Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Do stomata operate at the same relative opening range along a canopy profile of Betula pendula?

Eve Eensalu A C , Priit Kupper A , Arne Sellin A , Märt Rahi B , Anu Sõber A and Olevi Kull A
+ Author Affiliations
- Author Affiliations

A Institute of Ecology and Earth Sciences, Department of Botany, University of Tartu, Lai 40, Tartu 51005, Estonia.

B Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Riia 181, Tartu 51014, Estonia.

C Corresponding author. Email: eve.eensalu@ut.ee

Functional Plant Biology 35(2) 103-110 https://doi.org/10.1071/FP07258
Submitted: 2 November 2007  Accepted: 15 January 2008   Published: 19 March 2008

Abstract

Stomatal density and size were measured along the light gradient of a Betula pendula Roth. canopy in relation to microclimatic conditions. The theoretical stomatal conductance was calculated using stomatal density and dimensions to predict to what degree stomatal conductance is related to anatomical properties and relative stomatal opening. Stomatal density was higher and leaf area smaller in the upper canopy, whereas epidermal cell density did not change significantly along the canopy light gradient, indicating that stomatal initiation is responsible for differences in stomatal density. Stomatal dimensions – the length of guard cell on the dorsal side and the guard cell width – decreased with declining light availability. Maximum measured stomatal conductance and modelled stomatal conductance were higher at the top of the crown. The stomata operate closer to their maximum openness and stomatal morphology is a more important determinant of stomatal conductance in the top leaves than in leaves of lower canopy. As stomata usually limit photosynthesis more in upper than in lower canopy, it was concluded that stomatal morphology can principally be important for photosynthesis limitation in upper canopy.

Additional keywords: light intensity, stomatal conductance, stomatal density, stomatal morphology.


Acknowledgements

The work was sponsored by Estonian Science Foundation (Grants Nos. 6617, 6969 and 7016). We are grateful to Ingmar Tulva and Maarja Öpik for fruitful discussions and to Robert Szava-Kovats for language correction.


References


Aasamaa K, Sõber A (2001) Hydraulic conductance and stomatal sensitivity to changes of leaf water status in six deciduous species. Biologia Plantarum 44, 65–73.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aasamaa K, Sõber A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance and stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal of Plant Physiology 28, 765–774. open url image1

Aasamaa K, Sõber A, Hartung W, Niinemets Ü (2004) Drought acclimation of two deciduous tree species of different layers in a temperate forest canopy. Trees (Berlin) 18, 93–101. open url image1

Anderson MG (1966) Stand structure and light penetration. II. A theoretical analysis. Journal of Applied Ecology 3, 41–54.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Science 163, 375–379.
Crossref | GoogleScholarGoogle Scholar | open url image1

Büssis D, von Groll U, Fisahn J, Altmann T (2006) Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Functional Plant Biology 33, 1037–1043.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carr DJ (2000) On the supposed changes in stomatal frequency and size with height of leaf insertion. Annals of Botany 86, 911–912.
Crossref | GoogleScholarGoogle Scholar | open url image1

Carswell FE, Meir P, Wandell EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiology 20, 179–186.
PubMed |
open url image1

DeMichele DW, Sharpe PJH (1974) A parametric analysis of the anatomy and physiology of the stomata. Agricultural Meterology 14, 229–241.
Crossref | GoogleScholarGoogle Scholar | open url image1

Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytologist 172, 73–82.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Franks PJ, Farquhar GD (2001) The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiology 125, 935–942.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Garten CT, Taylor GE (1992) Foliar d13C within a temperate deciduous forest: spatial, temporal, and species resources of variation. Oecologia 90, 1–7.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hall JL , Hawes C (1991) ‘Electron microscopy of plant cells.’ (Academic Press Inc.: London)

Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424, 901–908.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Idso SB (1991) A general relationship between CO2-induced increases in net photosynthesis and concomitant reductions in stomatal conductance. Environmental and Experimental Botany 31, 381–383.
Crossref | GoogleScholarGoogle Scholar | open url image1

James SA, Bell DT (2000) Influence of light availability on leaf structure and growth of two Eucalyptus globulus ssp. globulus provenances. Tree Physiology 20, 1007–1018.
PubMed |
open url image1

Jones HG (1998) Stomatal control of photosynthesis and transpiration. Journal of Experimental Botany 49, 387–398.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kimura K, Ishida A, Uemura A, Matsumoto Y, Terashima I (1998) Effects of current-year and previous-year PPFDs on shoot gross morphology and leaf properties in Fagus japonica. Tree Physiology 18, 459–466.
PubMed |
open url image1

Klein M, Cheng G, Chung M, Tallman G (1996) Effects of turgor potentials of epidermal cells neghbouring guard cells on stomatal opening in detached leaf epidermis and intact leaflets of Vicia faba L. (faba bean). Plant, Cell & Environment 19, 1399–1407.
Crossref | GoogleScholarGoogle Scholar | open url image1

Klich MG (2000) Leaf variations in Elaegnus angustifolia related to environmental heterogeneity. Environmental and Experimental Botany 44, 171–183.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koike T, Watanabe T, Toda H, Haibara K (1998) Morphological diversity of stomata of representative broadleaved trees in a temperate region: detection with the Sump method. Forest Resources and Environment 36, 57–65. open url image1

Kull O, Niinemets Ü (1993) Variations in leaf morphometry and nitrogen concentration in Betula pendula Roth., Corylus avellana L. and Lonicera xylosteum L. Tree Physiology 12, 311–318.
PubMed |
open url image1

Kull O, Niinemets Ü (1998) Distribution of leaf photosynthetic properties in the tree canopies: comparison of species with different shade tolerance. Functional Ecology 12, 472–479.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Signals from mature to new leaves. Nature 411, 154.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Meidner H , Mansfield TA (1968) ‘Physiology of stomata.’ (McGraw Hill: London)

Meinzer FC, Grantz DA (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant, Cell & Environment 13, 383–388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miyazawa S-I, Livingston NJ, Turpin DH (2006) Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa × P. deltoides). Journal of Experimental Botany 57, 373–380.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mott KA (1988) Do stomata respond to CO2 concentrations ohter than intercellular? Plant Physiology 86, 200–203.
PubMed |
open url image1

Nejad AR, van Meeteren U (2005) Stomatal response characteristics of Tradescantia virginiana grown at high relative air humidity. Physiologia Plantarum 125, 324–332.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Kull O (2001) Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest canopy: photosystem II center openness, non-radiative energy dissipation and excess irradiance under field conditions. Tree Physiology 21, 899–914.
PubMed |
open url image1

Niinemets Ü, Sõber A, Kull O, Hartung W, Tenhunen JD (1999) Apparent controls on leaf conductance by soil water availability and via light-acclimation of foliage structural and physiological properties in a mixed deciduous, temperate forest. International Journal of Plant Sciences 160, 707–721.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Kull O, Tenhunen JD (2004a) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell & Environment 27, 293–313.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets Ü, Sonninen E, Tobias M (2004b) Canopy gradients in leaf intercellular CO2 mole fractions revisited: interactions between leaf irradiance and water stress need consideration. Plant, Cell & Environment 27, 569–583.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthesis light-acclimation need change in leaf anatomy? Plant, Cell & Environment 26, 505–512.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell & Environment 28, 916–927.
Crossref | GoogleScholarGoogle Scholar | open url image1

Paal J (1997) ‘Eesti taimkatte kasvukohatüüpide klassifikatsioon.’ (EV Keskkonnaministeeriumi Info- ja Tehnokeskus: Tallinn)

Paolleti E, Gellini R (1993) Stomatal density variation in beech and holm oak leaves collected over the last 200 years. Acta Oecologica 14, 173–178. open url image1

Parlange J-Y, Waggoner PE (1970) Stomatal dimensions and resistance to diffusion. Plant Physiology 46, 337–342.
PubMed |
open url image1

Poole I, Weyers JDB, Lawson T, Raven JA (1996) Variations in stomatal density and index: implications for palaeoclimatic reconstructions. Plant, Cell & Environment 19, 705–712.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rust S, Roloff A (2002) Reduced photosynthesis in old oak (Quercus robur): the impact of crown and hydraulic architecture. Tree Physiology 22, 597–601.
PubMed |
open url image1

Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective. Photosynthesis Research 39, 351–368.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sellin A (2001) Morphological and stomatal responses of Norway spruce foliage to irradiance within a canopy depending on shoot age. Environmental and Experimental Botany 45, 115–131.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sellin A, Kupper P (2005a) Variation in leaf conductance of silver birch: effects of irradiance, vapour deficit, leaf water status and position within a crown. Forest Ecology and Management 206, 153–166.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sellin A, Kupper P (2005b) Effects of light availability versus hydraulic constraints on stomatal responses within a crown of silver birch. Oecologia 142, 388–397.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sellin A, Kupper P (2007) Temperature, light and leaf hydraulic conductance of little-leaf linden (Tilia cordata) in a mixed forest canopy. Tree Physiology 27, 679–688.
PubMed |
open url image1

Sharpe PJH , Wu H , Spence RD (1987) Stomatal mechanics. In ‘Stomatal function’. (Eds E Zeiger, GD Farquhar, IR Cowan) pp. 91–114. (Stanford University Press: Stanford)

Spence RD, Sharpe PJH, Clark KG (1986) Water stress effects on guard cell anatomy and the mechanical advantage of the epidermal cells. Plant, Cell & Environment 9, 197–202. open url image1

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezana S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology 138, 2337–2343.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tenhunen JD , Pearcy RW , Lange OL (1987) Diurnal variations in leaf conductance and gas exchange in natural environments. In ‘Stomatal function’. (Eds E Zeiger, GD Farquhar, IR Cowan) pp. 323–351. (Stanford University Press: Stanford)

Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. Journal of Experimental Botany 57, 343–354.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomas PW, Woodward FI, Quick WP (2003) Rapid report. Systemic irradiance signalling in tobacco. The New Phytologist 161, 193–198. open url image1

Tichá I (1982) Photosynthetic characteristics during ontogenesis of leaves 7. Stomata density and sizes. Photosynthetica 16, 375–471. open url image1

Tricker PJ, Trewin H, Kull O, Clarkson GJJ, Eensalu E, Tallis MJ, Colella A, Doncaster CP, Sabatti M, Taylor G (2005) Stomatal conductance and not stomatal density determines the long-term reduction in leaf transpiration of poplar in elevated CO2. Oecologia 143, 652–660.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tyree MT , Zimmermann MH (2002) ‘Xylem structure and the ascent of sap.’ (Springer-Verlag: New York)

Uemura A, Ishida A, Nakano T, Terashima I, Tanabe H, Matsumoto Y (2000) Acclimation of leaf characteristics of Fagus species to previous-year and current-year solar irradiances. Tree Physiology 20, 945–951.
PubMed |
open url image1

van Gardingen PR, Jeffree CE, Grace J (1989) Variation in stomatal aperture in leaves of Avena fatua L. observed by low-temperature scanning electron microscopy. Plant, Cell & Environment 12, 887–898.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wagner F, Below R, De Klerk P, Dilcher DL, Joosten H, Kürschner WM, Visscher H (1996) A natural experiment on plant acclimation: lifetime stomatal frequency response of an individual tree to annual atmospheric CO2 increase. Proceedings of the National Academy of Sciences of the United States of America 93, 11705–11708.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Weyers JDB, Lawson T (1997) Heterogeneity in stomatal characteristics. Advances in Botanical Research 26, 317–352. open url image1

Williams M, Rastetter EB, Fernandes DN, Goulden ML, Wofsy SC, Shaver GR, Melillo JM, Munger JW, Fan S-M, Nadelhoffer KJ (1996) Modelling the soil-plant-atmosphere continuum in a Quercus-Acer stand at Harvard Forest: the regulation of stomatal conductance by light, nitrogen, and soil/plant hydraulic properties. Plant, Cell & Environment 19, 911–927.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wong SC, Cowan IR, Farquhar GD (1978) Leaf conductance in relation to assimilation in Eucalyptus pauciflora Sieb. ex Spreng. Plant Physiology 62, 670–674.
PubMed |
open url image1

Woodward FI (1998) Do plants really need stomata? Journal of Experimental Botany 49, 471–480.
Crossref | GoogleScholarGoogle Scholar | open url image1

Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytologist 131, 311–327.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wu H, Sharpe PJH, Spence RD (1985) Stomatal mechanics. III. Geometric interpretation of the mechanical advantage. Plant, Cell & Environment 8, 269–274. open url image1