Leaf morphology, photochemistry and water status changes in resprouting Quercus ilex during drought
Karen Peña-Rojas A , Xavier Aranda A B , Richard Joffre C and Isabel Fleck A DA Departament de Biologia Vegetal, Unitat Fisiologia Vegetal, Facultat Biologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, Spain.
B Present address: Departament de Tecnologia Hortícola, Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Ctra. de Cabrils s / n, 08348 Cabrils, Spain.
C Dream Unit, Centre d’Ecologie Fonctionnelle et Evolutive CNRS, 1919 Route de Mende, 34293 Montpellier cedex 5, France.
D Corresponding author. Email: ifleck@ub.edu
Functional Plant Biology 32(2) 117-130 https://doi.org/10.1071/FP04137
Submitted: 3 August 2004 Accepted: 23 December 2004 Published: 24 February 2005
Abstract
Functional and morphological (structural) characteristics of Quercus ilex L. leaves under drought stress were studied in the forest and in a nursery. We compared undisturbed individuals (controls) with resprouts emerging after clear-cut or excision. When soil water availability was high, gas-exchange was similar in resprouts and controls, despite higher midday leaf water potential, midday leaf hydration and relative water content (RWC). In moderate drought, stomatal closure was found to limit photosynthesis in controls, and in severe drought non-stomatal limitations of photosynthesis were also greater than in resprouts. Leaf structure and chemical composition changed under drought stress. Leaves tended to be smaller in controls with increasing drought, and resprouts had larger leaves and lower leaf mass area (LMA). The relationship between nitrogen (N) content and LMA implied lower N investment in photosynthetic components in controls, which could be responsible for their increased non-stomatal limitation of photosynthesis. Changes were more apparent in leaf density (D) and thickness (T), components of LMA. Decreases in D were related to reductions in cell wall components: hemicellulose, cellulose and lignin. In resprouts, reduced D and leaf T accounted for the higher mesophyll conductance (gmes) to CO2 measured.
Keywords: drought, gas exchange, leaf morphology, mesophyll conductance.
Acknowledgments
This research was supported by funds from the Generalitat de Catalunya 1999 SGR0020 and Laboratoire Européen Associé Ecosystèmes mediterranéens dans un monde changeant.We thank Dr R Savé for helpful discussion; Dr J Casadesús, J Matas and R Simmonneau (Servei de Camps Experimentals, Universitat de Barcelona) for technical assistance and R Rycroft (Servei d’Assessorament Lingüístic, Escola d’Idiomes Moderns, Universitat de Barcelona) for correcting the English manuscript. K Peña-Rojas was the recipient of a doctorate grant from the AECI (Agencia Española de Cooperación con Iberoamérica) and from the Faculty of Forestry Engineering, University of Chile.
Balaguer L,
Afif D,
Dizengremel P, Dreyer E
(1996) Specificity factor of ribulose bisphosphate carboxylase / oxygenase of Quercus robur. Plant Physiology and Biochemistry 36, 879–883.
Brooks A, Farquhar GD
(1985) Effect of temperature on the carbon dioxide-oxygen specificity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the rate of respiration in the light. Planta 165, 397–406.
| Crossref | GoogleScholarGoogle Scholar |
Chaumont M,
Morot-Gaudry J-F, Foyer C
(1995) Effects of photoinhibitory treatment on CO2 assimilation, the quantum yield of CO2 assimilation, D1 protein, ascorbate, glutathione and xanthophyll contents and the electron transport in vine leaves. Plant, Cell and Environment 18, 1358–1366.
Chaves MM,
Maroco JP, Pereira JS
(2003) Understanding plant responses to drought — from genes to the whole plant. Functional Plant Biology 30, 239–264.
| Crossref | GoogleScholarGoogle Scholar |
Demmig-Adams B, Adams WW
(1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among plant species. Planta 198, 460–470.
| Crossref | GoogleScholarGoogle Scholar |
Dijkstra, P (1989). Cause and effect of differences in specific leaf area. In ‘Causes and consequences of variation in growth rate and productivity of higher plants’. pp. 125–140. (SPB Academic Publishing: The Hague)
El Omari B,
Fleck I,
Aranda X,
Moret A, Nadal M
(2001) Effect of fungal infection on leaf gas exchange and chlorophyll fluorescence in Quercus ilex. Annals of Forest Science 58, 165–173.
| Crossref | GoogleScholarGoogle Scholar |
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.
Evans, JR ,
and
Loreto, F (2000). Acquisition and diffusion of CO2 in higher plant leaves. In ‘Photosynthesis: physiology and metabolism’. pp. 321–351. (Kluwer Academic Publishers: The Netherlands)
Farrar, J (1993). Carbon partitioning. In ‘Photosynthesis and production in a changing environment. A field and laboratory manual’. pp. 232–246. (Chapman and Hall: London)
Field, C ,
and
Mooney, HA (1986). The photosynthesis–nitrogen relationships in wild plants. In ‘On the economy of plant form and function’. pp. 25–56. (Cambridge University Press: Cambridge)
Fleck I,
Grau D,
Sanjosé M, Vidal D
(1996) Influence of fire and tree-fell on physiological parameters in Quercus ilex resprouts. Annals of Science 53, 337–346.
Fleck I,
Hogan KP,
Llorens L,
Abadía A, Aranda X
(1998) Photosynthesis and photoprotection in Quercus ilex resprouts after fire. Tree Physiology 18, 607–614.
| PubMed |
Flexas J,
Bota J,
Escalona JM,
Sampol B, Medrano H
(2002) Effects of drought on photosynthesis in gravepines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology 29, 1197–1207.
| Crossref | GoogleScholarGoogle Scholar |
Foley WJ,
Mc Ilwee A,
Lawler I,
Aragones L,
Woolnough AP, Berding N
(1998) Ecological applications of near infrared reflectance spectroscopy a tool for rapid, cost-effective prediction of the composition of plant and animal tissues and aspects of animal performance. Oecologia 116, 293–305.
| Crossref | GoogleScholarGoogle Scholar |
Garnier E,
Shipley B,
Roumet C, Laurent G
(2001) A standarized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology 15, 688–695.
| Crossref | GoogleScholarGoogle Scholar |
Genty B,
Briantais JM, Baker NR
(1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochemical Biophysical Acta 990, 87–92.
Gratani L, Bombelli A
(2000) Leaf anatomy, inclination, and gas exchange relationships in evergreen sclerophyllous and drought semideciduous shrub species. Photosynthetica 37, 573–585.
| Crossref | GoogleScholarGoogle Scholar |
Gulías J,
Flexas J,
Mus M,
Cifre J,
Lefi E, Medrano H
(2003) Relations between maximum leaf photosynthesis, nitrogen content and specific leaf area in Balearic endemic and non-endemic Mediterranean species. Annals of Botany 92, 215–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Houghton, JT ,
Ding, Y ,
Griggs, DJ ,
Noguer, M ,
van der Linden, PJ ,
Drai, X ,
Maskell, K ,
and
Johnson, CA (2001). ‘Climate change: the scientific basis’. Contribution of working group I in the third assessment report of intergovernmental panel on climate change. (Cambridge University Press: Cambridge)
Kruger EL, Reich PB
(1997) Response of hardwood regeneration to fire in mesic forest openings. II Leaf gas exchange, nitrogen concentration and water status. Canadian Journal of Forest Research 27, 1832–1840.
| Crossref | GoogleScholarGoogle Scholar |
Laing WA,
Ögren WL, Hegeman RH
(1974) Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2 and ribulose-1,5-diphosphate carboxylase. Plant Physiology 54, 678–685.
Loreto F,
Di Marco G,
Tricoli D, Sharkey TD
(1994) Measurements of mesophyll conductance, photosynthetic electron transport and alternative electron links of field grown wheat leaves. Photosynthesis Research 41, 397–403.
Lawlor DW, Cornic G
(2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell and Environment 25, 275–294.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Malanson GP, Trabaud L
(1988) Vigour of post-fire resprouting by Quercus coccifera L. Journal of Ecology 76, 351–365.
Martens, H ,
and
Naes, T (1989). ‘Multivariate calibration.’ (John Wiley and Sons: Chichester)
Mediavilla S,
Escudero A, Heilmeier H
(2001) Internal leaf anatomy and photosynthetic resource-use efficiency: interspecific and intraspecific comparisons. Tree Physiology 21, 251–259.
| PubMed |
Méthy M,
Damesin C, Rambal S
(1996) Drought and photosystem II activity in two Mediterranean oaks. Annals of Science 53, 255–262.
Meuret M,
Dardenne P,
Biston R, Poty O
(1993) The use of NIR in predicting nutritive value of Mediterranean tree and shrub foliage. Journal of Near Infrared Spectroscopy 1, 45–54.
Mouillot F,
Rambal S, Joffre R
(2002) Simulating climate change impacts on fire frequency and vegetation dynamics in a Mediterranean-type ecosystem. Global Change Biology 8, 423–437.
| Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü
(1999) Research review. Components of leaf mass per area — thickness and density — alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144, 35–47.
| Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü
(2001) Global-scale climatic controls of leaf mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
Nobel, PS (1991). ‘Physicochemical and environmental plant physiology.’ (Academic Press Inc.: San Diego)
Nogués S,
Munné-Bosch S,
Casadesús J,
López-Carbonell M, Alegre L
(2001) Daily time course of whole-shoot gas exchange rates in two drought-exposed Mediterranean shrubs. Tree Physiology 21, 51–58.
| PubMed |
Oechel, WC ,
and
Hastings, SJ (1983). The effects of fire on photosynthesis in chaparral resprout. In ‘Mediterranean-type ecosystems. Ecological studies Vol. 43’. pp. 274–285. (Springer-Verlag: Berlin)
Oxborough K, Baker NR
(1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components — calculation of qP and F′v / F′m without measuring F′o. Photosynthesis Research 54, 135–142.
| Crossref | GoogleScholarGoogle Scholar |
Peña-Rojas K,
Aranda X, Fleck I
(2004) Stomatal limitation to CO2 assimilation and down-regulation of photosynthesis in Quercus ilex L. resprouts under slowly-imposed drought. Tree Physiology 24, 813–822.
| PubMed |
Pereira, JS ,
and
Chaves, MM (1995). Plant responses to drought under climate change in Mediterranean-type ecosystems. In ‘Global change and Mediterranean-type ecosystems. Ecological studies Vol, 117’. pp. 140–160. (Springer-Verlag: Berlin)
Rascio A,
Cedola MC,
Toponi M,
Flagella Z, Wittmer G
(1990) Leaf morphology and water status changes in Tritricum durum under water stress. Physiologia Plantarum 78, 462–467.
| Crossref | GoogleScholarGoogle Scholar |
Reich PB,
Ellsworth DS,
Walters MB,
Vose JM,
Gresham C,
Volin JC, Bowman WD
(1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80, 1955–1969.
Retana J,
Riba J,
Castell C, Espelta JM
(1992) Regeneration by sprouting of holm-oak (Quercus ilex) stands exploited by selection thinning. Vegetatio 99–100, 355–364.
| Crossref | GoogleScholarGoogle Scholar |
Salleo S, Lo Gullo MA
(1990) Sclerophylly and plant water relations in three Mediterranean Quercus species. Annals of Botany 65, 259–270.
Saruwatari MW, Davis SD
(1989) Tissue water relations of three chaparral shrub species after wildfire. Oecologia 80, 303–308.
| Crossref | GoogleScholarGoogle Scholar |
Shenk JS, Westerhaus MO
(1991) Population definition, sample selection, and calibration procedures for near-infrared reflectance spectroscopy. Crop Science 31, 469–474.
Taylor JS,
Blake TJ, Pharis RP
(1982) The role of plant hormones and carbohydrates in the growth and survival of coppiced Eucalyptus seedlings. Physiologia Plantarum 55, 421–443.
Tenhunen, JD ,
Pearcy, RW ,
and
Lange, OL (1987). Diurnal variations in leaf conductance and gas exchange in natural environments. In ‘Stomatal function’. pp. 323–352. (Stanford University Press: Stanford)
Terashima I,
Miyazawa S-I, Hanba YT
(2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. Journal of Plant Research 114, 93–105.
van Soest, P ,
and
Robertson, J (1985). ‘Analysis of forages and fibrous foods: a laboratory manual for animal science.’ (Cornell University Publications: New York)
Witkowski ETF, Lamont BB
(1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88, 486–493.
