AOBPreview originally published online on February 14, 2006
Annals of Botany 2006 97(5):831-835; doi:10.1093/aob/mcl031
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Stomatal Oscillations in Orange Trees under Natural Climatic Conditions
1 Faculty of Bioscience Engineering, Laboratory of Plant Ecology, Ghent University, Coupure links 653, B-9000 Ghent, Belgium and 2 Agricultural Meteorology Group, Physics Department, University of Zimbabwe, PO Box MP167, Mt Pleasant, Harare, Zimbabwe
* For correspondence. E-mail kathy.steppe{at}UGent.be
Received: 6 October 2005 Returned for revision: 2 November 2005 Accepted: 5 January 2006 Published electronically: 14 February 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims Stomatal oscillations have been reported in many plant species, but they are usually induced by sudden step changes in the environment when plants are grown under constant conditions. This study shows that in navel orange trees (Citrus sinensis) pronounced stomatal oscillations occur and persist under natural climatic conditions.
• Methods Oscillations in stomatal conductance were measured, and related to simultaneous measurements of leaf water potential, and flow rate of sap in the stems of young, potted plants. Cycling was also observed in soil-grown, mature orchard trees, as indicated by sap flow in stem and branches.
• Key Results Oscillations in stomatal conductance were caused by the rapid propagation and synchronization of changes in xylem water potential throughout the tree, without rapid changes in atmospheric conditions.
• Conclusions The results show marked stomatal oscillations persisting under natural climatic conditions and underscore the need to discover why this phenomenon is so pronounced in orange trees.
Key words: Citrus sinensis, orange tree, sap flow, transpiration, leaf water potential, stomatal conductance, stomatal oscillation, natural climatic conditions
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Stomatal oscillations are defined as the phenomenon of cyclic opening and closing movements of stomates (Barrs, 1971
). They are believed to result from instability in the negative feedback loops that control stomatal aperture via leaf water status (Barrs, 1971; Herppich and von Willert, 1995). Such instability can be caused by a lag and/or an overshoot in response to the feedback signal (Kaiser and Kappen, 2001).
Based on the work of Apel (1967), Barrs (1971) proposed a tentative grouping of oscillations based on water or CO2. Short-period stomatal oscillations (<10 min) with small amplitudes are associated with control of CO2 status and appear to depend on the external CO2 concentration. Slower oscillations (30–50 min) with larger amplitudes are associated with control of the plant–water status. However, the general validity of this grouping is uncertain, because short-period oscillations related to CO2 content have been observed only in a small number of plant species.
Stomatal oscillations, described as water-based by Barrs (1971), have been reported in at least 30 plant species. However, most of these oscillations occurred when plants were grown in a constant environment that was suddenly changed (Barrs, 1971; Cowan, 1972; Farquhar and Cowan, 1974; Herppich and von Willert, 1995; Kaiser and Kappen, 2001; Prytz et al., 2003; West et al., 2005). Although there is no a priori reason why stomatal oscillations may not occur under field conditions, there is little evidence for their occurrence in plants grown under field conditions (Levy and Kaufmann, 1976; Hirose et al., 1994). If oscillations in stomatal aperture and conductance are a result of unbalanced water supply and demand, caused by sudden large increase in water loss from the plant, then such conditions might arise under natural conditions and result in oscillations.
This short communication shows that in navel orange trees pronounced stomatal oscillations occur and persist under naturally occurring atmospheric conditions unaffected by any specific environmental disturbance.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Experiments were done in the open-air laboratory on the flat roof of the Physics Department of the University of Zimbabwe (17·79°S, 31·04°W, elevation 1450 m a.s.l.) using six actively growing 2-year-old navel orange trees [Citrus sinensis (L.) Osbeck] of the baianinha selection grafted on a troyer citrange rootstock (Citrus sinensis x Poncirus trifoliate). The trees were approx. 1·0 m high and their stem diameter at soil surface ranged from 10 to 12 mm. The trees were planted in asbestos pots 0·7 m diameter and 0·5 m high filled with dark-red clayey loam soil (Hussein, 1982
). The soil water content was maintained close to field capacity (45 % v/v) by watering twice a week in the evening. The trees were grown under a transparent plastic shelter to exclude rain, but with all sides of the shelter open to allow free circulation of air. Although the results for one tree are presented in this short communication, observations in the other five trees were similar on other days. All the trees could not be measured at the same time due to limited equipment. Observations were made on mature, healthy and fully expanded leaves with equal exposure to solar radiation. The oscillations in stomatal conductance were related to changes in leaf water potential, and sap flow rate through the stem. Leaf water potential was measured using thermocouple psychrometers: four standard C-52 sample chambers (Wescor Inc., Logan, UT, USA), connected to a microvoltmeter (HR-33T; Wescor Inc.), kept at constant temperature in the laboratory. Measurements were made in the psychrometric (wet bulb depression) mode. The psychrometers were calibrated with NaCl solutions over the range 0 to –4·55 MPa. Samples were taken from leaves adjacent to those selected for porometer measurements (see below). In order to determine the changes in leaf water potential, measurements were taken at 10-min intervals. With four C-52 sample chambers, equilibration intervals were limited to approx. 40 min. Trials showed that equilibration was reached within this time interval. As a consequence, water potential measurement could not be replicated. However, the changes in water potential were much larger than the errors. Stomatal conductance was measured with a dynamic diffusion porometer (AP4; Delta-T devices, Cambridge, UK) on four selected leaves. Readings were taken in continuous cycles with each leaf measured at least once every 5 min. Sap flow rate in the stems was continuously measured with a Dynagage heat balance sap flow sensor (SGA9-WS, Dynamax Inc., Houston, TX, USA). Signals from the sap flow sensor, and from instruments for measuring air temperature, relative humidity and incoming short-wave radiation, were recorded automatically at 5-s intervals and 5-min averages were stored on a data logger (CR23X; Campbell Scientific Ltd, Shepshed, UK).
Oscillations in sap flow have also been measured in mature, 4·5-year-old trees in an orchard at the Mazowe Citrus Estate (Zimbabwe). Sap flow rates in stem and branches of selected, soil-grown orchard trees were continuously measured to study the effects of different irrigation strategies. Cycling occurred in the orchard trees, as indicated by the daily records of sap flow in stem and branches. A Delta-T weather station was used for recording microclimatic data.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Examples of measurements of stomatal conductance and stem sap flow in a young orange tree during a winter day (6 Jul. 2005) in Zimbabwe are given in Fig. 1B. The sky was largely clear with occasional patchy clouds as shown by the small fluctuations in conditions (Fig. 1A). The stomatal conductance (Fig. 1B) ranged from 0·007 to 0·145 mol m–2 s–1. Levy and Kaufmann (1976)
reported oscillations in stomatal conductance varying from 0·004 to 0·042 mol m–2 s–1 for 4-year-old citrus trees under controlled greenhouse conditions with root systems at different temperatures. Seven clear oscillations were observed in a time interval of approx. 8 h giving a mean period of about 70 min per oscillation (Fig. 1B). Oscillations generally have a period of up to 50 min (see Barrs, 1971). Also stem sap flow oscillated similarly with an identical cycle of about 70 min. However, the oscillations in stem sap flow lagged behind those in stomatal conductance by about 30 min (i.e. water uptake lagged behind water loss).
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These results show that, under atmospheric conditions without specific or abrupt disturbance, oscillations in stomatal conductance persist in young orange trees. Further sap flow measurements were made under field conditions on mature navel orange trees grown in soil in a commercial orchard at Mazowe Citrus Estate (Zimbabwe). A typical pattern of cyclic variations in branch and stem sap flow rate of a 4·5-year-old orange tree in the orchard is given in Fig. 2. Sap flow in the stem lagged behind branch sap flow by about 20 min. Despite the smooth increase in vapour pressure deficit of the air from 0 to 3·4 kPa, again pronounced cycling occurred.
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Oscillations in leaf conductance for the potted trees were accompanied by oscillations in leaf water potential (Fig. 3): maximum conductance and minimum water potential were out of phase by 10–25 min. Stomates started opening when leaf water potential was low (more negative) and started closing when leaf water potential was high (less negative) again. With roots of potted citrus trees at 5 °C, Levy and Kaufmann (1976)
observed that maximum conductance preceded minimum xylem potential by 30 min, while little time lag occurred with roots at 25 °C. In the present study the mean temperature of the soil was 16 °C. Because oscillations occurred in the whole tree, it is probable that xylem water potential is the signal transmitting agent (Cowan, 1972). The synchronization of stomatal movements by xylem water potential may occur by two mechanisms. The first involves a hydropassive, positive feedback response, which is purely hydraulic and causes stomata to open when increased transpiration and/or increased xylem tension reduces the turgor in guard and epidermal cells. The increased stomatal aperture is positively related to increased turgor pressure of the guard cells that form the pore, but negatively related to the pressure of adjacent subsidiary or epidermal cells that surround the guard cells. Guard and epidermal turgor is thereby decoupled by the mechanical advantage of the epidermis (Buckley, 2005). In other words, any increase of transpiration causes turgor to decline in both guard and epidermal cells and ensures an increase in stomatal aperture due to the mechanical advantage of the epidermis. This hydraulic effect increases the tendency of stomata to oscillate (Kaiser and Kappen, 2001). It may also synchronize the stomatal movements in different parts of the same leaf.
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The second mechanism is the hydro-active, negative feedback response where an increase in transpiration will act as the closing stimulus. It involves an active (i.e. biochemically mediated) physiological response of guard cells to perturbations of the leaf water potential. With increased transpiration, active regulation of guard cell osmotic pressure will reduce guard cell turgor and cause stomatal closure. This physiological response of guard cells lags behind the stimulus (probably leaf water potential) (Fig. 3) and is responsible for the relatively slow turgor mechanism (Kaiser and Kappen, 2001
). The hydraulic effect acts rapidly and precedes the slower, physiological feedback response which acts in the opposite direction (Kaiser and Kappen, 2001; Buckley, 2005).
The juxtaposition of the positive and the negative feedback loops explains the stomatal oscillations because both are involved in the stomatal responses to disturbances of the water balance and cause the two-phase response of stomates (Cowan, 1972; Farquhar and Cowan, 1974; Buckley, 2005). The present results demonstrate that water uptake lags behind water loss by approx. 30 min (Fig. 1B). Hence, this temporal non-synchronization between water uptake and loss leads to disturbances of the water balance which seems to be an essential feature for the occurrence of oscillation as hypothesized by Lang et al. (1969) amongst others. Cavitation in xylem conductive elements might play a role in oscillations, but is a matter of speculation (Buckley, 2005). It is not possible to explain why such pronounced oscillations in stomatal conductance occur in orange trees under field conditions.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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In orange trees stomatal oscillations occur and persist for many hours under atmospheric conditions without sudden changes, as shown by measurements on young potted trees and verified under orchard conditions. Simultaneous measurements of stomatal conductance and sap flow show that xylem water potential is probably the signal transmitting agent, which is propagated throughout the tree. The synchronization of stomatal movements by xylem water potential may occur by hydropassive positive feedback and by physiological negative feedback of stomates to the leaf water potential. However, the detailed mechanism of such pronounced oscillations in orange trees grown under natural field conditions without specific and abrupt disturbances in the atmospheric conditions remain to be described.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Many thanks to the Mazowe Citrus Estate of Zimbabwe for providing the plant material and management skills for the trees and to the Belgian Inter-University Council (VLIR Institutional Cooperation with the University of Zimbabwe) for providing financial support and a travel grant for the first author.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Apel P. 1967. Über rhythmisch verlaufende Änderungen in der CO2-Aufnahme von Blättern. Berlin Deutsche Botanische Garten 80: 3–9.
Barrs HD. 1971. Cyclic variations in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. Annual Review of Plant Physiology 22: 223–236.
Buckley TN. 2005. The control of stomata by water balance. New Phytologist 168: 275–292.[CrossRef][Web of Science][Medline]
Cowan IR. 1972. Oscillations in stomatal conductance and plant functioning associated with stomatal conductance: observations and a model. Planta 106: 185–219.[CrossRef]
Farquhar GD, Cowan IR. 1974. Oscillations in stomatal conductance: the influence of environmental gain. Plant Physiology 54: 769–772.
Herppich WB, von Willert DJ. 1995. Dynamic changes in leaf bulk water relations during stomatal oscillations in mangrove species: continuous analysis using a dewpoint hygrometer. Physiologia Plantarum 94: 479–485.[CrossRef]
Hirose T, Ikeda M, Izuta T, Miyake H, Totsuka T. 1994. Stomatal oscillation in peanut leaves observed under field conditions. Japanese Journal of Crop Science 63: 162–163.
Hussein J. 1982. An investigation into methods of flood irrigation of orange trees. Zimbabwe Agricultural Journal 79: 73–79.
Kaiser H, Kappen L. 2001. Stomatal oscillations at small apertures: indications for a fundamental insufficiency of stomatal feedback-control inherent in the stomatal turgor mechanism. Journal of Experimental Botany 52: 1303–1313.
Lang ARG, Klepper B, Cumming MJ. 1969. Leaf water balance during oscillation of stomatal aperture. Plant Physiology 44: 826–830.
Levy Y, Kaufmann MR. 1976. Cycling of leaf conductance in citrus exposed to natural and controlled environments. Canadian Journal of Botany 54: 2215–2218.
Prytz G, Futsaether CM, Johnsson A. 2003. Self-sustained oscillations in plant water regulation: induction of bifurcations and anomalous rhythmicity. New Phytologist 158: 259–267.[CrossRef]
West JD, Peak D, Peterson JQ, Mott KA. 2005. Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal images. Plant, Cell and Environment 28: 633–641.[CrossRef]
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