Stomatal and non-stomatal limitations on leaf carbon assimilation in beech (Fagus sylvatica L.) seedlings under natural conditions

  • I. Aranda Instituto Nacional de Investigaciones Agrarias y Tecnologías Agroalimentarias, Centro de Investigación Forestal, Madrid.
  • J. Rodríguez-Calcerrada Centre d’Ecologie Fonctionnelle et Evolutive. Montpellier Cedex.
  • T.M. Robson Department of Biological and Environmental Sciences, Plant Biology, University of Helsinki.
  • F.J. Cano Unidad de Anatomía, Grupo de Investigación de Genética y Fisiología Forestal, E.T.S.I. Montes, Universidad Politécnica de Madrid.
  • L. Alté Instituto Nacional de Investigaciones Agrarias y Tecnologías Agroalimentarias, Centro de Investigación Forestal, Madrid.
  • D. Sánchez-Gómez Unidad de Anatomía, Grupo de Investigación de Genética y Fisiología Forestal, E.T.S.I. Montes, Universidad Politécnica de Madrid.


Limitations to diffusion and biochemical factors affecting leaf carbon uptake were analyzed in young beech seedlings (Fagus sylvtica L.) growing in natural gaps of a beech-wood at the southern limit of the species. Half of the seedlings received periodic watering in addition to natural rainfall to reduce the severity of the summer drought. Plant water status was evaluated by measuring predawn water potential. Basic biochemical parameters were inferred from chlorophyll fluorescence and photosynthesis-CO2 curves (A-Cc) under saturating light. The curves were established on three dates during the summer months. The main variables studied included: stomatal and mesophyll conductance to CO2 (gs and gm respectively), maximum velocity of carboxylation (Vcmax) and maximum electron transport capacity (Jmax). The gm was estimated by two methodologies: the curve-fitting and J constant methosds. Seedlings withstood moderate water stress, as the leaf predawn water potential (Ψpd) measured during the study was within the range –0.2 to –0.5 MPa. Mild drought caused gs and gm to decrease only slightly in response to Ψpd. However both diffusional parameters explained most of the limitations to CO2 uptake. In addition, it should be highlighted that biochemical limitations, prompted by Vcmax and Jmax, were related mainly to ontogenic factors, without any clear relationship with drought under the moderate water stress experienced by beech seedlings through the study. The results may help to further understanding of the functional mechanisms influencing the carbon fixation capacity of beech seedlings under natural conditions.


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Author Biography

I. Aranda, Instituto Nacional de Investigaciones Agrarias y Tecnologías Agroalimentarias, Centro de Investigación Forestal, Madrid.
Investigador. Dpto de Ecologia y Genetica


Aranda I., Gil L., Pardos J.A., 2000. Water relations and gas exchange in Fagus sylvatica L. and Quercus petraea (Mattuschka) Liebl. in a mixed stand at their southern limit of distribution in Europe. Trees 14, 344-352.

Aranda I., Gil L., Pardos J.A., 2001. Effects of thinning in a Pinus sylvestris L. stand on foliar water relations of Fagus sylvatica L. seedlings planted within the pinewood. Trees, Structure and Function 15: 358- 364.

Aranda I., Gil L., Pardos J.A., 2002. Physiological responses of Fagus sylvatica L. seedlings under Pinus sylvestris L. and Quercus pyrenaica Willd. overstories. Forest Ecology and Management 162, 153-164.

Aranda I., Gil L., Pardos J.A., 2004. Improvement of growth conditions and gas exchange of Fagus sylvatica L. seedlings planted below a recently thinned Pinus sylvestris L. stand. Trees 18, 211-220.

Aranda I., Gil L., Pardos J.A., 2005. Seasonal changes in apparent hydraulic conductance and their implications for water use of European beech (Fagus sylvatica L.) and sessile oak [Quercus petraea (Matt.) Liebl ] in South Europe. Plant Ecology. 179, 155-167.

Backes K., Leuschner C., 2000. Leaf water relations of competitive Fagus sylvatica and Quercus petraea trees during 4 years differing in soil drought. Canadian Journal of Forest Research 30, 335-346.

Balandier P., Sinoquet H., Frak E., Giuliani R., Vandame M., Descamps S., Coll L., Adam B., Prévosto B., Curt T., 2007. Six-year evolution of light use efficiency, carbon gain and growth of beech saplings (Fagus sylvatica L.) planted under Scots pine (Pinus sylvestris L.) shelterwood. Tree Physiology 27, 1073-1082. PMid:17472934

Bernacchi C.J., Portis A.R., Nakano H., von Caemmerer S., Long S.P., 2002. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 130, 1992-1998. PMid:12481082 PMCid:166710

Breda N., Huc R., Granier A., Dreyer E., 2006. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Annals of Forest Science 63, 625-644.

Brodribb T.J., Jordan G.J., 2008. Internal coordination between hydraulics and stomatal control in leaves. Plant Cell and Environment 31, 1557-1564. PMid:18684244

Von Caemmerer S., 2000. Biochemical Models of Leaf Photosynthesis. CSIRO, Collingwood,Australia.

Cornic G., 1994. Drought stress and high light effects on leaf photosynthesis. In: Baker NR, Bowyer JR, eds. Photoinhibition of photosynthesis. Oxford: Bios Scientific Publishers, 297-313.

Chaves M.M., 1991. Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42, 1-16.

Chaves M.M., Pereira J.S., Maroco J.P., Rodrigues M.L., Ricardo C.P.P., Osorio M.L., Carvalho I., Faria T., Pinherio C., 2002. How plants cope with water stress in the field. Photosynthesis and growth. Annals of Botany 89, 907-916.

Chaves M.M., Maroco J.P., Pereira J.S., 2003. Understanding plant responses to drought - from genes to the whole plant. Functional Plant Biology 30, 239-264.

Damour G.a, Vandame, M.b, Urban, L.c., 2009. Long-term drought results in a reversible decline in photosynthetic capacity in mango leaves, not just a decrease in stomatal conductance. Tree Physiology 29, 675-684. PMid:19324697

Díaz-Espejo A., Nicolás E., Enrique Fernández J., 2007. Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell and Environment 30, 922-933. PMid:17617820

Dreyer E., Le Roux X., Montpied P., Daudet F.A., Masson F., 2001. Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiology 21, 223-232. PMid:11276416

Ennahli S., Earl H.J., 2005. Physiological limitations to photosynthetic carbon assimilation in cotton under water stress. Crop Science 45, 2374-2382.

Epron D., Godard D., Cornic G., Genty B. 1995 Limitation of net CO2 assimilation rate by internal resistances to CO2 transfer in the leaves of two tree species (Fagus sylvatica L. and Castanea sativa Mill.). Plant Cell and Environment 18, 43-51.

Ethier G.J., Livingston N.J., 2004. On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell and Environment 27, 137-153.

Evans J.R., Loreto F., 2000. Acquisition and diffusion of CO2 in higher plant leaves. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis, physiology and metabolism. Kluwer, Dordrecht, pp 321-351. PMCid:1300936

Farquhar G.D., von Caemmerer S., Berry J.A., 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78-90.

Flexas J., Bota J., Escalona J.M., Sampol B. & Medrano H., 2002. Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology 29, 461-471.

Flexas J., Medrano H., 2002. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Annals of Botany 89, 183-189.

Flexas J., Galmés J., Ribas-Carbó M., Medrano H., 2005. The effects of drought in plant respiration. In: Lambers H, Ribas-Carbó M (eds) Advances in Photosynthesis and Respiration 18. Plant Respiration: from Cell to Ecosystem. Kluwer Academic Publishers, Dordrecht, 85-94.

Flexas J., Bota J., Galmés J., Medrano H., Ribas-Carbo M., 2006. Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiogia Plantarum 127, 343-352.

Flexas J., Ribas-Carbó M., Diaz-Espejo A., Galmés J., Medrano H., 2008. Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell and Environment 31, 602-621. PMid:17996013

Flexas J., Barón M., Bota J., Ducruet J.-M., Gallé A., Galmés J., Jiménez M., Pou A., Ribas-Carbó M., Sajnani C., Tomás M and Medrano H., 2009. Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri•V. rupestris). Journal of Experimental Botany 60, 2361-2377. PMid:19351904

Fotelli M.N., Geßler A., Peuke A.D., Rennenberg H., 2001. Drought affects the competition between Fagus sylvatica L. seedlings and an early successional species (Rubus fruticosus): growth, water status and d13C composition. New Phytologist 151, 427-435.

Galmés J., Medrano H., Flexas J., 2007. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175, 81-93. PMid:17547669

Gallé A., Feller U., 2007. Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiologia Plantarum 131, 412-421. PMid:18251880

Galle A., Florez-Sarasa I., Tomas M., Pou A., Medrano H., Ribas-Carbo M., Flexas J., 2009. The role of mesophyll conductance during water stress and recovery in tobacco (Nicotiana sylvestris): acclimation or limitation? Journal of Experimental Botany 60, 2379-2390. PMid:19321646

Genty B., Briantais J.M., Baker N.R., 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87-92.

Grassi G., Magnani F., 2005. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell and Environment 28, 834-849.

Grassi G., Ripullone F., Borghetti M., Raddi S., Magnani F., 2009. Contribution of diffusional and non-diffusional limitations to midday depression of photosynthesis in Arbutus unedo L. Trees 23, 1149-1161.

Geßler A., Keitel C., Kreuzwieser J., Matyssek R., Seiler W., Rennenberg H., 2007. Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees 21, 1-11.

Granier A., Reichstein M., BrÉda N., Janssens I.A., Falge E., Ciais P., Grunwald T., Aubinet M., Berbigier P., Bernhofer C., Buchmann N., Facini O., Grassi G., Heinesch B., Ilvesniemi H., Keronen P., Knohl A., KÖstner B., Lagergren F., Lindroth A., Longdoz B., Loustau D., Mateus J., Montagnani L., Nys, C., Moors E., Papale D., Peiffer M., Pilegaard K., Pita G., Pumpanen J., Rambal S., Rebmann C., Rodrigues A., Seufert G., Tenhunen J., Vesala I., Wang Q., 2007. Evidence for soil water control on carbon and water dynamics in European forests during the extremely dry year: 2003. Agricultural and Forest. Meteorology 143, 123-145.

Granier A., Ceschia E., Damesin C., Dufrêne E., Epron D., Gross P., Lebaube S., Le Dantec V., Le Goff N., Lemoine D., Lucot E., Ottorini J.M., Pontailler J.Y., Saugier B., 2000. The carbon balance of a young Beech forest. Functional Ecology 14, 312-325.

Hanba Y.T., Kogami H., Terashima, I., 2003. The effect of internal CO2 conductance on leaf carbon isotope ratio. Isotopes in Environmental and Health Studies 39, 5-13. PMid:12812251

Harley P.C., Loreto F., Di Marco G., Sharkey T.D., 1992. Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology 98, 1429-1436. PMid:16668811 PMCid:1080368

Keenan T., Sabate S., Gracia C., 2010. The importance of mesophyll conductance in regulating forest ecosystem productivity during drought periods. Global Change Biology 16, 1019-1034.

Kramer D.M., Johnson G., Kiirats O., Edwards G.E., 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209-218. PMid:16228395

Kunstler G., Curt T., Bouchaud M., Lepart J., 2005. Growth, mortality, and morphological response of European beech and downy oak along a light gradient in sub-Mediterranean forest. Canadian Journal of Forest Research 35, 1657-1668.

Laisk A, Loreto F. 1996. Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence: rubisco specificity factor, dark respiration in the light, excitation distribution between photosystems, alternative electron transport rate and mesophyll diffusion resistance. Plant Physiology 110, 903-912. PMid:12226229 PMCid:157790

Lawlor D.W., Cornic G., 2002. Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell and Environment 25, 275-294. PMid:11841670

Lendzion J., Leuschner ch., 2008. Growth of European beech (Fagus sylvatica L.) saplings is limited by elevated atmospheric vapour pressure deficits. Forest Ecology and Management 256, 648-655.

Leuschner C.h., Backes K., Hertel D., Schipka F., Schmitt U., Terborg O., Runge M., 2001. Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and wet years. Forest Ecology and Management 149, 33-46.

Leuzinger S., Zotz G., Asshoff R., Körner C., 2005. Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiology 25, 641-650. PMid:15805084

Madsen P., 1994. Growth and survival of Fagus sylvatica seedlings in relation to light intensity and soil water content. Scandinavian Journal of Forest Research 9, 316-322.

Medrano H., Escalona J.M., Boto J., Gulias J., Flexas J., 2002. Regulation of photosynthesis of C3 plants in response to progressive drought: Stomatal conductance as a reference parameter. Annals of Botany 89, 895-905.

Montpied P., Granier A., Dreyer E., 2009. Seasonal timecourse of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. Journal of Experimental Botany 60, 2407-2418. PMid:19457983

Niinemets Ü., Sonninen E., Tobias M. 2004. Canopy gradients in leaf intercellular CO2 mole fractions revisited: interactions between leaf irradiance and water stress need consideration. Plant, Cell and Environment 27, 569-583

Niinemets U., Cescatti A., Rodeghiero M., Tosens T. 2005 Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant Cell and Environment 28, 1552-1566.

Robson M.T., Rodríguez-Calcerrada J., Sánchez-Gómez D., Aranda I., 2009. Summer drought impedes beech seedlings performance more in a sub-Mediterranean forest understory than in small gaps. Tree Physiology 29, 249-259. PMid:19203950

Rodríguez-Calcerrada J., Mutke S., Alonso J., Gil L., Pardos J.A., Aranda I., 2008a. Influence of overstory density on understory light, soil moisture, and survival of two underplanted oak species in a Mediterranean montane Scots pine forest. Investigación Agraria: Sistemas y Recursos Forestales. 17, 31-38.

Rodríguez-Calcerrada J., Pardos J.A., Gil L., Aranda I., 2008b. Ability to avoid water stress in seedlings of two oak species is lower in a dense forest understory than in a medium canopy gap. Forest Ecology and Management 255, 421-430.

Rodríguez-Calcerrada J., Atkin O.K., Robson M.T., Zaragoza- Castells J., Gil L., Aranda I. 2010. Acclimation of leaf dark respiration to shifts in summer temperature was independent of degree of canopy closure and water stress in a manipulative field experiment with beech seedlings. Tree Physiology 30, 214-224. PMid:20007131

Rosenqvist E., van Kooten O., 2003. Chlorophyll fluorescence: a general description and nomenclature. In, De Ell, J.R. and Toivonen, P.M.A. (eds.) Practical applications of chlorophyll fluorescence in plant biology, pp: 31-77. Kluwer Academic Publishers, The Netherlands.

Sharkey T.D., Bernacchi C.J., Farquhar G.D., Singsaas E.L., 2007. Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell and Environment 30, 1035-1040. PMid:17661745

Tognetti R., Michelozzi M., Borghetti M., 1994. Response to light of shade-grown beech seedlings subjected to different watering regimes. Tree Physiology 14, 751-758. PMid:14967645

Valladares F., Chico J.M., Aranda I., Balaguer L., Dizengremel P., Manrique E., Dreyer E., 2002. The greater seedling high-light tolerance of Quercus robur over Fagus syl vatica is linked to a greater physiological plasticity. Trees 16, 395-403.

Wagner, S., Collet C., Madsend P., Nakashizukae T., R.D. Nylandf, Khosro Sagheb-Talebi. 2010. Beech regeneration research: from ecological to silvicultural aspects. Forest Ecology and Management 259, 2172-2182.

Warren C.R., 2006. Estimating the internal conductance to CO2 movement. Functional Plant Biology 33, 431-442.

Warren C.R., Löw M., Matyssek R., Tausz M., 2007. Internal conductance to CO2 transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation. Environmental Experimental Botany 59, 130-138.

Wilson K.B., Baldocchi D.D. & Hanson P.J. 2000a. Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf ageing and drought in mature deciduous tree species. Tree Physiology 20, 787- 797. PMid:12651499

Wilson K.B., Baldocchi D.D., Hanson P.J., 2000b. Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiology 20, 565-578. PMid:12651421

Xu L., Baldocchi D.D., 2003. Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiology 23, 865-877. PMid:14532010

How to Cite
ArandaI., Rodríguez-CalcerradaJ., RobsonT., CanoF., AltéL., & Sánchez-GómezD. (2012). Stomatal and non-stomatal limitations on leaf carbon assimilation in beech (Fagus sylvatica L.) seedlings under natural conditions. Forest Systems, 21(3), 405-417.
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