress. Gas‐exchange was monitored in two adjacent regions (‘patches’) of a wheat leaf by two independent gas mixing and analysis systems. When photon flux density (PFD) was changed in only one of these patches, stomatal conductance responded in both patches in a manner consistent with hydraulic interactions propagated by changes in xylem water potential. These data are discussed in the context of mechanisms for patchy stomatal conductance and implications for the design and analysis of gas‐exchange experiments.     

Do Stomata Respond to CO(2) Concentrations Other than Intercellular?

Most studies on stomatal responses to CO₂ assume that guard cells respond only to intercellular CO₂ concentration and are insensitive to the CO₂ concentrations in the pore and outside the leaf. If stomata are sensitive to the CO₂ concentration at the surface of the leaf or in the stomatal pore, the stomatal response to intercellular CO₂ concentration will be incorrect for a `normally' operating leaf (where ambient CO₂ concentration is a constant). In this study asymmetric CO₂ concentrations for the two surfaces of amphistomatous leaves were used to vary intercellular and leaf surface CO₂ concentrations independently in Xanthium strumarium L. and Helianthus annuus L. The response of stomata to intercellular CO₂ concentration when the concentration at the leaf surface was held constant was found to be the same as the response when the surface concentration was varied. In addition, stomata did not respond to changes in leaf surface CO₂ concentration when the intercellular concentration for that surface was held constant. It is concluded that stomata respond to intercellular CO₂ concentration and are insensitive to the CO₂ concentration at the surface of the leaf and in the stomatal pore.     

The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells

The stomata of the fern Adiantum capillus-veneris lack a blue light-specific opening response but open in response to red light. We investigated this light response of Adiantum stomata and found that the light wavelength dependence of stomatal opening matched that of photosynthesis. The simultaneous application of red (2 micromol m(-2) s(-1)) and far-red (50 micromol m(-2) s(-1)) light synergistically induced stomatal opening, but application of only one of these wavelengths was ineffective. Adiantum stomata did not respond to CO2 in the dark; the stomata neither opened under a low intercellular CO2 concentration nor closed under high intercellular CO2 concentration. Stomata in Arabidopsis (Arabidopsis thaliana), which were used as a control, showed clear sensitivity to CO2. In Adiantum, stomatal conductance showed much higher light sensitivity when the light was applied to the lower leaf surface, where stomata exist, than when it was applied to the upper surface. This suggests that guard cells likely sensed the light required for stomatal opening. In the epidermal fragments, red light induced both stomatal opening and K+ accumulation in guard cells, and both of these responses were inhibited by a photosynthetic inhibitor, 3-(3,4-dichlorophenyl)-1,1-dimethylurea. The stomatal opening was completely inhibited by CsCl, a K+ channel blocker. In intact fern leaves, red light-induced stomatal opening was also suppressed by 3-(3,4-dichlorophenyl)-1,1-dimethylurea. These results indicate that Adiantum stomata lack sensitivity to CO2 in the dark and that stomatal opening is driven by photosynthetic electron transport in guard cell chloroplasts, probably via K+ uptake.     

Stomatal response characteristics of Tradescantia virginiana grown at high relative air humidity

Plants produced at high relative air humidity (RH) show poor control of water loss after transferring to low RH, a phenomenon which is thought to be due to their stomatal behaviour. The stomatal anatomy and responses of moderate (55%) and high (90%) RH grown Tradescantia virginiana plants to treatments that normally induce stomatal closure, i.e. desiccation, abscisic acid (ABA) application and exposure to darkness were studied using attached or detached young, fully expanded leaves. Compared with plants grown at moderate RH the transpiration rate, stomatal conductance and aperture of high RH grown plants measured at the same condition (40% RH) were, respectively, 112, 139 and 132% in light and 141, 188 and 370% in darkness. Besides the differences in stomatal size (guard cell length was 56.7 and 73.3 µm for moderate and high RH grown plants, respectively), there was a clear difference in stomatal behaviour. The stomata responded to desiccation, ABA and darkness in both moderate and high RH grown plants, but the high variability of stomatal closure in high RH grown plants was striking. Some stomata developed at high RH closed in response to darkness or to a decrease in relative water content to the same extent as did stomata from moderate RH grown plants, whereas others closed only partly or did not close at all. Evidently, some as yet unidentified physiological or anatomical changes during development disrupt the normal functioning of some stomata in leaves grown at high RH. The failure of some stomata to close fully in response to ABA suggests that ABA deficiency was not responsible for the lack of stomatal closure in response to desiccation.     

Fern and lycophyte guard cells do not respond to endogenous abscisic acid

Stomatal guard cells regulate plant photosynthesis and transpiration. Central to the control of seed plant stomatal movement is the phytohormone abscisic acid (ABA); however, differences in the sensitivity of guard cells to this ubiquitous chemical have been reported across land plant lineages. Using a phylogenetic approach to investigate guard cell control, we examined the diversity of stomatal responses to endogenous ABA and leaf water potential during water stress. We show that although all species respond similarly to leaf water deficit in terms of enhanced levels of ABA and closed stomata, the function of fern and lycophyte stomata diverged strongly from seed plant species upon rehydration. When instantaneously rehydrated from a water-stressed state, fern and lycophyte stomata rapidly reopened to predrought levels despite the high levels of endogenous ABA in the leaf. In seed plants under the same conditions, high levels of ABA in the leaf prevented rapid reopening of stomata. We conclude that endogenous ABA synthesized by ferns and lycophytes plays little role in the regulation of transpiration, with stomata passively responsive to leaf water potential. These results support a gradualistic model of stomatal control evolution, offering opportunities for molecular and guard cell biochemical studies to gain further insights into stomatal control.     

Stomatal sensing of the environment

The effects of environmental factors on stomatal behaviour are reviewed and the questions of whether photosynthesis and transpiration eontrol stomata or whether stomata themselves control the rates of these processes is addressed. Light affects stomata directly and indirectly. Light can act directly as an energy source resulting in ATP formation within guard cells via photophosphorylation, or as a stimulus as in the case of the blue light effects which cause guard cell H⁺ extrusion. Light also acts indirectly on stomata by affecting photosynthesis which influences the intercellular leaf CO₂ concentration ( C _i). Carbon dioxide concentrations in contact with the plasma membrane of the guard cell or within the guard cell acts directly on cell processes responsible for stomatal movements. The mechanism by which CO₂ exerts its effect is not fully understood but, at least in part, it is concerned with changing the properties of guard cell plasma membranes which influence ion transport processes. The C _i may remain fairly constant for much of the day for many species which is the result of parallel responses of stomata and photosynthesis to light. Leaf water potential also influences stomatal behaviour. Since leaf water potential is a resultant of water uptake and storage by the plant and transpirational water loss, any factor which affects these processes, such as soil water availability, temperature, atmospheric humidity and air movement, may indirectly affect stomata. Some of these factors, such as temperature and possibly humidity, may affect stomata directly. These direct and indirect effects of environmental factors interact to give a net opening response upon which is superimposed a direct effect of stomatal circadian rhythmic activity.     

Gas valves,forests and global change: a commentary on Jarvis (1976) ‘The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field’

Microscopic turgor-operated gas valves on leaf surfaces—stomata—facilitate gas exchange between the plant and the atmosphere, and respond to multiple environmental and endogenous cues. Collectively, stomatal activities affect everything from the productivity of forests, grasslands and crops to biophysical feedbacks between land surface vegetation and climate. In 1976, plant physiologist Paul Jarvis reported an empirical model describing stomatal responses to key environmental and plant conditions that predicted the flux of water vapour from leaves into the surrounding atmosphere. Subsequent theoretical advances, building on this earlier approach, established the current paradigm for capturing the physiological behaviour of stomata that became incorporated into sophisticated models of land carbon cycling. However, these models struggle to accurately predict observed trends in the physiological responses of Northern Hemisphere forests to recent atmospheric CO₂ increases, highlighting the need for improved representation of the role of stomata in regulating forest–climate interactions. Bridging this gap between observations and theory as atmospheric CO₂ rises and climate change accelerates creates challenging opportunities for the next generation of physiologists to advance planetary ecology and climate science. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society.     

Reversal by green light of blue light-stimulated stomatal opening in intact, attached leaves of Arabidopsis operates only in the potassium-dependent, morning phase of movement

Green light reversal of blue light-stimulated stomatal opening was discovered in isolated stomata. The present study shows that the response also occurs in stomata from intact leaves. Arabidopsis thaliana plants were grown in a growth chamber under blue, red and green light. Removal of the green light opened the stomata and restoration of green light closed them to baseline values under experimental conditions that rule out a mesophyll-mediated effect. Assessment of the response to green light over a daily time course showed that the stomatal sensitivity to green light was observed only in the morning, which coincided with the use of potassium as a guard cell osmoticum. Sensitivity to green light was absent during the afternoon phase of stomatal movement, which was previously shown to be dominated by sucrose osmoregulation in Vicia faba. Hence, the shift away from potassium-based osmoregulation in guard cells is further postulated to entail a shift from blue light to photosynthesis as the primary component of the stomatal response to light. Stomata from intact leaves of the zeaxanthin-less, npq1 mutant of Arabidopsis failed to respond to the removal or restoration of green light in the growth chamber, or to short, high fluence pulses of blue or green light. These data confirm previous studies showing that npq1 stomata are devoid of a specific blue light response. In contrast, stomata from intact leaves of phot1 phot2 double mutant plants had a reduced but readily detectable response to the removal of green light and to blue and green pulses.     

Effects of humidity on light-induced stomatal opening: evidence for hydraulic coupling among stomata

A mechanism for co-ordinating behaviour of stomata within an areole during patchy stomatal conductance has recently been proposed. This mechanism depends on hydraulic interactions among stomata that are mediated by transpiration-induced changes in epidermal turgor. One testable prediction that arises from this proposed mechanism is that the strength of hydraulic coupling among stomata should be proportional to evaporative demand and, therefore, inversely proportional to humidity. When a leaf is illuminated following a period of darkness, there is typically a period of time, termed the Spannungsphase, during which guard cell osmotic and turgor pressure are increasing, but the pore remains closed. If hydraulic coupling is proportional to evaporative demand, then variation among stomata in the duration of the Spannungsphase should be lower for leaves at low humidity than for leaves at high humidity. A similar prediction emerged from a computer model based on the proposed hydraulic mechanisms. These predictions were tested by measuring individual stomatal apertures on intact transpiring leaves at low and high humidity and on vacuum-infiltrated leaf pieces (to eliminate transpiration) as PFD was increased to high values from either darkness or a low value. Results showed that the range of Spannungsphasenamong stomata was reduced at low humidity compared to high humidities. Experiments that began at low PFD, rather than at darkness, showed no delay in stomatal opening. These results are discussed in the context of the proposed hydraulic coupling mechanisms.     

Active chloride transport in the leaf epidermis of Commelina communis in relation to stomatal activity

Summary A chloride selective micro-electrode has been used to determine vacuolar chloride concentrations in individual cells of the leaf epidermis of Commelina communis. When the stomata were open a gradient in chloride concentration across the stomatal complex was observed with the highest concentration in the guard cells. On stomatal closure the chloride gradient was reversed. Calculation of the driving forces on chloride indicated that active transport of chloride was occurring during both stomatal opening and closure. This transport appeared to be energetically independent of the transport of potassium. These results are discussed in relation to the behaviour of other anions during stomatal movements.     

Woody plants optimise stomatal behaviour relative to hydraulic risk

Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage. Using data from 34 species that span global forest biomes, we find that the recent carbon‐maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency. Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle.     

根系分区灌溉和水分利用效率

根系分区灌溉是指仅仅部分根系受到正常的灌溉,其余根系则受到人为的干旱,两项理论根据指出这种措施可减少植物的水分肖耗,并保持一定的生物产量,其一是植物蒸腾失水与气孔导性是线性关系,而光合作用与气孔导性则是一种渐趋饱和的关系,如果气孔导性从最大值适应调低,可显著降低蒸腾,但对光合影响应小得多,其二是处于干燥土壤中的根系可感觉干旱,产生干旱信号来调节地上部分的气孔开度,显然,这项措施在田间有多大效用值得深入研究。 先是大田作物的蒸腾失水仅部分地受气孔控制,界面层的扩散阻力起很大作用。因此该措施可能对界面层阻力较小的,如果树等作用大些,另外,根系干旱信号可否“长期”地产生和调控气孔仍需试验证明。     

A globule-like structure in leaf epidermis and its relation to stomatal regulation inCassia auriculata L.

The role of a globule-like structure in the leaf epidermal cells ofC. auriculata has been studied in relation to stomatal regulation. Water stress and direct sunlight promote the appearance of globules at the same time as the stomata close. Ample water supply and shade inhibit the appearance of globules and the stomata open. The number of stomata is the same on either leaf surface, but their behaviour is different because of different exposure to light.     

Guard cell photosynthesis is critical for stomatal turgor production,yet does not directly mediate CO2‐ and ABA‐induced stomatal closing

Stomata mediate gas exchange between the inter‐cellular spaces of leaves and the atmosphere. CO₂ levels in leaves (Ci) are determined by respiration, photosynthesis, stomatal conductance and atmospheric [CO₂]. [CO₂] in leaves mediates stomatal movements. The role of guard cell photosynthesis in stomatal conductance responses is a matter of debate, and genetic approaches are needed. We have generated transgenic Arabidopsis plants that are chlorophyll‐deficient in guard cells only, expressing a constitutively active chlorophyllase in a guard cell specific enhancer trap line. Our data show that more than 90% of guard cells were chlorophyll‐deficient. Interestingly, approximately 45% of stomata had an unusual, previously not‐described, morphology of thin‐shaped chlorophyll‐less stomata. Nevertheless, stomatal size, stomatal index, plant morphology, and whole‐leaf photosynthetic parameters (PSII, qP, qN, F_V′/F_M′) were comparable with wild‐type plants. Time‐resolved intact leaf gas‐exchange analyses showed a reduction in stomatal conductance and CO₂‐assimilation rates of the transgenic plants. Normalization of CO₂ responses showed that stomata of transgenic plants respond to [CO₂] shifts. Detailed stomatal aperture measurements of normal kidney‐shaped stomata, which lack chlorophyll, showed stomatal closing responses to [CO₂] elevation and abscisic acid (ABA), while thin‐shaped stomata were continuously closed. Our present findings show that stomatal movement responses to [CO₂] and ABA are functional in guard cells that lack chlorophyll. These data suggest that guard cell CO₂ and ABA signal transduction are not directly modulated by guard cell photosynthesis/electron transport. Moreover, the finding that chlorophyll‐less stomata cause a ‘deflated’ thin‐shaped phenotype, suggests that photosynthesis in guard cells is critical for energization and guard cell turgor production.     

Comparative Epidermal Ultrastructure of Cotton (Gossypium hirsutum L.) Leaf, Bract and Capsule Wall

Cotton leaves are more physiologically active than the bractand the capsule wall of the fruiting structures. To elucidatethe disparities in their physiological behaviour, epidermalcell density, stomatal index, stomatal size, trichome densityand type, and epicuticular wax ultrastructure of cotton leaf,bract and capsule wall were delineated using scanning electronmicroscopy (SEM). The epidermal cells of the outer periclinalwalls on both surfaces of the leaf and bract were raised andconvex. Conversely, the capsule wall epidermal cells were polygonalwith flat outer periclinal walls. The stomatal complex in theleaf and bract was paracytic, whereas in the capsule wall thestomatal complex was anomocytic. The adaxial and abaxial stomataof the leaf were coplanar to the epidermal surface, as opposedto the raised adaxial stomata on the bract. On the contrary,the stomata on the capsule wall surface appeared to be slightlysunken. Furthermore, the capsule wall stomata were larger thanthe stomata on either surface of both the leaf and the bract.The stomatal index was greater on the abaxial surfaces of theleaf and the bract (18.4 and 9.4, respectively) than their correspondingadaxial surfaces (14.4 and 4.7, respectively). Leaves had thehighest stomatal index followed by the bract and the capsulewall. The indumentum consisted of glandular and nonglandulartrichomes, the density of which was greater on the abaxial surfacesthan on the adaxial surfaces of the leaf and bract. The capsulewall indumentum lacked nonglandular trichomes. Epicuticularwax occurred in the form of striations. However, the striationpattern varied among the organs. This study clearly illustratesmorphological disparities in the epidermal features of leaf,bract and capsule wall, helping to explain their physiologicaldivergence. Copyright 2000 Annals of Botany Company Gossypium hirsutum, epicuticular wax, raised stomata, scanning electron microscopy, stomatal index, trichomes     

环境因素变化对冬小麦气孔阻力的影响

本文据同步观测到的气孔阻力和土壤水势、净辐射能、气温、叶温、水汽压、饱和差、风速等环境因素变化值,用统计方法分析了小麦叶片气孔阻力与环境因素的关系,结果表明：冬小麦叶片的气孔导性主要受土壤水势影响。叶片正反两面的气孔对环境因素变化的反应不同,正面气孔导性主要受土壤水势影响,而反面气孔导性则与气温、水汽压和饱和差关系较大。