Co-ordination of vapour and liquid phase water transport properties in plants

The pathway for water movement from the soil through plants to the atmosphere can be represented by a series of liquid and vapour phase resistances. Stomatal regulation of vapour phase resistance balances transpiration with the efficiency of water supply to the leaves, avoiding leaf desiccation at one extreme, and unnecessary restriction of carbon dioxide uptake at the other. In addition to maintaining a long-term balance between vapour and liquid phase water transport resistances in plants, stomata are exquisitely sensitive to short-term, dynamic perturbations of liquid water transport. In balancing vapour and liquid phase water transport, stomata do not seem to distinguish among potential sources of variation in the apparent efficiency of delivery of water per guard cell complex. Therefore, an apparent soil-to-leaf hydraulic conductance based on relationships between liquid water fluxes and driving forces in situ seems to be the most versatile for interpretation of stomatal regulatory behaviour that achieves relative homeostasis of leaf water status in intact plants. Components of dynamic variation in apparent hydraulic conductance in intact plants include, exchange of water between the transpiration stream and internal storage compartments via capacitive discharge and recharge, cavitation and its reversal, temperature-induced changes in the viscosity of water, direct effects of xylem sap composition on xylem hydraulic properties, and endogenous and environmentally induced variation in the activity of membrane water channels in the hydraulic pathway. Stomatal responses to humidity must also be considered in interpreting co-ordination of vapour and liquid phase water transport because homeostasis of bulk leaf water status can only be achieved through regulation of the actual transpirational flux. Results of studies conducted with multiple species point to considerable convergence with regard to co-ordination of stomatal and hydraulic properties. Because stomata apparently sense and respond to integrated and dynamic soil-to-leaf water transport properties, studies involving intact plants under both natural and controlled conditions are likely to yield the most useful new insights concerning stomatal co-ordination of transpiration with soil and plant hydraulic properties.     

Stomatal responses to humidity in isolated epidermes

The ability of guard cells to hydrate and dehydrate from the surrounding air was investigated using isolated epidermes of Tradescantia pallida and Vicia faba . Stomata were found to respond to the water vapour pressure on the outside and inside of the epidermis, but the response was more sensitive to the inside vapour pressure, and occurred in the presence or absence of living, turgid epidermal cells. Experiments using helium–oxygen air showed that guard cells hydrated and dehydrated entirely from water vapour, suggesting that there was no significant transfer of water from the epidermal tissue to the guard cells. The stomatal aperture achieved at any given vapour pressure was shown to be consistent with water potential equilibrium between the guard cells and the air near the bottom of the stomatal pore, and water vapour exchange through the external cuticle appeared to be unimportant for the responses. Although stomatal responses to humidity in isolated epidermes are the result of water potential equilibrium between the guard cells and the air near the bottom of the stomatal pore, stomatal responses to humidity in leaves are unlikely to be the result of a similar equilibrium.     

Interpretation of an empirical model for stomatal conductance in terms of guard cell function

An empirical model for stomatal conductance (g), proposed by Leuning (1995, this issue) as a modification of Ball, Woodrow & Berry's (1987) model, is interpreted in terms of a simple, steady-state model of guard cell function. In this model, stomatal aperture is a function of the relative turgor between guard cells and epidermal cells. The correlation between g and leaf surface vapour pressure deficit in Leuning's model is interpreted in terms of stomatal sensing of the transpiration rate, via changes in the gradient of total water potential between guard cells and epidermal cells. The correlation between g, CO₂ assimilation rate and leaf surface CO₂ concentration in Leuning's model is interpreted as a relationship between the corresponding osmotic gradient, irradiance, temperature, intercellular CO₂ concentration and stomatal aperture itself. The explicit relationship between osmotic gradient and stomatal aperture (possibly describing the effect of changes in guard cell volume on the membrane permeability for ion transport) results in a decrease in the transpiration rate in sufficiently dry air. Possible extension of the guard cell model to include stomatal responses to soil water status is discussed.     

The role of peristomatal transpiration in the mechanism of stomatal movement

Abstract. Peristomatal transpiration is defined as the relative high local rate of cuticular water loss from external and internal surfaces around the stomatal pore and its decisive role in the control of stomatal movement is re-emphasized. As the resistance towards changes in air humidity is low in the pore surroundings, the state of turgor is particularly unsteady there. Due to the inherent instability the guard cell 'senses' fluctuations in the supply-demand relationship of water and is thus the control unit proper. The environmental variables (supply and demand) are cross-correlated within the subsidiary cell and the information is transmitted to the guard cell through the water potential gradient between the two cells. A conceptual segregation of a 'humidity response' by 'passive' stomatal movements is rejected.
As ions always accumulate at the most distant point of the liquid path and as this point varies with pore width according to the prevailing water potential gradients, it is felt that the water stream is causing the characteristic pattern of ion distribution within the epidermis. Passive import of ions is attributed to local concentration gradients which are steepened by continuous supply and by water uptake into the guard cell in response to starch hydrolysis. A mechanistic model supplements the discussion.     

The kinetics of stomatal responses to VPD in Vicia faba: electrophysiological and water relations models

Abstract. An Ohm's law analogy is frequently employed to calculate parameters of leaf gas exchange. For example, resistance to water vapour loss is calculated as the quotient of vapour pressure difference (VPD) and vapour loss by transpiration. In the present research, this electrical analogy was extended. Steady-state transpiration as a function of VPD, assayed in leaflets of Vicia faba using gas exchange techniques, was compared with steady-state K⁺ current magnitude as a function of voltage in isolated guard cell protoplasts of Vicia faba, assayed using the patch clamping technique in the whole cell configuration. An electrophysiological model originally developed to explain the kinetics of current changes following step changes in voltage across a cell membrane was used to fit the kinetics of transpiration changes following step changes in VPD applied to leaflets of Vicia faba. Following step increases in VPD, transpiration exhibited an initial increase, reflecting the increased driving force for water loss and, for large step increases in VPD, a transient decrease in stomatal resistance. Transpiration subsequently declined, reflecting stomatal closure. By analogy to electrophysiological responses, it is hypothesized that the humidity parameter that is sensed by guard cells is VPD. Two models based on epidermal water relations were also applied to transpiration kinetics. In the first model, the transient increase in transpiration following a step increase in VPD was attributed partially to an increase in the Physical driving force (VPD) and partially to a transient decrease in stomatal resistance resulting from reduced epidermal backpressure. In the second model, the transient decrease in stomatal resistance was attributed to a direct response of the guard cells to VPD. Both models based on water relations gave good fits of the data, emphasizing the need for further study regarding the metabolic nature of the guard cell response to humidity.     

The Simulation of Leaf Conductance Responses to Changes in Environmental Water Status

A simulation model of stomatal response to change of environmental water status was set up based on the works on the mechanism of stomatal movement. The variations of leaf conductance, water potential and turgot pressure in guard cells, subsidiary cells and the other cells or tissues in leaf with leaf-air vapour pressure difference and soil water potential have been calculated by our model. The calculated results fit very well with the data from experiments. The different patterns of leaf transpiration variation with the difference between leaf-air and vapour pressure can be explained quantitatively.     

A model of stomatal conductance to quantify the relationship between leaf transpiration, microclimate and soil water stress

A model of stomatal conductance was developed to relate plant transpiration rate to photosynthetic active radiation (PAR), vapour pressure deficit and soil water potential. Parameters of the model include sensitivity of osmotic potential of guard cells to photosynthetic active radiation, elastic modulus of guard cell structure, soil‐to‐leaf conductance and osmotic potential of guard cells at zero PAR. The model was applied to field observations on three functional types that include 11 species in subtropical southern China. Non‐linear statistical regression was used to obtain parameters of the model. The result indicated that the model was capable of predicting stomatal conductance of all the 11 species and three functional types under wide ranges of environmental conditions. Major conclusions included that coniferous trees and shrubs were more tolerant for and resistant to soil water stress than broad‐leaf trees due to their lower osmotic potential, lignified guard cell walls, and sunken and suspended guard cell structure under subsidiary epidermal cells. Mid‐day depression in transpiration and photosynthesis of pines may be explained by decreased stomatal conductance under a large vapour pressure deficit. Stomatal conductance of pine trees was more strongly affected by vapour pressure deficit than that of other species because of their small soil‐to‐leaf conductance, which is explainable in terms of xylem tracheids in conifer trees. Tracheids transport water by means of small pit‐pairs in their side walls, and are much less efficient than the end‐perforated vessel members in broad‐leaf xylem systems. These conclusions remain hypothetical until direct measurements of these parameters are available.     

Is stomatal conductance in a tomato crop controlled by soil or atmosphere?

Summary The effects of soil water deficits and air vapour pressure deficits on stomatal conductance of tomato leaves were analysed separately under field conditions in central Portugal. Three conditions were created: low soil and air humidity (A), high soil and air humidity (B) and low soil but high air humidity (C). The results show that the effect of air vapour pressure deficit on stomatal behaviour is more important than the effect of soil water deficit when the predawn leaf water potential is above –0.4 MPa.     

叶片内水传输的模拟

根据水在介质中的流动规律和能量守恒原理,在植物叶片内建立了一个稳态的水传输模型。该模型考虑了气孔复合体内外、共质体与质外体、原生质与细胞壁在水传输上的不同,应用计算机详细地分析和计算了叶内(特别是气孔复合体内)水的传输,得到水势在叶片内近似分布的关系式。应用这些关系式对叶内的水势和水势差作了估计,并对不同解剖特征叶片内的水势差作了比较。     

A hydromechanical and biochemical model of stomatal conductance

A mathematical model of stomatal conductance is presented. It is based on whole‐plant and epidermal hydromechanics, and on two hypotheses: (1) the osmotic gradient across guard cell membranes is proportional to the concentration of ATP in the guard cells; and (2) the osmotic gradient that can be sustained per unit of ATP is proportional to the turgor pressure of adjacent epidermal cells. In the present study, guard cell [ATP] is calculated using a previously published model that is based on a widely used biochemical model of C₃ mesophyll photosynthesis. The conductance model for Vicia faba L. is parameterized and tested As with most other stomatal models, the present model correctly predicts the stomatal responses to variations in transpiration rate, irradiance and intercellular CO₂. Unlike most other models, however, this model can predict the transient stomatal opening often observed before conductance declines in response to decreases in humidity, soil water potential, or xylem conductance. The model also explicitly accommodates the mechanical advantage of the epidermis and correctly predicts that stomata are relatively insensitive to the ambient partial pressure of oxygen, as a result of the assumed dependence on ATP concentration.     

In the light of stomatal opening: new insights into 'the Watergate'

Stomata can be regarded as hydraulically driven valves in the leaf surface, which open to allow CO2 uptake and close to prevent excessive loss of water. Movement of these 'Watergates' is regulated by environmental conditions, such as light, CO2 and humidity. Guard cells can sense environmental conditions and function as motor cells within the stomatal complex. Stomatal movement results from the transport of K+ salts across the guard cell membranes. In this review, we discuss the biophysical principles and mechanisms of stomatal movement and relate these to ion transport at the plasma membrane and vacuolar membrane. Studies with isolated guard cells, combined with recordings on single guard cells in intact plants, revealed that light stimulates stomatal opening via blue light-specific and photosynthetic-active radiation-dependent pathways. In addition, guard cells sense changes in air humidity and the water status of distant tissues via the stress hormone abscisic acid (ABA). Guard cells thus provide an excellent system to study cross-talk, as multiple signaling pathways induce both short- and long-term responses in these sensory cells.     

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.     

ABA-deficient (aba1) and ABA-insensitive (abi1-1, abi2-1) mutants of Arabidopsis have a wild-type stomatal response to humidity

In most plant species, a decrease in atmospheric humidity at the leaf surface triggers a decrease in stomatal conductance. While guard cells appear to respond to humidity‐induced changes in transpiration rate, as opposed to relative humidity or vapour pressure difference, the underlying cellular mechanisms for this response remain unknown. In the present set of experiments, abscisic acid (ABA)‐deficient (aba1) and ABA‐insensitive (abi1‐1 and abi2‐1) mutants of Arabidopsis thaliana were used to test the hypothesis that the humidity signal is transduced by changes in the flux or concentration of ABA delivered to the stomatal complex in the transpiration stream. In gas exchange experiments, stomatal conductance was as sensitive to changes in vapour pressure difference in aba1, abi1‐1 and abi2‐1 mutant plants as in wild‐type plants. These experiments appear to rule out an obligate role for either the concentration or flux of ABA or ABA conjugates as mediators of the guard cell response to atmospheric water potential. The results stand in contrast to the well‐established role of ABA in mediating guard cell responses to decreases in soil water potential.     

Stomatal responses to humidity in air and helox

Abstract. Stomatal responses to humidity were studied in several species using normal air and a helium: oxygen mixture (79:21 v/v, with CO₂ and water vapour added), which we termed 'helox'. Since water vapour diffuses 2.33 times faster in helox than in air, it was possible to vary the water-vapour concentration difference between the leaf and the air at the leaf surface independently of the transpiration rate and vice versa. The CO₂ concentration at the evaporating surfaces ( c_i ), leaf temperature and photon flux density were kept constant throughout the experiments. The results of these experiments were consistent with a mechanism for Stomatal responses to humidity that is based on the rate of water loss from the leaf. Stomata apparently did not directly sense and respond to either the water vapour concentration at the leaf surface or the difference in water vapour concentration between the leaf interior and the leaf surface. In addition, stomatal responses that caused reductions in transpiration rate at low humidities were accompanied by decreases in photosynthesis at constant c_i , suggesting heterogeneous (patchy) stomatal closure.     

The temperature dependence of shoot hydraulic resistance: implications for stomatal behaviour and hydraulic limitation

Recent soil pressurization experiments have shown that stomatal closure in response to high leaf–air humidity gradients can be explained by direct feedback from leaf water potential. The more complex temperature‐by‐humidity interactive effects on stomatal conductance have not yet been explained fully. Measurements of the change in shoot conductance with temperature were made on Phaseolus vulgaris (common bean) to test whether temperature‐induced changes in the liquid‐phase transport capacity could explain these temperature‐ by‐humidity effects. In addition, shoot hydraulic resistances were partitioned within the stem and leaves to determine whether or not leaves exhibit a greater resistance. Changes in hydraulic conductance were calculated based on an Ohm’s law analogy. Whole‐plant gas exchange was used to determine steady‐ state transpiration rates. A combination of in situ psychrometer measurements, Scholander pressure chamber measurements and psychrometric measurements of leaf punches was used to determine water potential differences within the shoot. Hydraulic conductance for each portion of the pathway was estimated as the total flow divided by the water potential difference. Temperature‐induced changes in stomatal conductance were correlated linearly with temperature‐induced changes in hydraulic conductance. The magnitude of the temperature‐induced changes in whole‐plant hydraulic conductance was sufficient to account for the interactive effects of temperature and humidity on stomatal conductance.     

Stomatal control of transpiration from a developing sugarcane canopy

Abstract. Stomatal conductance of single leaves and transpiration from an entire sugarcane (Saccharum spp. hybrid) canopy were measured simultaneously using independent techniques. Stomatal and environmental controls of transpiration were assessed at three stages of canopy development, corresponding to leaf area indices (L) of 2.2, 3.6 and 5.6. Leaf and canopy boundary layers impeded transport of transpired water vapour away from the canopy, causing humidity around the leaves to find its own value through local equilibration rather than a value determined by the humidity of the bulk air mass above the canopy. This tended to uncouple transpiration from direct stomatal control, so that transpiration predicted from measurement of stomatal conductance and leaf-to-air vapour pressure differences was increasingly overestimated as the reference point for ambient vapour pressure measurement was moved farther from the leaf and into the bulk air. The partitioning of control between net radiation and stomata was expressed as a dimensionless decoupling coefficent ranging from zero to 1.0. When the stomatal aperture was near its maximum this coefficient was approximately 0.9, indicating that small reductions in stomatal aperture would have had little effect on canopy transpiration. Maximum rates of transpiration were, however, limited by large adjustments in maximum stomatal conductance during canopy development. The product of maximum stomatal conductance and L. a potential total canopy conductance in the absence of boundary layer effects, remained constant as L increased. Similarly, maximum canopy conductance, derived from independent micrometeorological measurements, also remained constant over this period. Calculations indicated that combined leaf and canopy boundary layer conductance decreased with increasing L such that the ratio of boundary layer conductance to maximum stomatal conductance remained nearly constant at approximately 0.5. These observations indicated that stomata adjusted to maintain both transpiration and the degree of stomatal control of transpiration constant as canopy development proceeded.     

冬小麦叶片气孔导度模型水分响应函数的参数化

植物气孔导度模型的水分响应函数用来模拟水分胁迫对气孔导度的影响过程, 是模拟缺水环境下植物与大气间水、碳交换过程的关键算法。水分响应函数包括空气湿度响应函数和土壤湿度(或植物水势)响应函数, 该研究基于田间实验观测, 分析了冬小麦(Triticum aestivum)叶片气孔导度对不同空气饱和差和不同土壤体积含水量或叶水势的响应规律。一个土壤水分梯度的田间处理在中国科学院禹城综合试验站实施, 不同水分胁迫下的冬小麦叶片气体交换过程和气孔导度以及其他的温湿度数据被观测, 同时观测了土壤含水量和叶水势。实验数据表明, 冬小麦叶片气孔导度对空气饱和差的响应呈现双曲线规律, 变化趋势显示大约1 kPa空气饱和差是一个有用的阈值, 在小于1 kPa时, 冬小麦气孔导度对空气饱和差变化反应敏感, 而大于1 kPa后则反应缓慢; 分析土壤体积含水量与中午叶片气孔导度的关系发现, 中午叶片气孔导度随土壤含水量增加大致呈现线性增加趋势, 但在平均土壤体积含水量大于大约25%以后, 气孔导度不再明显增加, 而是维持在较高导度值上下波动; 冬小麦中午叶片水势与相应的气孔导度之间, 随着叶水势的增加, 气孔导度呈现增加趋势。根据冬小麦气孔导度对空气湿度、土壤湿度和叶水势的响应规律, 研究分别采用双曲线和幂指数形式拟合了水汽响应函数, 用三段线性方程拟合了土壤湿度响应函数和植物水势响应函数, 得到的参数可以为模型模拟冬小麦的各类水、热、碳交换过程采用。     

Measurements of electrical leaf surface conductance reveal re-condensation of transpired water vapour on leaf surfaces

Electrical conductance ( λ ) was measured continuously and in vivo on leaf surfaces of Vicia faba and Aegopodium podagraria . λ increased with rise and decreased with fall in humidity, exhibiting a hysteresis during an applied humidity cycle [90–20–-90% relative humidity (r.h.)]. After treatment with NaNO₃ aerosols, a sudden increase in λ was observed at 73% r.h., which is close to the deliquescence point of the salt. Transpiration and electrical conductance of untreated leaves were measured simultaneously under conditions of constant r.h., while the photosynthetic photon flux density and CO₂ concentration of the air were varied to induce changes of stomatal aperture. At 35% r.h., changes of light and CO₂ level revealed a strong correlation between stomatal conductance ( g _S) and λ for Vicia faba leaves. This was also found at 90, 75, 60, 45 and 25% r.h. on the lower but not on the astomatous, upper surface of Aegopodium podagraria . The correlation between g _S and λ for stomata-bearing leaf surfaces indicates that an equilibrium exists between the ambient water vapour phase and the liquid water phase on and within the cuticle. This is modified by transpired water vapour influencing the air humidity inside the boundary layer. Our results imply re-condensation of transpired water vapour to salts on the leaf surface and its sorption to the cuticle.     

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.