, Volume 42, Issue 3, pp 399–407 | Cite as

Seasonal Differences in Photochemical Efficiency and Chlorophyll and Carotenoid Contents in Six Mediterranean Shrub Species under Field Conditions

  • F. Ain-Lhout
  • M.C. Díaz Barradas
  • M. Zunzunegui
  • H. Rodríguez
  • F. García Novo
  • M.A. Vargas


The effects of summer and winter stress on the chlorophyll and carotenoid contents and photosystem 2 efficiency were examined in six Mediterranean scrub species. These six species belong to two different plant functional types: drought semi-deciduous (Halimium halimifolium L., Rosmarinus officinalis L., Erica scoparia L.) and evergreen sclerophylls (Juniperus phoenicea L., Pistacia lentiscus L., Myrtus communis L.). Two sites with different water availability were chosen. In the xerophytic site, despite they belong to two different functional types, R. officinalis and J. phoenicea showed a similar response. These were the most affected species in summer. H. halimifolium showed optimal values of Fv/Fm and non-significant seasonal changes in xanthophyll content. In the mesic site, E. scoparia and M. communis were apparently the most affected species by winter climatic conditions. P. lentiscus presented a pattern similar to H. halimifolium, except for elevated F0 values. In all the studied species, lutein plus zeaxanthin content was negatively correlated with Fv/Fm in summer and with leaf water potential, thus indicating that the thermal dissipation of energy was a general pattern for all species. Under stress, plant response is more species-specific than dependent on its functional type.

carotenoids chlorophyll fluorescence photoinhibition photosystem 2 sclerophyllous plants semi-deciduous plants water stress xanthophyll cycle 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adams, W.W., III, Demmig-Adams, B.: Carotenoid com-position and down regulation of photosystem II in three coni-fer species during the winter.-Physiol. Plant. 92: 451–458, 1994.Google Scholar
  2. Adams, W.W., III, Demmig-Adams, B.: The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter.-Plant, Cell Environ. 18: 117–127, 1995.Google Scholar
  3. Adams, W.W., III, Demmig-Adams, B., Verhoeven, A.S., Baker, D.H.: Photoinhibition during winter stress: Involve-ment of sustained xanthophyll cycle-dependent energy dissi-pation.-Aust. J. Plant Physiol. 22: 261–276, 1994.Google Scholar
  4. Allier, C.F., González Bernáldez, F., Ramírez Díaz, L.: Ecologi-cal map of the Reserva Biológica de Doñana.-División de Ciencias del CSIC, Estación Biológica de Doñana, Sevilla 1974.Google Scholar
  5. Bilger, W., Björkman, O.: Role of the xanthophyll cycle in pho-toprotection elucidated by measurements of light-induced ab-sorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis.-Photosynth. Res. 25: 173–185, 1990.Google Scholar
  6. Björkman, O., Demmig-Adams, B.: Regulation of photo-synthetic light energy capture, conversion, and dissipation in leaves of higher plants.-In: Schulze, E.D., Caldwell, M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17–47. Springer, Berlin 1994.Google Scholar
  7. Brüggemann, W., Koroleva, O.Y.: Chilling sensitivity of viola-xanthin deepoxidation inhibits the development of energy-de-pendent chlorophyll fluorescence quenching in vivo.-Plant Physiol. Biochem. 33: 251–259, 1995.Google Scholar
  8. Demmig, B., Björkman, O.: Comparison of the effect of exces-sive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants.-Planta 171: 171–184, 1987.Google Scholar
  9. Demmig, B., Winter, K., Krüger, A., Czygan, F.-C.: Photo-inhibition and zeaxanthin formation in intact leaves. A pos-sible role of the xanthophylls cycle in the dissipation of ex-cess light energy.-Plant Physiol. 84: 218–224, 1987.Google Scholar
  10. Demmig, B., Winter, K., Krüger, A., Czygan, F.-C.: Zeaxanthin and the heat dissipation of excess light energy in Nerium oleander exposed to a combination of high light and water stress.-Plant Physiol. 87: 17–24, 1988.Google Scholar
  11. Demmig-Adams, B., Adams, W.W., III: Carotenoid composition in sun and shade leaves of plants with different life forms.-Plant Cell Environ. 15: 411–419, 1992a.Google Scholar
  12. Demmig-Adams, B., Adams, W.W., III: Photoprotection and other responses of plants to high light stress.-Annu. Rev. Plant Physiol. Plant mol. Biol. 43: 599–626, 1992b.Google Scholar
  13. Demmig-Adams, B., Adams, W.W., III: Xanthophyll cycle and light stress in nature: uniform response to excess direct sun-light among higher plant species.-Planta 98: 460–470, 1996.Google Scholar
  14. Demmig-Adams, B., Adams, W.W., III, Winter, K., Meyer, A., Schreiber, U., Pereira, J., Krüger, A., Czygan, F.-C., Lange, O.L.: Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthetic capacity, and carotenoid composition during the midday depression of net CO2 uptake in Arbutus unedo growing in Portugal.-Planta 177: 377–387, 1989.Google Scholar
  15. Demmig-Adams, B., Gilmore, A., Adams, W.W., III: In vivo functions of carotenoids in higher plants.-FASEB J. 10: 403–412, 1996.Google Scholar
  16. Díaz Barradas, M.C., García Novo, F.: [Light modification and extinction through the canopy of four scrub species in Doñana National Park.]-Monogr. Inst. piren. Ecol. 4: 503–516, 1988. [In Span.]Google Scholar
  17. Díaz Barradas, M.C., Zunzunegui, M., García Novo, F.: Auto-ecological traits of Halimium halimifolium in contrasting habitats under a Mediterranean type climate.-Folia geobot. 34: 189–208, 1999.Google Scholar
  18. Epron, D., Dreyer, E., Breda, N.: Photosynthesis of oak trees (Quercus petraea (Matt.) Liebl.) during drought under field conditions: diurnal course of net CO2 assimilation and photo-chemical efficiency of photosystem II.-Plant Cell Environ. 15: 809–820, 1992.Google Scholar
  19. Faria, T., García-Plazaola, J.L., Abadia, A., Pereira, J.S., Chaves, M.M.: Diurnal changes in photoprotective mecha-nisms in leaves of cork oak (Quercus suber) during summer.-Tree Physiol. 16: 115–123, 1996.Google Scholar
  20. Faria, T., Silvério, D., Breia, E., Cabral, R., Abadia, A., Abadia, J., Pereira, J.S., Chaves, M.M.: 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, 1998.Google Scholar
  21. García Novo, F.: The ecosystem of Doñana National Park.-In: García Novo, F., Crawford, R.M.M., Díaz Barradas, M.C. (ed.): The Ecology and Conservation of European Dunes. Pp. 97–116. Universidad de Sevilla, Sevilla 1997.Google Scholar
  22. García Novo, F., Merino, J.: Pattern and process in the dune system of the Doñana National Park, Southwestern Spain.-In: van der Maarel, E. (ed.): Dry Coastal Ecosystems-Gene-ral Aspects. Pp. 453–468. Elsevier, Amsterdam 1997.Google Scholar
  23. García-Plazaola, J.I., Faria, T., Abadia, A., Chaves, M.M., Pereira, J.S.: Seasonal changes in xanthophyll compositionand photosynthesis of cork oak (Quercus suber L.) leaves under Mediterranean climate.-J. exp. Bot. 48: 1667–1674, 1997.Google Scholar
  24. Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron trans-port and quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 990: 87–92, 1989.Google Scholar
  25. Gill, D.S., Mahall, B.E.: Quantitative phenology and water rela-tions of an evergreen and a deciduous chaparral shrub.-Ecol. Monogr. 56: 127–143, 1986.Google Scholar
  26. Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-de-pendent photoprotection in higher plant chloroplasts and leaves.-Physiol. Plant. 99: 197–209, 1997.Google Scholar
  27. Gilmore, A.M., Yamamoto, H.Y.: Zeaxanthin formation and en-ergy-dependent fluorescence quenching in pea chloroplasts under artificially mediated linear and cyclic electron transport.-Plant Physiol. 96: 635–643, 1991.Google Scholar
  28. Gilmore, A.M., Yamamoto, H.Y.: Linear models relating xan-thophylls and lumen acidity to non-photochemical fluores-cence quenching. Evidence that antheraxanthin explains zea-xanthin-independent quenching.-Photosynth. Res. 35: 67–78, 1993.Google Scholar
  29. Griffiths, H., Maxwell, K.: In memory of C. S. Pittendrigh: Does exposure in forest canopies relate to photoprotective strategies in epiphytic bromeliads?-Funct. Ecol. 13: 15–23, 1999.Google Scholar
  30. Hendry, G.A.F., Houghton, J.D., Brown, S.B.: The degradation of chlorophyll-a biological enigma.-New Phytol. 107: 255–302, 1987.Google Scholar
  31. Herrera, C.: [Morphological and functional types of plants of Mediterranean matorral in Spain.]-Studia oecol. 5: 23–34, 1984. [In Span.]Google Scholar
  32. Herrera, C.: Historical effects and sorting processes as explana-tions for contemporary ecological patterns: character syndro-mes in Mediterranean woody plants.-Amer. Natural. 140: 421–446, 1992.Google Scholar
  33. Hurry, V.M., Huner, N.P.A.: Effect of cold hardening on sen-sitivity of winter and spring wheat leaves to short-term photo-inhibition and recovery of photosynthesis.-Plant Physiol. 100: 1283–1290, 1992.Google Scholar
  34. Jung, S.Y., Steffen, K.L.: Influence of photosynthetic photon flux densities before and during long-term chilling on xantho-phyll cycle and chlorophyll fluorescence quenching in leaves of tomato (Lycopersicon hirsutum).-Physiol. Plant. 100: 958–966, 1997.Google Scholar
  35. Karavatas, S., Manetas, Y.: Seasonal patterns of photosystem II photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions.-Photosynthetica 36: 41–49, 1999.Google Scholar
  36. Koroleva, O.Y., Brüggemann, W., Krause, G.H.: Photo-inhibition, xanthophyll cycle and in vivo chlorophyll fluores-cence quenching of chilling-tolerant Oxyria digyna and chil-ling-sensitive Zea mays.-Physiol. Plant. 92: 577–584, 1994.Google Scholar
  37. Kyparissis, A., Drilias, P., Manetas, Y.: Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlo-rophylls) capacity in eight Mediterranean plant species be-longing to two different growth forms.-Aust. J. Plant Physiol. 27: 265–272, 2000.Google Scholar
  38. Kyparissis, A., Petropoulou, Y., Manetas, Y.: Summer survival of leaves in a soft-leaved shrub (Phlomis fructicosa L., Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll con-tents.-J. exp. Bot. 46: 1825–1831, 1995.Google Scholar
  39. Lange, O.L., Harley, P.C., Beyschlag, W., Tenhunen, J.D.: Gas exchange methods for characterizing the impact of stress on leaves.-In: Tenhunen, J.D., Catarino, F.M., Lange, O.L., Oechel, W.C. (ed.): Plant Response to Stress. Pp. 3–25. Springer-Verlag, Berlin-Heidelberg-New York-London-Paris-Tokyo 1987.Google Scholar
  40. Lichtenthaler, H.K.: Chlorophylls and carotenoids-pigments of photosynthetic biomembranes.-In: Colowick, S.P., Kaplan, N.O. (ed.): Methods in Enzymology. Vol. 148. Pp. 350–382. Academic Press, San Diego-New York-Berkeley-Boston-London-Sydney-Tokyo-Toronto 1987.Google Scholar
  41. Margalef, R.: [Ecology.].-Omega, Barcelona 1982. [In Span.] Maslova, T.G., Popova, L.A.: Adaptive properties of the plant pigment systems.-Photosynthetica 29: 193–203, 1993.Google Scholar
  42. Merino, J., García Novo, F., Sánchez Díaz, M.: Annual fluctua-tion of water potential in the xerophytic shrub of Doñana Bio-logical Reserve (Spain).-Oecol. Plant. 11: 1–11, 1976Google Scholar
  43. Merino, O., Villar, R., Martín, A., García, D., Merino, J.: Vege-tation response to climatic change in a dune ecosystem in Southern Spain.-In: Moreno, J.M., Oechel, W.C. (ed.): Glo-bal Change and Mediterranean Type Ecosystems. Pp. 225238. Springer-Verlag, Berlin 1995.Google Scholar
  44. Mínguez-Mosquera, M.I., Gandul-Rojas, B., Gallardo-Guerrero, M.L.: Rapid method of quantification of chlorophylls and ca-rotenoids in virgin olive oil by high-performance liquid chro-matography.-J. agr. Food Chem. 40: 60–63, 1992.Google Scholar
  45. Mitrakos, K.: A theory for Mediterranean plant life.-Acta oecol. 1: 245–252, 1980.Google Scholar
  46. Munné-Bosch, S., Alegre, L.: The xanthophyll cycle is induced by light irrespective of water status in field-grown lavender (Lavandula stoechas) plants.-Physiol. Plant. 108: 147–151, 2000a.Google Scholar
  47. Munné-Bosch, S., Alegre, L.: The significance of â-carotene, á-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants.-Aust. J. Plant Physiol. 27: 139–146, 2000b.Google Scholar
  48. Munné-Bosch, S., Alegre, L.: Changes in carotenoids, toco-pherols and diterpenes during drought and recovery, and the biological significance of chlorophyll loss in Rosmarinus of-ficinalis plants.-Planta 210: 925–931, 2000c.Google Scholar
  49. Muñoz Reinoso, J.C.: Sequential pattern in the stabilized dune of Doñana Biological Reserve (SW of Spain).-J. coast. Res. 17: 90–94, 2001.Google Scholar
  50. Núñez-Olivera, E., Martínez-Abaigar, J., Escudero, J.C.: Adapt-ability of leaves of Cistus ladanifer to widely varying envi-ronmental conditions.-Funct. Ecol. 10: 636–646, 1996.Google Scholar
  51. Oliveira, G., Peñuelas, J.: Comparative photochemical and phe-nomorphological 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, 2000.Google Scholar
  52. Powles, S.B.: Photoinhibition of photosynthesis induced by vis-ible light.-Annu. Rev. Plant Physiol. 25: 15–44, 1984.Google Scholar
  53. Scholander, P.F., Hammel, H.T., Bradstreet, E.D., Hemmingsen, E.A.: Sap pressure in vascular plants.-Science 148: 339–346, 1965.Google Scholar
  54. Schreiber, U., Hormann, H., Neubauer, C., Klughammer, C.: Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis.-Aust. J. Plant Physiol. 22: 209–220, 1995.Google Scholar
  55. Serrano, L., Toja, J.: Limnological description of four tempo-rary ponds in the Doñana National Park (SW, Spain).-Arch. Hydrobiol. 133: 497–516, 1995.Google Scholar
  56. Sobrado, M.A.: Drought resistance of tropical corn. 1. Leaf area and yield components in the field.-Maydica 35: 221–226, 1990.Google Scholar
  57. Thiele, A., Schirwitz, K., Winter, K., Krause, G.H.: Increased xanthophyll cycle activity and reduced D1 protein inactivation related to photoinhibition in two plant systems acclimated to excess light.-Plant Sci. 115: 237–250, 1996.Google Scholar
  58. Valladares, F., Pearcy, R.W.: Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia.-Plant Cell Environ. 20: 25–36. 1997.Google Scholar
  59. Verdu, M.: Ecological and evolutionary differences between Mediterranean seeders and resprouters.-J. Veget. Sci. 11: 265–268, 2000.Google Scholar
  60. Werner, C., Correia, O., Beyschlag, W.: Two different strategies of Mediterranean machia plants to avoid photoinhibitory da-mage by excessive radiation levels during summer drought.-Acta oecol. 20: 15–23, 1999.Google Scholar
  61. Werner, C., Ryel, R.J., Correia, O., Beyschlag, W.: Structural and functional variability within the canopy and its relevance for carbon gain and stress avoidance.-Acta oecol. 22: 129–138, 2001.Google Scholar
  62. Zunzunegui, M., Díaz Barradas, M.C., García Novo, F.: Vege-tation fluctuation in Mediterranean dune ponds in relation to rain fall variation and water extraction.-Appl. Veget. Sci. 1: 151–160, 1998.Google Scholar
  63. Zunzunegui, M., Díaz Barradas, M.C., García Novo, F.: Diffe-rent phenotypic response of Halimium halimifolium in relation to groundwater availability.-Plant Ecol. 148: 165-174, 2000.Google Scholar
  64. Zunzunegui, M., Fernández Baco, L., Díaz Barradas, M.C., García Novo, F.: Seasonal changes in photochemical effi-ciency in leaves of Halimium halimifolium, a Mediterranean semideciduous shrub.-Photosynthetica 37: 17–31, 1999.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • F. Ain-Lhout
    • 1
  • M.C. Díaz Barradas
    • 1
  • M. Zunzunegui
    • 1
  • H. Rodríguez
    • 2
  • F. García Novo
    • 1
  • M.A. Vargas
    • 2
  1. 1.Departamento de Biologíaxca Vegetal y EcologíaSpain
  2. 2.Instituto de Bioquímica Vegetal y FotosíntesisUniversidad Sevilla-CSICCentro de Investigaciones Científicas Isla de la CartujaSpain

Personalised recommendations