Plant Biol (Stuttg) 2004; 6(3): 325-332
DOI: 10.1055/s-2004-817883
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Role of Red Carotenoids in Photoprotection During Winter Acclimation in Buxus sempervirens Leaves

K. Hormaetxe1 , A. Hernández1 , J. M. Becerril1 , J. I. García-Plazaola1
  • 1Department of Plant Biology and Ecology, Universidad del País Vasco-EHU, Bilbao, Spain
Further Information

Publication History

Publication Date:
14 May 2004 (online)

Abstract

The red leaf coloration of several plant species during autumn and winter is due to the synthesis of phenolic compounds such as anthocyanins or red carotenoids. The latter occur very rarely and are non-ubiquitous and taxonomically restricted compounds. The present study shows that the leaves of common box (Buxus sempervirens L.) accumulate red carotenoids (eschscholtzxanthin, monoanhydroeschscholtzxanthin, anhydroeschscholtzxanthin) as a response to photoinhibitory conditions during winter acclimation. These compounds are produced in a coordinated manner with the operation of other photoprotective systems: accumulation and sustained deepoxidation of VAZ pigments with a concomitant decrease in maximal photochemical efficiency, accumulation of α-tocopherol and a gradual decrease on chlorophyll content. All these processes were reversed when the photosynthetic tissues were transferred from photoinhibitory winter conditions to room temperature for 9 days. Buxus leaves showed a large degree of phenotype variation in the degree of reddening, ranging from green to orange. The differences in colour pattern were mainly due to differences in the accumulation of red carotenoids and xanthophyll esters. Red pigments were mainly anhydroeschscholtzxanthin and esters of eschscholtzxanthin. Conversely to fruit or petal chromoplasts, the plastids of red leaves in this species are not the terminal differentiated state but are able to redifferentiate again to chloroplasts. Their photoprotective role during winter as a light screen system or as antioxidants, in a similar way to other red pigments, and their implications on the wide ecological tolerance of this evergreen species are discussed.

References

  • 1 Adams W. W., Demmig-Adams B., Verhoeven A. S., Barker D. H.. “Photoinhibition” during winter stress: involvement of sustained xanthophyll cycledependent energy dissipation.  Aust. J. Plant Physiol.. (1994);  22 261-276
  • 2 Barry P., Evershed R. P., Young A., Prescott M. C., Britton G.. Characterization of carotenoid acyl esters produced in drought-stressed barley seedlings.  Phytochem.. (1992);  31 3163-3168
  • 3 Bouvier F., Backhaus R. A., Camara B.. Induction and control of chromoplasts-specific carotenoid genes by oxidative stress.  J. Biol. Chem.. (1998);  273 30651-30659
  • 4 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 and plants.  Proc. Nat. Acad. Sci. USA. (1999);  96 1135-1139
  • 5 Chalker-Scott L.. Environmental significance of anthocyanins in plant stress responses.  Photochem. Photobiol.. (1999);  70 1-9
  • 6 Demmig-Adams B., Adams W. W.. Photoprotection and other responses of plants to high light stress.  Annu. Rev. Plant Phys. Plant Molec. Biol.. (1992);  43 599-626
  • 7 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
  • 8 Díaz M., Ball E., Lüttge U.. Stress-induced accumulation of the xanthophyll rhodoxanthin in leaves of Aloe vera. .  Plant Physiol. Biochem.. (1990);  28 679-682
  • 9 Duke S. O., Becerril J. M., Sherman T. D., Matsumoto H.. Photosensitizing porphyrins as herbicides. Hedin, P. A., ed. Naturally Ocurring Pest Bioregulators. Washington; ACS (1990): 371-386
  • 10 Feild T. S., Lee D. W., Holbrook M. M.. Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood.  Plant Physiol.. (2001);  127 566-574
  • 11 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
  • 12 García-Plazaola J. I., Hernández A., Becerril J. M.. Photoprotective responses to winter stress in evergreen Mediterranean ecosystems.  Plant Biol.. (2000);  2 530-535
  • 13 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
  • 14 García-Plazaola J. I., Errasti E., Hernández A., Becerril J. M.. Occurrence and operation of the lutein epoxide cycle in Quercus species.  Funct. Plant Biol.. (2002);  29 1075-1080
  • 15 Gratani L., Ghia E.. Adaptive strategy at the leaf level of Arbutus unedo L. to cope with Mediterranean climate.  Flora. (2002);  197 275-284
  • 16 Han Q., Shinohara K., Kakubari Y., Mukai Y.. Photoprotective role of rhodoxanthin during cold acclimation in Cryptomeria japonica. .  Plant Cell Environ.. (2003);  26 715-723
  • 17 Hansen U., Schneiderheinze J., Stadelmann 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
  • 18 Havaux M., Tardy F., Ravenel J., Chanu D., Parot P.. Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of the xanthophyll content.  Plant Cell Environ.. (1996);  19 1359-1368
  • 19 Havaux M., Niyogi K. K.. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism.  Proc. Nat. Acad. Sci. USA. (1999);  96 8762-8767
  • 20 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
  • 21 Hirayama O., Nakamura K., Hamada S., Kobayasi Y.. Singlet oxygen quenching ability of naturally occurring carotenoids.  Lipids. (1994);  29 149-150
  • 22 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.  J. Plant Res.. (1995);  108 369-376
  • 23 Masojídek J., Torzillo G., Koblízek M., Kopecky J., Nidiaci L., Komenda J.. Changes in chlorophyll fluorescence quenching and pigment composition in the green alga Chlorococcum sp. grown under nitrogen deficiency and salinity stress.  J. Appl. Phycol.. (2000);  12 417-426
  • 24 Miskiewicz E., Ivanov A. G., Williams J. P., Khan M. U., Falk S., Huner N. P. A.. Photosynthetic acclimation of the filamentous cyanobacterium, Plectonema boryanum UTEX 485, to temperature and light.  Plant and Cell Physiol.. (2000);  41 767-775
  • 25 Neill S. O., Gould K. S., Kilmartin P. A., Mitchell K. A., Markham K. R.. Antioxidant activities of red versus green leaves in Elatostema rugosum. .  Plant Cell Environ.. (2002);  25 539-547
  • 26 Niinemets Ü., Bilger W., Kull O., Tenhunen J. D.. Responses of foliar photosynthetic electron transport, pigment stoichiometry, and stomatal conductance to interacting environmental factors in a mixed species forest canopy.  Tree Physiol.. (1999);  19 839-852
  • 27 Niinemets Ü., Kollist H., García-Plazaola J. I., Hernández A., Becerril J. M.. Do the capacity and kinetics for modification of xanthophyll cycle pool size depend on growth irradiance in temperate trees?.  Plant Cell Environ.. (2003);  26 1787-1801
  • 28 Nishio J. N.. Why are higher plants green? Evolution of the higher plant photosynthetic pigment complement.  Plant Cell Environ.. (2000);  23 539-548
  • 29 Öquist G., Huner N. P. A.. Photosynthesis of overwintering evergreen plants.  Ann. Rev. Plant Biol.. (2003);  54 329-355
  • 30 Phillip D., Hobe S., Paulsen H., Molnar P., Hashimoto H., Young A. J.. The binding of xanthophylls to the bulk light-harvesting complex of photosystem II of higher plants.  J. Biol Chem.. (2002);  277 25160-25169
  • 31 Pietrini F., Iannelli M. A., Massacci A.. Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photoinhibitory risks at low temperature, without further limitation to photosynthesis.  Plant Cell Environ.. (2002);  25 1251-1259
  • 32 Polle A., Rennenberg H.. Photooxidative stress in trees. Foyer, C. H. and Mullineaux, P. M., eds. Causes of Photooxidative Stress and Amelioration of Defence Systems in Plants. London; CRC Press (1994): 199-218
  • 33 Rice-Evans C. A., Miller N. J., Paganga G.. Antioxidant properties of phenolic compounds.  Trends Plant Sci.. (1997);  2 152-159
  • 34 Schaberg P. G., van den Berg A. K., Murakami P. F., Shane J. B., Donnelly J. R.. Factors influencing red expression in autumn foliage of sugar maple trees.  Tree Physiol. (2003);  23 325-333
  • 35 Steinbrenner J., Linden H.. Regulation of two carotenoid biosynthesis genes coding for phytoene synthase and carotenoid hydroxylase during stressinduced astaxanthin formation in the green alga Haematococcus pluvialis. .  Plant Physiol.. (2001);  125 810-817
  • 36 Steyn W. J., Wand S. J. E., Holcroft D. M., Jacobs G.. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection.  New Phytol.. (2002);  155 349-361
  • 37 Strain H. H.. Eschscholtzxanthin: a new xanthophyll from the petals of the california poppy, Escholtzia californica. .  J. Biol. Chem.. (1938);  123 425-437
  • 38 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.  J. Exp. Bot.. (2003);  387 1505-1510
  • 39 Tevini M., Steinmüller D.. Composition and function of plastoglobuli. II Lipid composition of leaves and plastoglobuli during beech senescence.  Planta. (1985);  163 91-96
  • 40 Valladares F., Balaguer L., Martínez-Ferri E., Perez-Corona E., Manrique E.. Plasticity, instability and canalization: is the phenotypic variation in seedlings of sclerophyll oaks consistent with the environmental unpredictability of Mediterranean ecosystems?.  New Phytol.. (2002);  156 457-467
  • 41 Verhoeven A. S., Demmig-Adams B., Adams W. W.. Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress.  Plant Physiol.. (1997);  113 817-824
  • 42 Wada M., Kagawa T., Sato Y.. Chloroplast movement.  Ann. Rev. Plant Biol.. (2003);  54 455-468
  • 43 Weger H. G., Silim S. N., Guy R. D.. Photosynthetic acclimation to low temperature by western red cedar seedlings.  Plant Cell Environ.. (1993);  16 711-717
  • 44 Young A. J., Phillip D., Savill J.. Carotenoids in higher plant photosynthesis. Pessaraki, M., ed. Handbook of Photosynthesis. New York; Marcel Dekker Inc. (1997): 575-596

J. I. García-Plazaola

Department of Plant Biology and Ecology
Universidad del País Vasco-EHU

Apdo 644

48080 Bilbao

Spain

Email: gvpgaplj@lg.ehu.es

Guest Editor: F. Loreto

    >