Peristomatal Transpiration Research Articles

Leaf hydraulics II: Vascularized tissues

Current models of leaf hydration employ an Ohm's law analogy of the leaf as an ideal capacitor, neglecting the resistance to flow between cells, or treat the leaf as a plane sheet with a source of water at fixed potential filling the mid-plane, neglecting the discrete placement of veins as well as their resistance. We develop a model of leaf hydration that considers the average conductance of the vascular network to a representative areole (region bounded by the vascular network), and represent the volume of tissue within the areole as a poroelastic composite of cells and air spaces. Solutions to the 3D flow problem are found by numerical simulation, and these results are then compared to 1D models with exact solutions for a range of leaf geometries, based on a survey of temperate woody plants. We then show that the hydration times given by these solutions are well approximated by a sum of the ideal capacitor and plane sheet times, representing the time for transport through the vasculature and tissue respectively. We then develop scaling factors relating this approximate solution to the 3D model, and examine the dependence of these scaling factors on leaf geometry. Finally, we apply a similar strategy to reduce the dimensions of the steady state problem, in the context of peristomatal transpiration, and consider the relation of transpirational gradients to equilibrium leaf water potential measurements.

Comparing model predictions and experimental data for the response of stomatal conductance and guard cell turgor to manipulations of cuticular conductance, leaf‐to‐air vapour pressure difference and temperature: feedback mechanisms are able to account for all observations

Stomata respond to increasing leaf-to-air vapour pressure difference (LAVPD) (D) by closing. The mechanism by which this occurs is debated. A role for feedback and peristomatal transpiration has been proposed. In this paper, we apply a recent mechanistic model of stomatal behaviour, and compare model and experimental data for the influence of increasing D on stomatal conductance. We manipulated cuticular conductance (g(c)) by three independent methods. First, we increased g(c) by using a solvent mixture applied to both leaf surfaces prior to determining stomatal responses to D; second, we increased g(c) by increasing leaf temperature at constant D; and third, we coated a small area of leaf with a light oil to decrease g(c). In all three experiments, experimental data and model outputs showed very close agreement. We conclude, from the close agreement between model and experimental data and the fact that manipulations of g(c), and hence cuticular transpiration, influenced g(s) in ways consistent with a feedback mechanism, that feedback is central in determining stomatal responses to D.

Solute sorting in grass leaves: the transpiration stream.

Solutes distribute differentially between leaf tissues and cells. The present study tested the hypothesis that certain solutes are supplied preferentially to the epidermis in the transpiration stream, by-passing mesophyll cells along bundle sheath extensions. Using energy dispersive X-ray analysis of extracted cell sap, the distribution of solutes was studied in the emerged zone (transpiring) and the elongation zone (non-transpiring) of the developing leaf three of barley (Hordeum vulgare L.). The basic distribution of Cl, K, P and Ca between epidermis and bulk tissue, and between cells within the epidermis, was similar in the two leaf regions. However, in the emerged zone differences in solute concentrations between tissues and cells were greater. A local reduction in transpiration rate along the emerged portion of the blade specifically prevented Ca from accumulating to high levels in epidermal cells close to stomata. It is concluded that differences in solute concentrations between epidermal cells and other leaf tissues can be established in the absence of transpiration, but that they require transpiration for their full expression. Peristomatal transpiration appears to be responsible for high Ca in interstomatal cells.

Viewpoint: New light on the importance of peristomatal transpiration

The purpose of this paper is to discuss in detail once again some controversial views on the stomatal control mechanism, because it is essential that a consistent, universally valid concept of plant water relations provides a basis for an understanding of the impact of air pollutants on plants. The reader is reminded of the original concept of peristomatal transpiration, and its central role in the stomatal control system is reinforced, i.e. its function as a sensory mechanism in the negative feedback loop of stomatal conductance. The described stomatal dysfunction subsequent to the exposure of ozone to Picea abies (L.) Karst. needles can be traced to a specific impairment of this sensory mechanism, and this demonstrates once again the paramount importance of peristomatal transpiration.

Dynamics of change in stomatal response and water status of Picea abies during a persistent drought period: a contribution to the traditional view of plant water relations.

Four experiments on the simulation of a persistent drought period were carried out with cloned Picea abies (L.) Karst. trees: two in the field under varying weather conditions and two in a climate chamber under variously manipulated humidity conditions. Patterns of diurnal dynamics in gas exchange rates and water potential were monitored and analyzed. The first phase of the drought was characterized by relatively high daily maxima for photosynthesis and transpiration. With decreasing humidity during the day, the values dropped steeply, and the declines were larger and occurred earlier on each passing day of the drought period. When soil water potential was lower than -2000 hPa, maximum stomatal aperture was greatly reduced despite a humid atmosphere. Under these conditions, rates of photosynthesis and transpiration decreased less steeply from the daily maxima and differences between maxima and minima were small. In the field, the daily sums of transpiration and photosynthesis were more dependent on atmospheric conditions than on soil water potential. In the growth chamber experiments, the daily sums of transpiration and photosynthesis decreased continuously as the soil dried, at first steeply until a soil water potential of -2000 hPa was reached, then slowly. Predawn water potential values fluctuated under field conditions, but tended to decrease with time, whereas needle osmotic potential increased slightly. Because relative humidities did not reach 100% in the growth chamber, predawn water potentials of plants in the growth chamber were never higher than -1.0 MPa although the soil was saturated. In the experiment with a high average air humidity during the daily stress period, relatively high predawn water potentials were maintained until lower soil water potentials of -8000 hPa were reached. Results were used to assess the importance of evaporative demand versus soil drying on stomatal responses within the context of current concepts of plant water relations. The observed trends in diurnal dynamics can be explained solely by the interdependency of leaf conductance and water potential. Stomata react directly to the ratio of water supply to demand. The central role of peristomatal transpiration in this system is emphasized.

Cell water potential, osmotic potential, and turgor in the epidermis and mesophyll of transpiring leaves

Water potential, osmotic potential and turgor measurements obtained by using a cell pressure probe together with a nanoliter osmometer were compared with measurements obtained with an isopiestic psychrometer. Both types of measurements were conducted in the mature region of Tradescantia virginiana L. leaves under non-transpiring conditions in the dark, and gave similar values of all potentials. This finding indicates that the pressure probe and the osmometer provide accurate measurements of turgor, osmotic potentials and water potentials. Because the pressure probe does not require long equilibration times and can measure turgor of single cells in intact plants, the pressure probe together with the osmometer was used to determine in-situ cell water potentials, osmotic potentials and turgor of epidermal and mesophyll cells of transpiring leaves as functions of stomatal aperture and xylem water potential. When the xylem water potential was-0.1 MPa, the stomatal aperture was at its maximum, but turgor of both epidermal and mesophyll cells was relatively low. As the xylem water potential decreased, the stomatal aperture became gradually smaller, whereas turgor of both epidermal and mesophyll cells first increased and afterward decreased. Water potentials of the mesophyll cells were always lower than those of the epidermal cells. These findings indicate that evaporation of water is mainly occurring from mesophyll cells and that peristomatal transpiration could be less important than it has been proposed previously, although peristomatal transpiration may be directly related to regulation of turgor in the guard cells.

Stomatal Movements and Repartition of the Elements K, Cl, Na, P, Ca, Mg and S in the Stomatal Complexes of Vicia faba and Commelina commuais. Electron probe studies

Summary Using an electron microprobe, the variation of K and Cl elements in the stomatal complexes of Vicia faba and Commelina communis were followed. Our purpose was also to assess whether migrations of other elements such as Na, P, Ca, Mg and S occur during stomatal movements. Differences were found in the total ionic amount between open and closed states in the stomatal complexes and also an imbalance in ion fluxes between guard cells and epidermal cells. Tentatively, this could be explained by peristomatal transpiration mechanisms as described by Maier-Maercker.

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.

Stomatal pore and cuticle formation inFunaria

Cuticle and pore development in the guard cells ofFunaria were investigated with the electron microscope. Pore cuticle formation is simultaneous with the creation of the pore itself. The morphology of the pore cuticle is unlike that of any cuticle described in the literature. It has many lamellae which are penetrated by electron dense fibrils. Three different cuticular morphologies exist from the pore to the subsidiary cell walls. The cuticles on the pore and outer walls contain fibrils that sometimes reach to the surface. The subsidiary cell cuticle lacks fibrils altogether. It is hypothesized that (1) cuticularization of the middle lamella contributes to ventral wall separation and (2) differences in extent of cuticular fibrils are related to greater water loss from stomata than from subsidiary cells (peristomatal transpiration).

Accumulation of 86Rb and 43K Ions in the Cells Surrounding the Air Pores of Conocephalum conicum

Summary 86Rb and 43K were introduced into the thallus of Conocephalum conicum through the rhizoids and were finally localized by microautoradiography in the cells around the air pores. Parallel experiments with T12SO4 led to massive accumulation of Tl+ in the same sites. Due to the spatial separation of the air pore apparatus from the rest of the thallus, evaporation must be strong around the pore. In accordance with the conditions of peristomatal transpiration in vascular plants, ion concentration in the apoplast around the pore must increase. As in the cells lining the pore the activity of s-glycerophosphatase was high, it was thought that carbohydrate transport must take place there, and that this process helped to pull water and ions from the apoplast into the cell.

»Peristomatal Transpiration« and Stomatal Movement: A Controversial View: VIII.Stomatal Control by Conditions of Water Supply and Peristomatal Transpiration

Summary On the basis of a sluice model relating leaf water potential to the flow of water through the plant the following conclusions were drawn: 1.The bulk leaf water potential is not a relevant parameter with which to correlate stomatal movements.Leaf water potential is regarded as one output signal among others.The flow of water through the plant which is related to stomatal aperture provides another output signal. 2.Peristomatal transpiration is not the underlying process of a control mechanism, additional to the main system.Peristomatal transpiration can be regarded as the capacity of the guard cell to determine the sensitivity of its response to environmental perturbations. For these grounds a mechanistic model was designed in which peri stomatal transpiration has a central role.

»Peristomatal Transpiration« and Stomatal Movement: A Controversial View: VII. Correlation of Stomatal Aperture with Evaporative Demand and Water Uptake Through the Roots

Responses of stomata to changes in air humidity and osmolarity of the root medium were studied using seedlings of Commelina communis. 1. The lower a chosen level of air humidity was, the lower was also the osmolarity at which pore closure started. 2. Stomata which were found to respond with great sensitivity to a water vapour deficit of the air were also strongly affected by minor increases in osmolarity of the root medium. 3. A lateral and a longitudinal gradient in stomatal sensitivity to stress factors was found in the leaf. The response to osmolarity of the root medium and humidity of the air significantly increased towards the leaf margin. The humidity response of the stomata is not considered as an additional and independent system. Peristomatal transpiration is seen as the capacity of the guard cell to determine the sensitivity of the hydraulic system.

«Peristomatal Transpiration» and Stomatal Movement: A Controversial View: V. Rubidium-86 in the Epidermal Transpiration Stream

Summary 86Rb was introduced into the transpiration stream of detached leaves and rooted seedlings of several plant species and traced by microautoradiography. When the pores stayed open during the feeding 86Rb was found in the guard cells. When a dark period of 4 hours followed feeding in the light, 86Rb ions did not return to the subsidiary cells although the stomata had closed. Rubidium transport to the guard cells was reduced when the pores were closed. Then, accumulation occurred in the subsidiary cells while at the site of the guard cells grain density of the film was generally low. Using a gelatine layer, with which the leaf surfaces remained coated throughout the feeding period, small quantities of 86Rb were picked up from the external surfaces of the leaves. This was considered sufficient evidence of 86Rb excretion from the guard cells. Major conclusions are: 1. Ions accumulate by the action of peristomatal transpiration. 2. Ion fluxes are -secondary- processes in all cases of stomatal reaction. 3. The role of peristomatal transpiration is a sensory and triggering one. Peristomatal transpiration is the process by which plants sense environmental conditions. It is not a mechanism for closing stomata.

≪Peristomatal Transpiration≫ and Stomatal Movement: A Controversial View: VI. Lanthanum Deposits in the Epidermal Apoplast

Lanthanum ions were used as a tracer for ion movement in the epidermal apoplast. Electron dense deposits of the tracer were mainly found in the external wall portions of subsidiary and guard cells. This supported the view that ion accumulation in these cells is the result of peristomatal transpiration. All - i.e. external and internal - surfaces of subsidiary and guard cells contribute towards the ≪humidity response≫ of the stomata. I is suggested that internal and external components are not ≪independent≫ from the outcome of stomatal response i.e. the degree of stomatal opening established by the stomatal response to humidity, as is generally assumed. It seems unlikely that the stomatal control mechanism operates on the basis of a K + flow which is mediated by the external K + concentration in the apoplast. Peristomatal transpiration is supposed to regulate passive transport channels by affecting the water potential gradients within the epidermis.

«Peristomatal Transpiration» and Stomatal Movement: A Controversial View III. Visible Effects of Peri stomatal Transpiration on the Epidermis

Summary 1. Experiments with berberine sulfate brought to light that stomatal opening depended on a water front which freely expanded within the epidermis when the transpiration rate was low. 2. The subsidiary cells underwent changes during stomatal response to evaporative demand. These changes offered a basis for an explanation of the hysteresis in stomatal response. 3. Stomata responded to changes in air humidity with repeated closing and opening reactions provided «their» vein was intact. 4. The turgor reduction of the subsidiary cells, caused by peristomatal transpiration was demonstrated by the isopiestic method. 5. From the experiments it is concluded that each stomatal complex is an independent unit, and that it acts according to its own supply-demand-relationship. 6. The experiments suggest that the lateral water flow within the epidermis is a fine instrument for transmitting information about fluctuations of the supply-demand-relationship to the stomatal control system.

«Peristomatal Transpiration» and Stomatal Movement: A Controversial View IV. Ion Accumulation by Peristomatal Transpiration

Summary Ions of silver, lead and mercury and potassium were fed into the transpiration stream and their accumulation in the epidermis has been demonstrated. The results were consistent with earlier experiments using thallium ( Maercker, 1965 b ). When special care was taken to provide open stomata, the deposits were found in the lumina of the guard cells. In all other instances the ions accumulated mainly in the subsidiary cells or in both the guard and the subsidiary cells. Deposits were also found to occur on the surface of these cells, in particular along the cuticular ledges of the pore. The characteristic distributional pattern reflects the pattern of peristomatal transpiration ( Maercker, 1965 , Maercker, 1965 ; Maier-Maercker, 1979a ). Transpiration rate of the guard cell, which during stomatal opening exceeds that of the subsidiary cell, explains the high accumulation rate in the guard cell. When during stomatal closure the subsidiary cell, due to its enhanced transpiration, maintains the lateral water flow, the ions are trapped before they reach the guard cell. Accumulation is seen as consequence of the water flux into the cell; the rates of accumulation are determined by the concentration gradient between a particular cell and its surrounding wall. Since the interpretation of the results apply for toxic heavy metal ions and potassium ions, it is concluded that all ions accumulate by the action of peristomatal transpiration. Shortcomings of the K+ shuttle hypothesis are discussed in the light of the findings.

«Peristomatal Transpiration» and Stomatal Movement: A controversial View

Summary Another direct method – hygrophotography – produced further evidence of peristomatal transpiration. Enhanced cuticular transpiration is shown to be a characteristic of guard and subsidiary cells. There is a gradient of cuticular transpiration rate within the entire epidermis. Normal epidermal cells never show a uniform transpiration intensity. Antagonism exists between guard and subsidiary cells: During stomatal opening transpiration rate of the guard cell exceeds by far that of the subsidiary cell, while during stomatal closure it falls behind it. The main issue of this paper was to re-emphasize the decisive role of peristomatal transpiration in stomatal movement and to place peristomatal transpiration within the scope of recent developments in this field of research. Peristomatal transpiration was not considered as «loss of water from the guard cell to the atmosphere» ( Raschke , 1975) but was integrated into the model of the soil-plant-atmosphere continuum. The special role of the subsidiary cell in the negative feedback transmission has been discussed. The view is held that the environmental variables (supply and demand) are cross-correlated by the competition between water flux into the guard cell and transpiration of the subsidiary cell. It was concluded that peristomatal transpiration does not exert an additional open-loop control but is the prime cause of the hydroactive system.

«Peristomatal Transpiration» and Stomatal Movement: A Controversial View

Stomatal movement was observed under controlled cuvette conditions. When the humidity of the air was changed, stomatal response was linear or slightly curvilinear and exhibited hysteresis. While with detached Vicia faba plants the response became steeper with every succeeding day, curves obtained from rooted plants of Commelina communis had a common regression line during five consecutive days. The influence of air velocity and water supply to the roots were then studied. Increased air velocity (in the range of 0,3-1,3 m × sec-1 made impossible wide stomatal apertures while moderate stomatal opening) was not impeded. Restrictions of water supply (with mannitol solutions) resulted in depressions of opening relative to the humidity range; parallel graphs were obtained. After removing the mannitol from the roots, the original response was resumed. When potassium chloride was added to the water supply, maximum aperture was reached in high humidity. However, the response to changes in humidity was stronger. Rinsing the roots had no effect, but when in imitation of rain, the leaves were exposed to trickling water, the potassium effect was occasionally overcome. The results were discussed in the light of peristomatal transpiration. The view is held that the environmental variables (supply and demand) are cross-correlated and that stomatal response meets the supply-demand-relationship at the level of the subsidiary cell. Hysteresis is explained with the competition between water flux into the guard cell and transpiration of the subsidiary cell. Salt effects are seen in terms of local gradients between cell wall and cell vacuole. Following sudden illumination a steep gradient will enhance salt permeation into the guard cell and with it wide opening. On increased evaporative demand, the steep gradient assists in drawing water from the vacuole, increased closing tendency being the result.

A study of the transpiration surfaces of Avena sterilis L. var. Algerian leaves using monosilicic acid as a tracer for water movement

The sites and pathways of transpiration from leaves of Avena sterilis L. var. Algerian were studied using the accumulation of monosilicic acid as a tracer for water movement. Seedlings of Algerian oats were grown under silicon free conditions and fed monosilicic acid, in a normal nutrient solution, via the roots. The silicon component of monosilicic acid was located in freeze substituted tissue by means of x-ray microprobe analysis. Methods of tissue fixation preventing post treatment movement of tracer were developed and it was determined that monosilicic acid is a suitable tracer for water.Sites of water loss were marked by accumulation of silicon. Internal evaporating surfaces having a high intensity of water loss were demonstrated. Evaporation from epidermal surfaces was most intense over the guard and subsidiary cells with very little evaporation from the cuticular surfaces of normal epidermal cells. Moderately high evaporation occurred from epidermal fibre cells located above the veins. Evaporation from all exposed walls of guard cells including the wall adjacent to the pore was intense. Smaller amounts of tracer were located in the unexposed anticlinal walls of epidermal cells as well as within the unexposed walls of mesophyll cells. The results are interpreted as demonstrating the extent of internal transpiration surfaces and that cuticular epidermal transpiration is low. Strong support is given to the existence of peristomatal transpiration. Internal pathways of water movement are defined and the occurrence of these is discussed in relation to cuticular transpiration and lateral water movement in the epidermis.

Localization of Thallium in Stomata is Independent of Transpiration

The specific locations of the evaporating surfaces in the leaf are not yet known. However, Maercker (1965) repeated successfully the early experiments of Stahl (1894) and concluded from her evidence that the cuticular component oftranspiration could be further divided into "cuticular" and "peristomatal" transpiration, where the latter term refers to transpiration from the surfaces of the guard cells and their subsidiary cells. Peristomatal transpiration has been the subject of considerable recent interest (e.g. Lange et al. 1971).