, Volume 17, Issue 4, pp 285–291 | Cite as

Photoprotection in evergreen Mediterranean plants during sudden periods of intense cold weather

  • J. I. García-PlazaolaEmail author
  • J. M. Olano
  • A. Hernández
  • J. M. Becerril
Original Article


The photoprotective responses to an abrupt period of exceptional cold weather were studied in several Mediterranean evergreen species with different ecological requirements. The same pattern of response was observed in most of the species with little change in hydrophilic antioxidants (ascorbate and glutathione) and the carotenoid pool, an increase in the content of α -tocopherol, and a night retention of de-epoxidised xanthophylls (antheraxanthin and zeaxanthin). The accumulation of these xanthophylls correlated with a sustained decrease in maximal photochemical efficiency (F v/F m). This reduction in the rate of electron transport would reduce the production of superoxide in photosystem I, as well as the subsequent hydrogen peroxide and hydroxyl radical. Thereby if any transitory photooxidative stress is produced under these conditions it should be due mainly to the formation of singlet oxygen by triplet excited chlorophyll within the antenna. Since α-tocopherol is the main scavenger of singlet oxygen and lipid peroxy radicals, the large increase of this antioxidant within the species could be enough to compensate for the higher degree of photooxidative stress, playing an essential role in the survival of vegetation during the incidence of exceptional cold fronts in the Mediterranean region.


α-Tocopherol Antioxidants Photooxidative stress Xanthophyll cycle 



A. Hernández received a postdoctoral fellowship from the Department of Education of the Basque Government. This research was supported by research grant AGL 2001–1131 from the Ministry of Science and Technology of Spain. We also thank to José Antonio Aranda from the Basque Government for meteorological data.


  1. Adams WW, Demmig-Adams B, Verhoeven AS, Baker DH (1994) 'Photoinhibition' during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–246Google Scholar
  2. Adams WW, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation upon growth form and light environment during the winter. Photosynth Res 67:51–62Google Scholar
  3. Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles. Plant Physiol 98:501–508Google Scholar
  4. Burton GW and Ingold KU (1984) β-carotene: an unusual type of lipid antioxidant. Science 224:569–573Google Scholar
  5. Esterbauer H, Grill D (1978) Seasonal variation of glutathione and glutathione reductase in needles of Picea abies. Plant Physiol 61:119–121Google Scholar
  6. García-Plazaola JI, Becerril JM (1999) A rapid HPLC method to measure lipophylic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 10:307–313CrossRefGoogle Scholar
  7. García-Plazaola JI, Artetxe U, Duñabeitia MK, Becerril JM (1999) Role of photoprotective systems of holm-oak (Quercus ilex) in the adaptation to winter conditions. J Plant Physiol 155:625–630Google Scholar
  8. García-Plazaola JI, Hernández A, Becerril JM (2000) Photoprotective responses to winter stress in evergreen Mediterranean ecosystems. Plant Biol 2:530–535Google Scholar
  9. Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proc Natl Acad Sci USA 97:11098–11101PubMedGoogle Scholar
  10. Griffith OW (1980) Glutathione and glutathione disulfide. Anal Biochem 106:207–212PubMedGoogle Scholar
  11. Groom QJ, Baker NR, Long SP (1991) Photoinhibition of holly (Ilex aquifolium) in the field during the winter. Physiol Plant 83:585–590Google Scholar
  12. Guy CL (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu Rev Plant Phys Plant Mol Biol 41:187–223CrossRefGoogle Scholar
  13. Kyparissis A, Drilias P, Manetas Y (2000) Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Aust J Plant Physiol 27:265–272Google Scholar
  14. Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst 134:279–295Google Scholar
  15. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis. Testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24Google Scholar
  16. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  17. Leipner J; Franchebound Y; Stamp P (1999) Effect of growing season on the photosynthetic apparatus and leaf antioxidative defenses in two maize genotypes of different chilling tolerance. Environ Exp Bot 42:129–139CrossRefGoogle Scholar
  18. McKersie DD, Desker Y (1994) Chilling stress. In: McKersie BD, Leshem YY (eds) Stress and stress coping in cultivated plants. Kluwer Academic, Dordrecht, pp 79–103Google Scholar
  19. Minkov YN, Jahoubjan GT, Denev YD, Toneva VT (1999) Photooxidative stress in higher plants. In: Pessaraki M (ed) Handbook of plants and crop stress. Dekker, New York, pp 499–526Google Scholar
  20. Mitrakos (1982) A theory for Mediterranean plant life. Acta Oecol Plant 1:234–252Google Scholar
  21. Müller P, Li X-P, Niyogi K (2001) Non- photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedGoogle Scholar
  22. Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21:31–57CrossRefGoogle Scholar
  23. Munné-Bosch S, Schwarz K, Alegre L (1999) Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. Plant Physiol 121:1047–1052PubMedGoogle Scholar
  24. Nageswara RR, Madamanchi A, Hausladen RG, Alscher RG, Amundson, Fellows S (1991) Seasonal changes in antioxidants in red spruce (Picea rubens Sarg.) from three field sites in northeastern United States. New Phytol 118:331–338Google Scholar
  25. Oberhuber W, Bauer H (1991) Photoinhibition of photosynthesis under natural conditions in ivy (Hedera helix L.) growing in an understory of deciduous trees. Planta 185:545–553Google Scholar
  26. Olivera G, Peñuelas J (2001) Allocation of absorbed light energy into photochemistry and dissipation in a semi-deciduous and an evergreen Mediterranean woody species during winter. Aust J Plant Physiol 28:471–480Google Scholar
  27. Polle A, Rennenberg H (1994) Photooxidative stress in trees. In: Foyer CH; Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defence systems in plants. CRC, London, pp 199–218Google Scholar
  28. Tausz M, Hietz P, Briones O (2001) The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of a Mexican cloud forest. Aust J Plant Physiol 28:1–9Google Scholar
  29. Ter Braak CJR, Smilauer P (1997) Canoco for Windows version 4.0. Centre for Biometry Wagenigen, The NetherlandsGoogle Scholar
  30. Terradas J, Savé R (1992) The influence of summer and winter stress and water relationships on the distribution of Quercus ilex L. Vegetatio 99–100:137–145Google Scholar
  31. Treitach, Bolognini G, Rondi A (1997) Photosynthetic activity of Quercus ilex at the extremes of a transect between Mediterranean and submediterranean vegetation (Trieste-NE Italy). Flora 192:369–378Google Scholar
  32. 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 96:567–576CrossRefGoogle Scholar
  33. 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 29:999–1011CrossRefGoogle Scholar
  34. Wise RR, Naylor AW (1987) Chilling-anhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigment and endogenous antioxidants. Plant Physiol 83:278–282Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • J. I. García-Plazaola
    • 1
    Email author
  • J. M. Olano
    • 2
  • A. Hernández
    • 1
  • J. M. Becerril
    • 1
  1. 1.Department of Plant Biology and EcologyUniversidad del País Vasco-EHUBilbaoSpain
  2. 2.Área de Biología Vegetal, Departamento de Ciencias AgroforestalesEscuela de Ingenierías AgrariasSoriaSpain

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