Plasticity of Photoprotective Mechanisms of Buxus sempervirens L. Leaves in Response to Extreme Temperatures

Abstract

Summer 2003 was unusually hot in Western Europe, with local droughts and an intense heatwave, that led to a massive damage in vegetation. Since high temperatures are supposed to generate photooxidative stress, we analysed photoprotective responses in leaves of the evergreen boxtree (Buxus sempervirens L.) during summer 2003. All the photoprotective compounds analysed (α-tocopherol, β-carotene, and xanthophylls cycle pigments) were simultaneously induced in parallel with a reduction in photochemical efficiency (Fv/Fm). To characterise these responses, we compared these data with other data obtained during cold stress periods (2003, 2005) and with an unstressful summer (2002). Photoprotective responses observed during the heatwave were also induced by low temperature stress, and in both situations, this effect was exacerbated by light. In parallel with such induction the accumulation of red retro-carotenoids and xanthophyll esters was also observed under unfavourable conditions, suggesting a photoprotective role for both groups of carotenoids. This is the first report showing that in any species (Buxus sempervirens L.), the same retro-carotenoids can be induced in response to winter and summer stress. Present results demonstrate that the same mechanisms are induced as response to sub- and supraoptimal temperatures and the plasticity of such responses plays a critical role in plant acclimation to extreme temperatures, an ability that is specially important in the context of any future climate warming.

Key words

Anhydroeschscholtzxanthin - boxtree - climate warming - heatwave - photoinhibition - red carotenoids - xanthophyll cycle.

References

• 1 Adams III., W. W., Demmig-Adams B., Rosentiel T. N., Brightwell A. K., Ebbert V.. Photosynthesis and photoprotection in overwintering plants.  Plant Biology. (2002);  4 545-557
• 2 Adams III., W. W., Zarter C. R., Ebbert V., Demmig-Adams B.. Photoprotective strategies of overwintering evergreens.  BioScience. (2004);  54 41-49
• 3 Badiani M., Paolacci A. R., Fusari A., D'Ovidio R., Scandalios J. G., Porceddu E., Sermanni G. G.. Non-optimal growth temperatures and antioxidants in the leaves of Sorghum bicolor (L.) Moench. II. Short-term acclimatization.  Journal of Plant Physiology. (1997);  151 409-442
• 4 Baker D. H., Adams III., W. W., Demmig-Adams B., Logan B. A., Verhoeven A. S., Smith S. D.. Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species growing in the Mojave Desert.  Plant, Cell and Environment. (2002);  25 95-103
• 5 Berry J., Björkman O.. Photosynthetic response and adaptation to temperature in higher plants.  Annual Review of Plant Physiology. (1980);  31 491-543
• 6 Bouvier F., Backhaus R. A., Camara B.. Induction and control of chromoplasts-specific carotenoid genes by oxidative stress.  Journal of Biological Chemistry. (1998);  273 30651-30659
• 7 Bungard R. A., Ruban A. V., Hibberd J. M., Press M. C., Horton P., Scholes J. D.. Unusual carotenoid composition and a new type of xanthophyll cycle in plants.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 1135-1139
• 8 Ciais P., Reichstein M., Viovy N., Granier A., Ogée J., Allard V., Aubinet M., Buchmann N., Bernhofer C., Carrara A., Chevallier F., De Noblet N., Friend A. D., Friedlingstein P., Grünwald T., Heinesch B., Keronen P., Knohl A., Krinner G., Loustau D., Manca G., Matteucci G., Miglietta F., Ourcival J. M., Papale D., Pilegaard K., Rambal S., Seufert G., Soussana J. F., Sanz M. J., Schulze E. D., Vesala T., Valentini R.. Europe-wide reduction in primary productivity caused by heat and drought in 2003.  Nature. (2005);  437 529-533
• 9 Close D. C., Beadle C. L.. Xanthophyll-cycle dynamics and rapid induction of anthocyanin synthesis in Eucaliptus nitens seedlings transferred to photoinhibitory conditions.  Journal of Plant Physiology. (2003);  162 37-46
• 10 Decocq G., Bordier D., Wattez J. R., Racinet P.. A practical approach to assess the native status of a rare plant species: the controverse of Buxus sempervirens L. in northern France revisited.  Plant Ecology. (2004);  173 139-151
• 11 Demmig-Adams B., Adams W. W.. Photoprotection and other responses of plants to high light stress.  Annual Review of Plant Physiology and Plant Molecular Biology. (1992);  43 599-626
• 12 Demmig-Adams B., Adams W. W.. Chlorophyll and carotenoid composition in leaves of Euonymus kiautschovicus acclimated to different degrees of light stress in the field.  Australian Journal of Plant Physiology. (1996);  23 649-659
• 13 Demmig-Adams B., Adams W. W., Ebbert V., Logan B. A.. Ecophysiology of the xanthophyll cycle. Frank, H. A., Young, A. J., Britton, G., and Cogdell, R. J., eds. The Photochemistry of Carotenoids. Dordrecht, The Netherlands; Kluwer Academic Publishers (1999): 245-269
• 14 Diaz M., Ball E., Lüttge U.. Stress-induced accumulation of the xanthophyll rhodoxanthin in leaves of Aloe vera.  Plant Physiology and Biochemistry. (1990);  28 679-682
• 15 Fryer M. J.. The antioxidant effects of thylakoid vitamin E (α-tocopherol).  Plant, Cell and Environment. (1992);  15 381-392
• 16 García-Plazaola J. I., Becerril J. M.. A rapid HPLC method to measure lipophylic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols.  Phytochemical Analysis. (1999);  10 1-7
• 17 García-Plazaola J. I., Hernández A., Becerril J. M.. Photoprotective responses to winter stress in evergreen mediterranean ecosystems.  Plant Biology. (2000);  2 530-535
• 18 García-Plazaola J. I., Becerril J. M.. Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis.  Australian Journal of Plant Physiology. (2001);  28 225-232
• 19 García-Plazaola J. I., Hernández A., Becerril J. M.. Antioxidant and pigment composition during autumnal leaf senescence in woody deciduous species differing in their ecological traits.  Plant Biology. (2003);  5 1-10
• 20 García-Plazaola J. I., Hormaetxe K., Hernández A., Olano J. M., Becerril J. M.. The lutein epoxide cycle in vegetative buds of woody plants.  Functional Plant Biology. (2004);  31 815-823
• 21 Ghoul H., Montpied P., Epron D., Ksontini M., Hanchi B., Dreyer E.. Thermal optima of photosynthetic functions and thermostability of photochemistry in cork oak seedlings.  Tree Physiology. (2003);  23 1031-1039
• 22 Groom P. K., Larmont B. B., Leighton S., Leighton P., Burrows C.. Heat damage in sclerophylls is influenced by their leaf properties and plant environment.  Ecoscience. (2004);  11 94-101
• 23 Han Q., Katahata S., Kakubari Y., Mukai Y.. Seasonal changes in the xanthophyll cycle and antioxidants in sun-exposed and shaded parts of crown of Cryptomeria japonica in relation to rhodoxanthin accumulation during cold acclimatization.  Tree Physiology. (2004);  24 609-616
• 24 Hanson D. T., Sharkey T. D.. Effect of growth conditions on isoprene emission and other thermotolerance-enhancing compounds.  Plant, Cell and Environment. (2001);  24 929-936
• 25 Havaux M., Tardy F.. Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments.  Planta. (1996);  198 324-333
• 26 Havaux M., Dall -Osto L., Cuine S., Giuliano G., Bassi R.. The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana.  Journal of Biological Chemistry. (2004);  279 13878-13888
• 27 Hormaetxe K., Hernández A., Becerril J. M., García-Plazaola J. I.. Role of red carotenoids in photoprotection during winter acclimatization in Buxus sempervirens leaves.  Plant Biology. (2004);  6 325-332
• 28 Hormaetxe K., Becerril J. M., Fleck I., Pinto M., García-Plazaola J. I.. Functional role of (retro)-carotenoids as passive light filters in the leaves of Buxus sempervirens L.: increased protection of photosynthetic tissues?.  Journal of Experimental Botany. (2005 a);  56 2629-2636
• 29 Hormaetxe K., Esteban R., Becerril J. M., García-Plazaola J. I.. Dynamics of the α-tocopherol pool as affected by external (environmental) and internal (leaf age) factors in Buxus sempervirens leaves.  Physiologia Plantarum. (2005 b);  125 333-344
• 30 Hirayama O., Nakamura K., Hamada S., Kobayasi Y.. Singlet oxygen quenching ability of naturally occurring carotenoids.  Lipids. (1994);  29 149-150
• 31 Ida K.. Eco-physiological studies on the response of taxodiaceous conifers to shading, with special reference to the behaviour of leaf pigments I. Distribution of carotenoids in green and autumnal reddish brown leaves of gymnosperms.  Botanical Magazine Tokyo. (1981);  94 41-54
• 32 Ida K., Masamoto K., Maoka T., Fujiwara Y., Takeda S., Hasegawa E.. The leaves of the common box, Buxus sempervirens (Buxaceae), become red as the level of a red carotenoid, anhydroeschscholtzxanthin, increases.  Journal of Plant Research. (1995);  108 369-376
• 33 Ladjal M., Epron D., Ducrey M.. Effects of drought preconditioning on thermolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings.  Tree Physiology. (2000);  20 1235-1241
• 34 Larcher W.. Temperature stress and survival ability of Mediterranean sclerophyllous plants.  Plant Biosystems. (2000);  134 279-295
• 35 Larkindale J., Huang B.. Thermotolerance and antioxidant systems in Agrostis stolonifera: involvementy of salicylic acid, abscisic acid, calcium, hydrogen peroxide and ethylene.  Journal of Plant Physiology. (2004);  161 405-413
• 36 Leuzinger S., Zotz G., Asshoff R., Körner C.. Responses of deciduous forests trees to severe drought in Central Europe.  Tree Physiology. (2005);  25 641-650
• 37 Manetas Y., Drinia A., Petropoulou Y.. High contents of anthocianins in young leaves are correlated with low pools of xanthophyll cycle components and low risk of photoinhibition.  Photosynthetica. (2002);  40 349-354
• 38 Matsubara S., Morosinotto Y., Bassi R., Christian A. L., Fischer-Schliebs E., Lüttge U., Orthen B., Franco A. C., Scarano F. R., Förster B., Pogson B. J., Osmond C. B.. Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae.  Planta. (2003);  217 868-879
• 39 Merzlyak M., Solovchenko A., Pogosyan S.. Optical properties of rhodoxanthin accumulated in Aloe arborescens Mill. Leaves under high-light stress with special reference to its photoprotective function.  Photochemical and Photobiological Sciences. (2005);  4 333-340
• 40 Munné-Bosch S., Peñuelas J., Asensio D., Llusiá J.. Airborne ethylene may alter antioxidant protection and reduce tolerance of holm oak to heat and drought stress.  Plant Physiology. (2004);  136 2937-2947
• 41 Paolacci A. R., Badiani M., D'Annibale A., Fusari A., Matteucci G.. Antioxidants and photosynthesis in the leaves of Triticum durum Desf. seedlings acclimated to non-stressing high temperature.  Journal of Plant Physiology. (1997);  150 381-387
• 42 Peñuelas J., Munné-Bosch S.. Isoprenoids: an evolutionary pool for photoprotection.  Trends in Plant Science. (2005);  10 166-169
• 43 Steyn W. J., Wand S. J. E., Holcroft D. M., Jacobs G.. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection.  New Phytologist. (2002);  155 349-361
• 44 Stott A., Stone D. A., Allen M. R.. Human contribution to the European heatwave of 2003.  Nature. (2004);  432 610-614
• 45 Steinbrenner J., Linden H.. Regulation of two carotenoid biosynthesis genes coding for phytoene synthase and carotenoid hydroxylase during stress-induced astaxanthin formation in the green alga Haematococcus pluvialis.  Plant Physiology. (2001);  125 810-817
• 46 Tausz M., Wonisch A., Grill D., Morales D., Jiménez M. S.. Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation.  Journal of Experimental Botany. (2003);  387 1505-1510
• 47 Thayer S. S., Björkman O.. Leaf xanthophyll content and composition in sun and shade determined by HPLC.  Photosynthesis Research. (1990);  23 331-343
• 48 Torzillo G., Goksan Y., Faraloni C., Kopecky J., Masojidek J.. Interplay between photochemical activities and pigment composition in an outdoor culture of Haematococcus pluvialis during the shift from the green to red stage.  Journal of Applied Phycology. (2003);  15 127-136
• 49 Valladares F., Chico J. M., Aranda I., Balaguer L., Dizengremel P., Manrique E., Dreyer E.. Greater high light seedling tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity.  Trees. (2002);  16 395-403
• 50 Wang B., Zarka A., Trebst A., Boussiba S.. Astaxanthin accumulation in Haematococcus pluvialis (Chlorophyceae) as an active photoprotective process under high irradiance.  Journal of Phycology. (2002);  39 1116-1124
• 51 Weger H. G., Silim S. N., Guy R. D.. Photosynthetic acclimatization to low-temperature by western red cedar seedlings.  Plant, Cell and Environment. (1993);  16 711-717
• 52 Werner C., Correia O., Beyschlag W.. Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem.  Functional Plant Biology. (2002);  29 999-1011
• 53 Williams E. L., Hovenden M. J., Close D. C.. Strategies of light energy utilisation, dissipation and attenuation in six co-occurring alpine heath species in Tasmania.  Functional Plant Biology. (2003);  30 1205-1218
• 54 Ytterberg A. J., Peltier J. B., van Wijk K. J.. Protein profiling of platoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes.  Plant Physiology. (2006);  140 984-997
• 55 Zarter C. R., Adams W. W., Ebbert V., Adamska I., Jansson S., Demmig-Adams B.. Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment.  Plant, Cell and Environment. (2006);  29 869-878

Editor: W. W. Adams III