Antioxidant and Pigment Composition during Autumnal Leaf Senescence in Woody Deciduous Species Differing in their Ecological Traits

Abstract

Photoprotection mechanisms have been studied during autumnal senescence in sun and shade leaves of woody plants with different ecological characteristics and senescence patterns. Three of them belonging to the same family, Betulaceae: the shade-intolerant and early successional species (Betula alba L.), the shade-tolerant and late successional species (Corylus avellana L.), and an N-fixing tree with low N resorption efficiency (Alnus glutinosa L.). The other two species: a shade-intolerant (Populus tremula L.) and a shade-tolerant (Cornus sanguinea L.), were chosen because of their ability to accumulate anthocyanins during autumnal leaf senescence. The study of plants with different ecological strategies allowed us to establish general trends in photoprotection mechanisms during autumnal senescence, when nutrient remobilisation occurs, but also during whole leaf ontogeny. We have not found a clear relationship between shade tolerance and the level of photoprotection; the main difference between both groups of species being the presence of α-carotene in shade leaves of shade-tolerant species. Preceding autumn, nitrogen resorption started in mid-summer and occurred in parallel with a slight and continuous ascorbate, chlorophyll and carotenoid degradation. However, the ascorbate pool remained highly reduced and lipid oxidation did not increase at this time. Contrasting with ascorbate, α-tocopherol accumulated progressively in all species. Only during the last stages of senescence was chlorophyll preferentially degraded with respect to carotenoids, leading to the yellowing of leaves, except in A. glutinosa in which a large retention of chlorophyll and N took place. Senescing leaves were characterised, except in C. sanguinea, by a relative increase in the proportion of de-epoxidised xanthophylls: zeaxanthin, antheraxanthin and lutein. The light-induced accumulation of anthocyanins in C. sanguinea could play an additional protective role, compensating for the low retention of de-epoxidised xanthophylls. These different strategies among deciduous species are consistent with a role for photoprotective compounds in enhancing nitrogen remobilization and storage for the next growing season.

Anthocyanins - ascorbate - carotenoids - nitrogen remobilization - α-tocopherol - shade tolerance - xanthophyll cycle

References

• 1 Adams W. W., Winter K., Schreiber U., Schramel P.. Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal leaf senescence.  Plant Physiol.. (1990);  93 1184-1190
• 2 del Arco J. M., Escudero A., Vega M.. Effects of site characteristics on nitrogen retranslocation from senescing leaves.  Ecology. (1991);  72 701-708
• 3 Biswal B.. Carotenoid catabolism during leaf senescence and its control by light.  J. Photochem. Photobiol.. (1995);  30 3-13
• 4 Biswal B.. Chloroplast metabolism during leaf greening and degreening. Pessaraki, M., ed. Handbook of Photosynthesis. New York; Marcel Dekker Inc. (1996): 71-81
• 5 Burton G. W., Ingold K. U.. β-Carotene: an unusual type of lipid antioxidant.  Science. (1984);  224 569-573
• 6 Chrost B., Falk J., Kernebeck B., Molleken H., Krupinska K.. Tocopherol biosynthesis in senescing chloroplasts - A mechanism to protect envelope membranes against oxidative stress and a prerequisite for lipid remobilization?.  Chloroplast from Molecular Biology to Biotechnology. (1999);  64 171-176
• 7 Collier D. E., Thiobodeau B. A.. Changes in respiration and chemical content during autumnal senescence of Populus tremuloides and Quercus rubra leaves.  Tree Physiol.. (1995);  15 759-764
• 8 Demmig-Adams B., Adams W. W.. Chorophyll and carotenoid composition in leaves of Euonymus kiatschovicus acclimated to different degrees of light stress in the field.  Aust. J. Plant Physiol.. (1996);  23 649-659
• 9 Feild T. S., Lee D. W., Holbrook N. M.. Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood.  Plant Physiol.. (2001);  127 566-574
• 10 García-Plazaola J. I., Becerril J. M.. A rapid HPLC method to measure lipophylic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols.  Phytochem. Anal.. (1999);  10 307-313
• 11 García-Plazaola J. I., Hernández A., Becerril J. M.. Photoprotective responses to winter stress in evergreen Mediterranean ecosystems.  Plant Biol.. (2000);  2 530-535
• 12 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.  Aust. J. Plant Physiol.. (2001);  28 225-232
• 13 Goodwin T. W.. The biochemistry of carotenoids, Vol. I, Plants. London, New York; Chapman and Hall (1980)
• 14 Gould K. S., Markhams K. R., Smith R. H., Goris J. J.. Functional role of anthocyanins in the leaves of Quintinia serrata A.  Cunn. J. Exp. Bot.. (2000);  51 1107-1115
• 15 Hansen U., Friedler B., Rank B.. Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance.  Trees. (2002);  16 354-364
• 16 Hansen U., Schneiderheinze J., Stadelman S., Rank B.. The α-tocopherol content of leaves of pedunculate oak (Quercus robur L.) - variation over the growing season and along the vertical light gradient in the canopy.  J. Plant Physiol.. (2003);  160 91-96
• 17 Henry H. A. L., Aarssen L. W.. On the relationship between shade tolerance and shade avoidance strategies in woodland species.  Oikos. (1997);  80 575-582
• 18 Hertog J., Stulen I., Posthumus F., Poorter H.. Interactive effects of growth-limiting N supply and elevated atmospheric CO₂ concentration on growth and carbon balance of Plantago major. .  Physiol. Plant.. (1998);  103 451-460
• 19 Hoch W. A., Zeldin E. L., McCown B. H.. Physiological significance of anthocyanins during autumnal leaf senescence.  Tree Physiol.. (2001);  21 1-8
• 20 Hodges D. M., DeLong J. M., Forney C. F., Prange R. K.. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.  Planta. (1999);  207 604-611
• 21 Hörtensteiner S., Feller U.. Nitrogen metabolism and remobilization during senescence.  J. Exp. Bot.. (2002);  53 927-937
• 22 Kar M., Streb P., Hertwig B., Feierabend J.. Sensitivity to photodamage increases during senescence in excised leaves.  J. Plant Physiol.. (1993);  141 538-544
• 23 Killingbeck K. T.. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency.  Ecology. (1996);  77 1716-1727
• 24 Kitao M., Lei T. T., Koike T., Tobita H., Maruyama Y.. Susceptibility to photoinhibition of three deciduous broadleaf species with different successional traits raised under various light regimes.  Plant Cell Environ.. (2000);  23 81-89
• 25 Krause G. H., Koroleva O. Y., Dalling J. W., Winter K.. Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps.  Plant Cell Environ.. (2001);  24 1345-1352
• 26 Kunert K. J., Ederer M.. Leaf ageing and lipid peroxidation: the role of the antioxidants vitamin C and E.  Physiol. Plant. (1985);  65 85-88
• 27 Logan B. A., Barker D. H., Demmig-Adams B., Adams W. W.. Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest.  Plant Cell Environ.. (1996);  19 1083-1090
• 28 Lu C., Lu Q., Zhang J., Kuang T.. Characterization of photosynthetic pigments composition, photosystem II photochemistry and thermal energy dissipation during leaf senescence of wheat plants grown in the field.  J. Exp. Bot.. (2001);  52 1805-1810
• 29 Matile P., Hörtensteiner S., Thomas H.. Chlorophyll degradation. Ann. Rev. Plant Physiol.  Plant Molec. Biol.. (1999);  50 67-95
• 30 May J. D., Killingbeck K. T.. Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics.  Ecology. (1992);  73 1868-1878
• 31 Merzlyak M. N., Gitelson A.. Why and what for the leaves are yellow in autumn? On the interpretation of optical spectra of senescencing leaves (Acer platanoides L).  J. Plant Physiol.. (1995);  145 315-320
• 32 Miersch I., Heie J., Zelmer I., Humbeck K.. Differential degradation of the photosynthetic apparatus during leaf senescence in barley (Hordeum vulgare L.).  Plant Biol.. (2000);  2 618-623
• 33 Müller P., Li X.-P., Niyogi K.. Non-photochemical quenching. A response to excess light energy.  Plant Physiol.. (2001);  125 1558-1566
• 34 Munné-Bosch A., Jubany-Marí T., Alegre L.. Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts.  Plant Cell Environ.. (2001);  24 1319-1327
• 35 Munné-Bosch S., Alegre L.. Plant ageing increases oxidative stress in chloroplasts.  Planta. (2002 a);  214 608-615
• 36 Munné-Bosch S., Alegre L.. The function of tocopherols and tocotrienols in plants.  Crit. Rev. Plant Sci.. (2002 b);  21 31-57
• 37 Murray J. R., Hackett W. P.. Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L.  Plant Physiol.. (1991);  97 343-351
• 38 Prochazkova D., Sairam R. K., Srivastava G. C., Singh D. V.. Oxidative stress and antioxidant activity as the basis of senescence in maize leaves.  Plant Sci.. (2001);  161 765-771
• 39 Rise M., Cojocaru M., Gottieb H. E., Goldschmidt E. E.. Accumulation of α-tocopherol in senescing organs as related to chlorophyll degradation.  Plant Physiol.. (1989);  89 1028-1030
• 40 Rosenthal S. I., Camm E. L.. Photosynthetic decline and pigment loss during autumn foliar senescence in western larch (Larix occidentalis). .  Tree Physiol.. (1997);  17 767-775
• 41 Siefermann-Harms D.. Light and temperature control of season-dependent changes in the α- and β-carotene content of spruce needles.  J. Plant Phys.. (1994);  143 488-494
• 42 Tevini M., Steinmüller D.. Composition and function of plastoglobuli. II Lipid composition of leaves and plastoglobuli during beech senescence.  Planta. (1985);  163 91-96
• 43 Thomas H., Ougham H., Canter P., Donnison L.. What stay-green mutants tell us about nitrogen remobilization during leaf senescence.  J. Exp. Bot.. (2002);  53 801-808
• 44 Young A. J., Britton G.. The distibution of α-carotene in the photosynthetic pigment complexes of higher plants.  Plant Sci.. (1989);  64 179-183
• 45 Young A. J., Wellings R., Britton G.. The fate of chloroplast pigments during senescence of primary leaves of Hordeum vulgare and Avena sativum. .  J. Plant Physiol.. (1991);  137 701-705

Section Editor: M. C. Ball