Skip to main content
SpringerLink
Log in

The effect of low temperatures on the photosynthetic apparatus of Quercus ilex subsp. ballota at its lower and upper altitudinal limits in the Iberian peninsula and during a single freezing-thawing cycle

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

We investigated the response of the photosynthetic apparatus during an episode of extreme low winter temperature in Quercus ilex subsp. ballota (Desf.) Samp., a typical Mediterranean evergreen species in the Iberian peninsula. Both plants in a woodland located at high altitude (1,177 m. a.s.l.) and potted plants obtained from acorns of the same populations grown at low altitude (225 m. a.s.l.) were analyzed. Net CO2 assimilation rate was negative and there was a marked decrease in photosystem II (PSII) efficiency during winter in leaves of the woodland population (high altitude individuals). These processes were accompanied by increases in non-photochemical quenching (NPQ) and in the de-epoxidated carotenoids within the xanthophyll cycle, mechanisms aimed to dissipate excess energy. In addition, these de-epoxidated carotenoids were largely preserved during the night. There was no chlorophyll bleaching during the winter, which suggests that leaves were not experiencing photoinhibitory damage. In fact, the net photosynthetic rate and the PSII efficiency recovered in spring. These changes were not observed, or were much more reduced, in individuals located at lower altitude after a few frosts. When the response to rapid temperature changes (from 20°C to −5°C and from −5°C to 20°C) was studied, it was found that the maximum potential PSII efficiency was fairly stable, ranging from 0.70 to 0.75. The rest of the photosynthetic parameters measured, actual and intrinsic PSII efficiency, photochemical and NPQ, responded immediately to the changes in temperature and, also, the recovery after cold events was practically immediate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abadía J, Abadía A (1993) Iron and plant pigments. In: Barton L, Hemming B (eds) Iron chelation in plants and soil microorganisms. Academic, San Diego, pp 327–344

    Google Scholar 

  • Abadía A, Gil E, Morales F, Montañés L, Monserrat G, Abadía J (1996) Marcescence and senescence in a submediterranean oak (Quercus subpyrenaica E.H. del Villar): photosynthetic characteristics and nutrient composition. Plant Cell Environ 19:685–694

    Google Scholar 

  • Adams WW, Demig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiol Plant 92:451–458

    Article  CAS  Google Scholar 

  • Adams WW, Demmig-Adams B (1995) The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant Cell Environ 18:117–127

    Google Scholar 

  • Allué Andrade JL (1990) Atlas Fitoclimático de España: Taxonomías. MAPA-INIA, Madrid

    Google Scholar 

  • Barbero M, Loisel R, Quèzel P (1992) Biogeography, ecology and history of Mediterranean Quercus ilex ecosystems. Vegetatio 99–100:19–34

    Google Scholar 

  • Belkhodja R, Morales F, Quílez R, López-Millán AF, Abadía A, Abadía J (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the photosystem II acceptor side. Photosynth Res 25:173–185

    Google Scholar 

  • Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185

    CAS  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Google Scholar 

  • Blondel J, Aronson J (1995) Biodiversity and ecosystems function in the Mediterranean basin: human and non-human determinants. In: Davis GW, Richardson DM (eds) Mediterranean type ecosystems. The function of biodiversity. Springer, Berlin Heidelberg New York, pp 43–119

    Google Scholar 

  • Butler WL. (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378

    Article  CAS  Google Scholar 

  • Corcuera L (2003) Respuesta al clima de distintas especies del género Quercus: Estructura y funcionamiento comparado. PhD thesis, University of Lérida, Spain

  • De las Rivas J, Abadía A, Abadía J (1989) A new reversed phase HPLC method resolving all major higher plant photosynthetic pigments. Plant Physiol 91:190–192

    Google Scholar 

  • Deltoro VI, Calatayud A, Morales F, Abadía A, Barreno E (1999) Changes in net photosynthesis, chlorophyll fluorescence and xanthophyll cycle interconversions during freeze-thaw cycles in the Mediterranean moss Leucodon sciuroides. Oecologia 120:499–505

    Article  Google Scholar 

  • Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171:171–184

    CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants. A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198:460–470

    CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Czygan FC (1989) Zeaxanthin and the induction and relaxation kinetics of the dissipation of excess excitation energy in leaves in 2% O2, 0% CO2. Plant Physiol 90:887–893

    CAS  Google Scholar 

  • Demmig-Adams B, Adams WW, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264

    Article  CAS  Google Scholar 

  • Faria T, Silvério D, Breia E, Cabral R, Abadía A, Abadía J, Pereira JS, Chaves MM (1998) Differences in the response of carbon assimilation to summer stress (water deficits, high light and temperature) in four Mediterranean tree species. Physiol Plant 102:419–428

    Article  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plant 92:696–717

    Article  CAS  Google Scholar 

  • García-López JM, Gonzalo-Jiménez J, Allue-Camacho C (2002) Caracterización fitoclimática de procedencias de encinar (Quercus ilex L. subsp. ballota (Desf.) Samp. y Quercus ilex L. subsp. ilex) en el centro-norte peninsular. Inv Agric Sist Rec For 11:77–96

    Google Scholar 

  • García-Plazaola JI, Faria T, Abadía J, Abadía A, Chaves MM, Pereira JS (1997) Seasonal changes in xanthophyll composition and photosynthesis of cork oak (Quercus suber L.) leaves under Mediterranean climate. J Exp Bot 48:1667–1674

    Article  Google Scholar 

  • García-Plazaola JI, Artetxe U, Becerril JM (1999a) Diurnal changes in antioxidant and carotenoid composition in the Mediterranean schlerophyll tree Quercus ilex (L) during winter. Plant Sci 143:125–133

    Article  Google Scholar 

  • García-Plazaola JI, Artetxe U, Duñabeitia MK, Becerril JM (1999b) Role of photoprotective systems of holm-oak (Quercus ilex) in the adaptation to winter conditions. J Plant Physiol 155:625–630

    Google Scholar 

  • García-Plazaola JI, Olano JM, Hernández A, Becerril JM (2003) Photoprotection in evergreen Mediterranean plants during sudden periods of intense cold weather. Trees 17:285–291

    Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 97:11098–11101

    Article  CAS  PubMed  Google Scholar 

  • Gilmore AM, Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynth Res 35:67–78

    CAS  Google Scholar 

  • González Rebollar JL (1996) Sistemas agrarios sostenibles en áreas marginales. In: Lasanta T, García Ruíz JM (eds) Erosión y Recuperación de Tierras en Areas Marginales. Instituto de Estudios Riojanos y Soc. Esp. Geomorfología, Logroño, pp 173–182

    Google Scholar 

  • González Rebollar JL, García-Alvarez A, Ibáñez JJ (1995) A mathematical model for predicting the impact of climate changes on mediterranean plant landscapes. In: Zewer S, van Rompaey RSAR, Kok MTJ, Berk MM (eds) Climate change research: evaluation and policy implications. Elsevier, Amsterdam, pp 757–762

    Google Scholar 

  • Gratani L (1993) Response to microclimate of morphological leaf attributes, photosynthetic and water relations of evergreen sclerophyllous species. Photosynthetica 29:573–582

    Google Scholar 

  • Gratani L (1996) Leaf and shoot growth dynamics of Quercus ilex L. Acta Oecol 17:17–27

    Google Scholar 

  • Groom QJ, Baker NR, Long SP (1991) Photoinhibition of holly (Ilex aquifolium) in the field during the winter. Physiol Plant 83:585–590

    Article  Google Scholar 

  • Harbison J, Genty B, Baker NR (1989) Relationship between the quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol 90:1029–1034

    CAS  Google Scholar 

  • Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39

    CAS  Google Scholar 

  • Ibáñez JJ, González Rebollar JL, García Alvarez A, Saldaña A (1997) Los Geosistemas mediterráneos en el espacio y en el tiempo. In: El paisaje mediterráneo a través del espacio y del tiempo. Implicaciones en la desertificación. Geoforma, Madrid, pp 27–130

  • IPCC (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Jiménez-Sancho MP, Díaz-Fernández PM, Iglesias S, De Tuero, De Reyna M, Gil Sánchez L (1996) Las regiones de procedencia de Quercus ilex L. en España. Ed. ICONA

  • Krause G, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Lamontagne M, Bigras FJ, Margolis HA (2000) Chlorophyll fluorescence and CO2 assimilation of black spruce seedlings following frost in different temperature and light conditions. Tree Physiol 20:249–255

    PubMed  Google Scholar 

  • Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst 134:279–295

    Google Scholar 

  • Llorens L, Aranda X, Abadía A, Fleck I (2002) Variations in Quercus ilex chloroplast pigment content during summer stress: involvement in photoprotection according to principal component analysis. Funct Plant Biol 29:81–88

    Article  CAS  Google Scholar 

  • Lo Gullo MA, Salleo S (1993) Different vulnerabilities of Quercus ilex to freeze- and summer drought-induced xylem embolism: an ecological interpretation. Plant Cell Environ 16:511–519

    Google Scholar 

  • Merino J, Field C, Mooney HA (1982) Construction and maintenance costs of mediterranean-climate evergreen and deciduous leaves. I. Growth and CO2 exchange analysis. Oecologia 53:208–213

    Google Scholar 

  • Mitrakos K. (1980) A theory for Mediterranean plant life. Acta Oecol/Oecol Plant 15:245–252

    Google Scholar 

  • Morales F, Abadía A, Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97:886–893

    CAS  Google Scholar 

  • Morales F, Abadía A, Belkhodja R, Abadía J (1994) Iron deficiency-induced changes in the photosynthetic pigment composition of field-grown pear (Pyrus communis L.) leaves. Plant Cell Environ 17:1153–1160

    CAS  Google Scholar 

  • Morales F, Abadía A, Abadía J, Montserrat G, Gil-Pelegrín E (2002) Trichomes and photosynthetic pigment composition changes: responses of Quercus ilex subsp. ballota (Desf.) Samp. and Quercus coccifera L. to Mediterranean stress conditions. Trees 16:504–510

    Article  CAS  Google Scholar 

  • Nardini A, Salleo S, Lo Gullo MA, Pitt F (2000) Different responses to drought and freeze stress of Quercus ilex L. growing along a latitudinal gradient. Plant Ecol 148:139–147

    Article  Google Scholar 

  • Nishio JN (2000) Why are higher plants green? Evolution of the higher plant photosynthetic pigment complement. Plant Cell Environ 23:539–548

    Article  CAS  Google Scholar 

  • Ogaya R, Peñuelas J (2003) Comparative seasonal gas exchange and chlorophyll fluorescence of two dominant woody species in a holm oak forest. Flora 198:132–141

    Google Scholar 

  • Oliveira G, Peñuelas J (2000) Comparative photochemical and phenomorphological responses to winter stress of an evergreen (Quercus ilex L.) and a semi-deciduous (Cistus albidus L.) Mediterranean woody species. Acta Oecol 21:97–107

    Article  Google Scholar 

  • Onate-Rubalcaba JJ, Pou-Royo A (1995) Climatic changes in western Spain. Are there any correlations with phytoclimates? Int J Biometeorol 39:22–28

    Google Scholar 

  • Öquist G, Huner NPA (1993) Frost-hardening induced resistance to photoinhibition of photosynthesis in winter rye depends on an increased capacity of photosynthesis. Planta 189:150–156

    Google Scholar 

  • Öquist G, Ogren E (1985) Effects of winter stress on photosynthetic electron transport and energy distribution between the two photosystems of pine as assayed by chlorophyll fluorescence kinetics. Photosynth Res 7:19–30

    Google Scholar 

  • Piñol J, Terradas J, Lloret F (1998) Climate warming, wildfire hazard, and wildfire occurrence in coastal eastern Spain. Clim Change 38:345–357

    Article  Google Scholar 

  • Pons A, Suc JP (1980) Lés témoignages de structures de végétation Méditerranéennes dan le passée antérieur à l’action de l’home. Natur Monsp HS:69–78

    Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44

    Article  CAS  Google Scholar 

  • Scharberg PG, Shane JB, Hawley GJ, Strimbeck GR, DeHayes DH, Cali PF, Donnelly JR (1996) Physiological changes in red spruce seedlings during a simulated winter thaw. Tree Physiol 16:567–574

    PubMed  Google Scholar 

  • Schöner S, Krause H (1990) Protective systems against active oxygen species in spinach: response to cold acclimation in excess light. Planta 180:383–389

    Google Scholar 

  • Somersalo S, Krause GH (1990) Photoinhibition at chilling temperatures and effects of freezing stress on cold acclimated spinach leaves in the field. A fluorescence study. Physiol Plant 79:617–622

    Article  Google Scholar 

  • Tretiach M, Bolognii G, Rondi A (1997) Photosynthetic activity of Quercus ilex at the extremes of a transect between mediterranean and submediterranean vegetation (Trieste, NE Italy). Flora 192:369–378

    Google Scholar 

  • Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence in plant stress physiology. Photosynth Res 25:147–150

    Google Scholar 

  • Verhoeven AS, Adams WW, Demmig-Adams B (1996) Close relationship between the state of xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiol Plant 96:567–576

    Article  CAS  Google Scholar 

  • Walter H (1977) Zonas de vegetación y clima. Omega, Barcelona

    Google Scholar 

  • Werner C, Correia O, Beyschlag W (2002) Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. Funct Plant Biol 29:999–1011

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by INIA SC96-086 and 1FD97-0911-C03-01 (Subpr.1) projects, and an INIA grant to L.C.

Author information

Authors and Affiliations

  1. Unit of Forest Resources, C.I.T.A. de Aragón, Apdo. 727, 50080, Saragossa, Spain

    L. Corcuera & E. Gil-Pelegrin

  2. Department of Plant Nutrition, Aula Dei Experimental Station, CSIC, Apdo. 202, 50080, Saragossa, Spain

    F. Morales & A. Abadia

Authors
  1. L. Corcuera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Abadia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Gil-Pelegrin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Gil-Pelegrin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Corcuera, L., Morales, F., Abadia, A. et al. The effect of low temperatures on the photosynthetic apparatus of Quercus ilex subsp. ballota at its lower and upper altitudinal limits in the Iberian peninsula and during a single freezing-thawing cycle. Trees 19, 99–108 (2005). https://doi.org/10.1007/s00468-004-0368-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-004-0368-1

Keywords

Search

Navigation