Abstract
Stomatal pores regulate CO2 uptake and water loss from leaves. Stomatal responses are dynamic by nature and often lag behind the faster changing environmental conditions as is common in tree canopies. Even under constant conditions, gas exchange of angiosperms occasionally shows cycling fluctuations, called stomatal oscillations. They are interpreted as an effect of feedback control failing to achieve stable regulation and thus demonstrate that stomata not only respond to external factors, but also to the environment inside the leaf. The processes which translate transpiration into turgor are called the physiological gain. The physical processes and environmental conditions which control stomatal aperture, stomatal conductance and transpiration are called the physical gain. More research on the physiological gain is needed in order to understand these processes. In order to overcome the epidermal backpressure, guard cell turgor has to reach a certain threshold level, although guard cell swelling anticipates the opening. When the pore opens, the relation between pore area and stomatal conductance determines the physical gain. In contrast to the Fick’s first law of diffusion, this relation is not linear, but convex shaped, with a rapid increase of conductance just after opening and much less effect of aperture changes at large apertures. The high and abruptly changing gain at smallest pore openings can promote overshooting oscillatory responses, as supported by microscopic observations of stomatal apertures. A review of the literature suggests that stomatal movements are metabolically active responses of guard cells to local water status. A full understanding of the mechanisms, however, is complex because stomatal movements result from the interaction of two processes that are difficult to separate experimentally: hydraulic effects, and active osmotic adjustment of guard cells and epidermal cells. Hydropassive movement, resulting from an unbalance of turgor pressure between guard cells and the surrounding epidermis, may also occur. An example of hydropassive movement is the so-called Iwanoff effect or Wrong Way Response (WWR), i.e. a fast opening response followed by a slow closure, that occurs as a response to a steep increase in the leaf to air difference in water vapor pressure and may last 2.5–38 min depending on the species and the experimental conditions. An additional 10–60 min may be required for completing the closing response. In contrast to the rather slow osmoregulatory negative feedback, hydraulic responses act fast, starting within seconds and completing within minutes, and have been suggested as a key mechanism in stomatal oscillations. In a plant displaying oscillations, movements of individual stomata are more or less synchronized on a very small scale within a leaf (1–2 mm). The nature of the synchronizing mechanism is not clear. Synchronization can also occur among leaves, ultimately leading to concerted cycling of gas exchange of entire plants. Comprehensive models of stomatal behaviour based on the mechanisms operating in and around stomatal guard cells are still missing, and may help explaining gas exchange response to stressors. Studies with the air pollutant of most concern to forests, i.e. ground-level ozone, suggest that stomata show a transient decrease of stomatal conductance upon exposure and are sluggish in responding to further stimuli.
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References
Assmann S, Gershenson A (1991) The kinetics of stomatal responses to VPD in Vicia faba: electrophysiological and water relations models. Plant Cell Environ 14:455–465
Assmann SM, Grantz DA (1990) The magnitude of the stomatal response to blue light – modulation by atmospheric humidity. Plant Physiol 93:701–709
Assmann SM, Shimazaki K (1999) The multisensory guard cell. Stomatal responses to blue light and abscisic acid. Plant Physiol 119:337–361
Assmann SM, Wang XQ (2001) From milliseconds to millions of years: guard cells and environmental responses. Curr Opin Plant Biol 4:421–428
Barrs HD (1968) Effect of cyclic variations in gas exchange under constant environmental conditions on ratio of transpiration to net photosynthesis. Physiol Plant 21:918–920
Barrs HD (1971) Cyclic variation in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. Ann Rev Plant Physiol 22:223–236
Bravdo BA (1977) Oscillatory transpiration and CO2 exchange of Citrus leaves at the CO2 compensation concentration. Physiol Plantarum 41:36–41
Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162:663–670
Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585
Brogårdh T, Johnsson A (1973) Oscillatory transpiration and water uptake of Avena plants II. Effects of deformation of xylem vessels. Physiol Plantarum 28:341–345
Brun WA (1961) Photosynthesis and transpiration of banana leaves as affected by severing the vascular system. Plant Physiol 36:577–580
Buckley TN (2005) The control of stomata by water balance. New Phytol 168:275–292
Buckley TN, Mott KA (2000) Stomatal responses to non-local changes in PFD: evidence for long-distance hydraulic interactions. Plant Cell Environ 23:301–309
Buckley T, Mott K (2002) Dynamics of stomatal water relations during the humidity response: implications of two hypothetical mechanisms. Plant Cell Environ 25:407–419
Cardon ZG, Mott KA, Berry JA (1994) Dynamics of patchy stomatal movements, and their contribution to steady-state and oscillating stomatal conductance calculated using gas-exchange techniques. Plant Cell Environ 17:995–1007
Cochard H, Coll L, Le Roux X, Améglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol 128:282–290
Comstock JP, Mencuccini M (1998) Control of stomatal conductance by leaf water potential in Hymenoclea salsola (T. & G.), a desert subshrub. Plant Cell Environ 21:1029–1038
Cowan IR (1972) Oscillations in stomatal conductance and plant functioning associated with stomatal conductance: observations and a model. Planta 106:185–219
Cowan IR (1977) Stomatal behaviour and environment. Adv Bot Res 4:117–228
Cox EF (1968) Cyclic changes in transpiration of sunflower leaves in a steady environment. J Exp Bot 19:167–175
Delwiche MJ, Cooke JR (1977) An analytical model of the hydraulic aspects of stomatal mechanics. J Theor Biol 69:113–141
DeMichele DW, Sharpe PJH (1973) An analysis of the mechanics of guard cell motion. J Theor Biol 41:77–96
Dewar RC (1995) Interpretation of an empirical model for stomatal conductance in terms of guard cell function. Plant Cell Environ 18:365–372
Dzikiti S, Steppe K, Lemeur R, Milford JR (2007) Whole-tree level water balance and its implications on stomatal oscillations in orange trees Citrus sinensis (L.) Osbeck under natural climatic conditions. J Exp Bot 58:1893–1901
Eamus D, Shanahan S (2002) A rate equation model of stomatal responses to vapour pressure deficit and drought. BMC Ecol 2:8
Ehrler WL, Nakayama FS, Vanbavel CH (1965) Cyclic changes in water balance and transpiration of cotton leaves in a steady environment. Physiol Plant 18:766–775
Elias P (1979) Stomatal oscillations in adult forest trees in natural-environment. Biol Plant 21:71–74
Farquhar G (1978) Feedforward responses of stomata to humidity. Aust J Plant Physiol 5:787–900
Florell C, Rufelt H (1960) Transpiration of wheat plants cultivated under different environmental conditions. Physiol Plant 13:482–486
Franks PJ (2004) Stomatal control and hydraulic conductance, with special reference to tall trees. Tree Physiol 24:865–878
Franks P, Cowan I, Farquhar G (1997) The apparent feedforward response of stomata to air vapour pressure deficit: information revealed by different experimental procedures with two rainforest trees. Plant Cell Environ 20:142–145
Franks P, Cowan I, Farquhar G (1998) A study of stomatal mechanics using the cell pressure probe. Plant Cell Environ 21:94–100
Fuchs EE, Livingston NJ (1996) Hydraulic control of stomatal conductance in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco] and alder [Alnus rubra (Bong)] seedlings. Plant Cell Environ 19:1091–1098
Grantz DA (1990) Plant response to atmospheric humidity. Plant Cell Environ 13:667–679
Grulke NE, Neufeld HS, Davison AW, Chappelka A (2007a) Stomatal behavior of O3-sensitive and -tolerant cutleaf coneflower (Rudbeckia laciniata var. digitata) Great Smoky Mountain National Park. New Phytol 173:100–109
Grulke NE, Paoletti E, Heath RL (2007b) Comparison of calculated and measured foliar O3 flux in crop and forest species. Environ Pollut 146:640–647
Haefner J, Buckley T, Mott K (1997) A spatially explicit model of patchy stomatal responses to humidity. Plant Cell Environ 20:1087–1097
Harris M, Outlaw WH Jr, Mertens R, Weiler EW (1988) Water-stress-induced changes in the abscisic acid content of guard cells and other cells of Vicia faba L. leaves as determined by enzyme-amplified immunoassay. Proc Nat Acad Sci 85:2584–2588
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. Physiol Plant 94:479–485
Hetherington AM (2001) Guard cell signaling. Cell 107:711–714
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Hirose T, Ikeda M, Izuta T, Miyake H, Totsuka T (1994) Stomatal oscillation in peanut leaves observed under field conditions. Jpn J Crop Sci 63:162–163
Hoshika Y, Omasa K, Paoletti E (2012) Whole-tree water use efficiency is decreased by ambient ozone and not affected by O3-induced stomatal sluggishness. PLoS ONE 7:e39270
Hoshika Y, Omasa K, Paoletti E (2013) Both ozone exposure and soil water stress are able to induce stomatal sluggishness. Environ Exp Bot 88:19–23
Iwanoff L (1928) Zur Transpirationsbestimmung am Standort. Berichte der Deutschen Botanischen Gesellschaft 46:306–310
Johnsson A (1973) Oscillatory transpiration and water uptake of Avena plants I. Preliminary observations. Physiol Plant 28:40–50
Johnsson A (2007) Oscillations in plant transpiration. In: Mancuso S, Shabala S (eds) Rhythms in plants. Springer, Berlin
Johnsson M, Brogardh T, Holje Ø (1979) Oscillatory transpiration of Avena plants: perturbation experiments provide evidence for a stable point of singularity. Physiol Plant 45:393–398
Kaiser H (2009) The relation between stomatal aperture and gas exchange under consideration of pore geometry and diffusional resistance in the mesophyll. Plant Cell Environ 32:1091–1098
Kaiser H, Kappen L (2000) In-situ-observation of stomatal movements and gas exchange of Aegopodium podagraria L. in the understory. J Exp Bot 51:1741–1749
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. J Exp Bot 52:1303–1313
Kaiser H, Legner N (2007) Localization of mechanisms involved in hydropassive and hydroactive stomatal responses of Sambucus nigra to dry air. Plant Physiol 143:1068–1077
Kappen L, Andresen G, Lösch R (1987) In situ observations of stomatal movements. J Exp Bot 38:126–141
Keller T, Häsler R (1984) The influence of a fall fumigation with ozone on the stomatal behavior of spruce and fir. Oecologia 64:284–286
Kellomäki S, Wang KY (1997) Effects of elevated O3 and CO2 concentrations on photosynthesis and stomatal conductance in Scots pine. Plant Cell Environ 20:995–1006
Kerstiens G (1997) Cuticular water permeance and its physiological significance. J Exp Bot 47:1813–1832
Laisk A, Oja V, Kull K (1980) Statistical distribution of stomatal apertures of Vicia faba and Hordeum vulgare and the Spannungs phase of stomatal opening. J Exp Bot 31:49–58
Levy Y, Kaufmann MR (1976) Cycling of leaf conductance in citrus exposed to natural and controlled environments. Can J Bot 54:2215–2218
Lu P, Outlaw WH Jr, Smith BG, Freed GA (1997) A new mechanism for the regulation of stomatal aperture size in intact leaves: accumulation of mesophyll-derived sucrose in the guard-cell wall of Vicia faba. Plant Physiol 114:109–118
Maier-Maercker U (1983) The role of peristomatal transpiration in the mechanism of stomatal movement. Plant Cell Environ 6:369–380
Marenco RA, Siebke K, Farquhar GD, Ball MC (2006) Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum. Funct Plant Biol 33:1103–1113
McAdam SAM, Brodribb TJ (2012) Stomatal innovation and the rise of seed plants. Ecol Lett 15:1–8
McAinsh MR, Gray JE, Hetherington AM, Leckie CP, Ng C (2000) Ca2+ signalling in stomatal guard cells. Biochem Soc Trans 28:476–481
Meidner H (1986) Cuticular conductance and the humidity response of stomata. J Exp Bot 37:517–525
Meidner H (1987) The humidity response of stomata and its measurement. J Exp Bot 38:877–882
Meinzer FC (2002) Coordination of vapour and liquid phase water transport properties in plants. Plant Cell Environ 25:265–274
Mills G, Hayes F, Wilkinson S, Davies WJ (2009) Chronic exposure to increasing background ozone impairs stomatal functioning in grassland species. Glob Change Biol 15:1522–1533
Monteith JL (1995) A reinterpretation of stomatal responses to humidity. Plant Cell Environ 18:357–364
Mott KA (2007) Leaf hydraulic conductivity and stomatal responses to humidity in amphistomatous leaves. Plant Cell Environ 30:1444–1449
Mott KA, Franks PJ (2001) The role of epidermal turgor in stomatal interactions following a local perturbation in humidity. Plant Cell Environ 24:657–662
Mott KA, Parkhurst DF (1991) Stomatal response to humidity in air and helox. Plant Cell Environ 14:509–515
Mott KA, Cardon ZG, Berry JA (1993) Asymmetric patchy stomatal closure for the 2 surfaces of Xanthium strumarium L leaves at low humidity. Plant Cell Environ 16:25–34
Nagarajah S (1978) Some differences in the responses of stomata of the two leaf surfaces in cotton. Ann Bot 42:1141–1147
Naidoo G, von Willert DJ (1994) Stomatal oscillations in the mangrove Avicennia germinans. Funct Ecol 8:651–657
Nikolic E (1925) Beiträge zur Physiologie der Spaltöffnungsbewegung. II. Über die Beziehung der Stomatarbewegung zur Lichtintensität. Beihefte zum Botanischen Centralblatt 41:309–346 (in German)
Omasa K (1990) Study on changes in stomata and their surroundings cells using a nondestructive light microscope system: responses to air pollutants. J Agric Meteorol 45:251–257 (in Japanese with English summary)
Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schafer KVR (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526
Outlaw WH Jr, De Vlieghere-He X (2001) Transpiration rate. An important factor controlling the sucrose content of the guard cell apoplast of broad bean. Plant Physiol 126:1716–1724
Paoletti E (2005) Ozone slows stomatal response to light and leaf wounding in a Mediterranean evergreen broadleaf, Arbutus unedo. Environ Pollut 134:439–445
Paoletti E, Grulke NE (2010) Ozone exposure and stomatal sluggishness in different plant physiognomic classes. Environ Pollut 158:2664–2671
Paoletti E, Contran N, Bernasconi P, Günthardt-Goerg MS, Vollenweider P (2009) Structural and physiological responses to ozone in Manna ash (Fraxinus ornus L.) leaves of seedlings and mature trees under controlled and ambient conditions. Sci Total Environ 407:1631–1643
Parlange J-Y, Waggoner PE (1970) Stomatal dimensions and resistance to diffusion. Plant Physiol 46:337–342
Peak D, Mott KA (2011) A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant Cell Environ 34:162–178
Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453
Pei Z-M, Kuchitsu K (2005) Early ABA signalling events in guard cells. J Plant Growth Regul 24:296–307
Phillips NG, Oren R, Licata J, Linder S (2004) Time series diagnosis of tree hydraulic characteristics. Tree Physiol 24:879–890
Pieruschka R, Huber G, Berry JA (2010) Control of transpiration by radiation. Proc Natl Acad Sci 107:13372–13377
Powles JE, Buckley TN, Nicotra AB, Farquhar GD (2006) Dynamics of stomatal water relations following leaf excision. Plant Cell Environ 29:981–992
Prytz G, Futsaether CM, Johnsson A (2003) Thermography studies of the spatial and temporal variability in stomatal conductance of Avena leaves during stable and oscillatory transpiration. New Phytol 158:249–258
Rand RH, Storti DW, Upadhyaya SK, Cooke JR (1982) Dynamics of coupled stomatal oscillators. J Math Biol 15:131–149
Raschke K (1965) Die Stomata als Glieder eines schwingungsfähigen CO2-Regelsystems Experimenteller Nachweis an Zea mays L. Z Naturforsch 20b:1261–1270, in German
Reich PB (1984) Oscillations in stomatal conductance of hybrid poplar leaves in the light and dark. Physiol Plant 61:541–548
Reich PB, Lassoie JP (1984) Effects of low level O3 exposure on leaf diffusive conductance and water-use efficiency in hybrid poplar. Plant Cell Environ 7:661–668
Reiling K, Davison AW (1995) Effects of ozone on stomatal conductance and photosynthesis in populations of Plantago major L. New Phytol 129:587–594
Rose MA, Rose MA (1994) Oscillatory transpiration may complicate stomatal conductance and gas-exchange measurements. HortSci 29:693–694
Rose MA, Beattie DJ, White JW (1994) Oscillations of whole-plant transpiration in ‘Moonlight’ rose. J Am Soc Hortic Sci 119:439–445
Sack L, Holbrook NM (2006) Leaf hydraulics. Ann Rev Plant Biol 57:361–381
Saliendra NZ, Sperry JS, Comstock JP (1995) Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196:357–366
Santrucek J, Hronkova M, Kveton J, Sage RF (2003) Photosynthesis inhibition during gas exchange oscillations in ABA-treated Helianthus annuus: relative role of stomatal patchiness and leaf carboxylation capacity. Photosynthetica 41:241–252
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658
Schulze ED, Lange OL, Buschbom U, Kappen L, Evenari M (1972) Stomatal responses to changes in humidity in plants growing in the desert. Planta 108:259–270
Serengil Y, Augustaitis A, Bytnerowicz A, Grulke N, Kozovitz AR, Matyssek R, Müller-Starck G, Schaub M, Wieser G, Coskun AA, Paoletti E (2011) Adaptation of forest ecosystems to air pollution and climate change: a global assessment on research priorities. iForest Biogeosci For 4:44–48
Shaner DL, Lyon JL (1979) Stomatal cycling in Phaseolus vulgaris L. in response to glyphosate. Plant Sci Lett 15:83–87
Sharpe PJH, Wu H, Spence RD (1987) Stomatal mechanics. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Stanford
Shirazi GA, Stone JF (1976) Oscillatory transpiration in a cotton plant. I. Experimental characterization. J Exp Bot 27:608–618
Shirazi GA, Stone JF, Bacon CM (1976) Oscillatory transpiration in a cotton plant. II. A model. J Exp Bot 27:619–633
Siebke K, Weis E (1995) Assimilation images of leaves of Glechoma-Hederaceae – analysis of nonsynchronous stomata related oscillations. Planta 196:155–165
Stålfelt MG (1928) Die Abhängigkeit der photischen Spaltöffnungsreaktionen von der Temperatur. Planta 6:183–191
Steppe K, Dzikiti S, Lemeur R, Milford JR (2006) Stomatal oscillations in orange trees under natural climatic conditions. Ann Bot 97:831–835
Teoh CT, Palmer JH (1971) Nonsynchronized oscillations in stomatal resistance among sclerophylls of Eucalyptus umbra. Plant Physiol 47:409–411
Thomas SC, Winner WE (2002) Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. Tree Physiol 22:117–127
Tjoelker MG, Volin JC, Oleksyn J, Reich PB (1995) Interaction of ozone pollution and light effects on photosynthesis in a forest canopy experiment. Plant Cell Environ 18:895–905
Upadhyaya SK, Rand RH, Cooke JR (1988) Role of stomatal oscillations on transpiration, assimilation and water-use efficiency of plants. Ecol Model 41:27–40
Vahisalu T, Puzorjova I, Brosché M, Valk E, Lepiku M, Moldau H, Pechter P, Wang Y-S, Lindgren O, Salojarvi J, Loog M, Kangasjarvi J, Kollist H (2010) Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62:442–453
Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165:665–682
Vico G, Manzoni S, Palmroth S, Katul G (2011) Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytol 192:640–652
Wallach R, Da-Costa N, Raviv M, Moshelion M (2010) Development of synchronized, autonomous, and self-regulated oscillations in transpiration rate of a whole tomato plant under water stress. J Exp Bot 61:3439–3449
Wang YP, Jarvis PG (1990) Influence of crown structural properties on PAR absorption, photosynthesis, and transpiration in Sitka spruce: application of a model (MAESTRO). Tree Physiol 7:297–316
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 Environ 28:633–641
Wilkinson S, Davies WJ (2008) Manipulation of the apoplastic pH of intact plants mimics stomatal and growth responses to water availability and microclimatic variation. J Exp Bot 59:619–631
Wilkinson S, Davies W (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant community. Plant Cell Environ 33:510–525
Yang H-M, Zhang W-X, Wang G-X, Li Y, Wei X-P (2003) Cytosolic calcium oscillation may induce stomatal oscillation in Vicia faba. Plant Sci 165:1117–1122
Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318
Zhang SQ, Outlaw WH Jr (2001) Abscisic acid introduced into the transpiration stream accumulates in the guard-cell apoplast and causes stomatal closure. Plant Cell Environ 24:1045–1054
Zhang X, Xu D (2000) Seasonal changes and daily courses of photosynthetic characteristics of 18-year-old Chinese fir shoots in relation to shoot ages and positions within tree crown. Sci Silvae Sin 19(03):36
Zhang W, Fan LM, Wu WH (2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol 143:1140–1151
Zipperlen SW, Press MC (1997) Photosynthetic induction and stomatal oscillations in relation to the light environment of two Dipterocarp rain forest tree species. J Ecol 85:491–503
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Kaiser, H., Paoletti, E. (2014). Dynamic Stomatal Changes. In: Tausz, M., Grulke, N. (eds) Trees in a Changing Environment. Plant Ecophysiology, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9100-7_4
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