The lutein epoxide cycle in vegetative buds of woody plants
José I. García-Plazaola A D , Koldobika Hormaetxe A , Antonio Hernández A B , José M. Olano C and José M. Becerril AA Department of Plant Biology and Ecology, University of the Basque Country EHU, Aptdo 644, E-48 080 Bilbao, Spain.
B Dirección de Innovación y Desarrollo, OHL, Gobelas 35-37, El Plantío, E-28 023 Madrid, Spain.
C Área de Biología Vegetal, Departamento de Ciencias Agroforestales, Escuela de Ingenierías Agrarias, Los Pajaritos s / n, Soria, E-42 003 Spain.
D Corresponding author; email: gvpgaplj@lg.ehu.es
Functional Plant Biology 31(8) 815-823 https://doi.org/10.1071/FP04054
Submitted: 12 March 2004 Accepted: 12 May 2004 Published: 23 August 2004
Abstract
Recent works have shown that two xanthophyll cycles operate simultaneously in several plant species: the ubiquitous violaxanthin + anteraxanthin + zeaxanthin (VAZ) cycle and the lutein epoxide (Lx) cycle. In the present work we tested for the presence of the Lx cycle in vegetative buds of woody plants. After an extensive screening of 130 species, we have shown that Lx is present in buds of many different plant species and leaf primordia are enriched in Lx compared with leaves. As a result, the Lx pool was higher than the violaxanthin (V) pool in several species. Although Lx can be potentially de-epoxidised in buds, light attenuation by scales inhibited the daily operation of the Lx cycle. This finding would imply that the Lx cycle is not involved in short-term reversible photoprotection in buds. However, a light-induced decrease in Lx was observed through the winter. An extensive screening of 130 species in 49 families conducted to elucidate the taxonomic extension of this cycle showed a widespread presence of the Lx cycle. The presence of Lx has a high fidelity at the family level, but its presence in unrelated taxa suggests that this character has appeared independently in several different groups of plants.
Keywords: lutein, taxanomic distribution, xanthophyll cycle.
Acknowledgments
KH received a fellowship from the Ministry of Science and Technology of Spain and AH 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 UPV 118.310-13533/2001. We thank the Real Jardín Botánico of Madrid and its staff for access to the plant collection and to Raquel Esteban for technical assistance.
Bungard RA,
Ruban AV,
Hibberd JM,
Press MC,
Horton P, Scholes JD
(1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proceedings of the National Academy of Sciences USA 96, 1135–1139.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Becerril JM
(1999) A rapid HPLC method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochemical Analysis 10, 307–313.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Becerril JM
(2001) 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 28, 225–232.
| Crossref |
García-Plazaola JI,
Faria T,
Abadía J,
Abadía A,
Chaves MM, Pereira JS
(1997) Seasonal changes in xanthopyll composition and photosynthesis of cork oak (Quercus suber L.) leaves under Mediterranean climate. Journal of Experimental Botany 48, 1667–1674.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI,
Hernández A, Becerril JM
(2000) Photoprotective responses to winter stress in evergreen Mediterranean ecosystems. Plant Biology 2, 530–535.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI,
Errasti E,
Hernández A, Becerril JM
(2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.
| Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI,
Hernández A,
Olano JM, Becerril JM
(2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biology 30, 319–324.
| Crossref | GoogleScholarGoogle Scholar |
Goss R
(2003) Substrate specificity of the violaxanthin de-epoxidase of the primitive green alga Mantoniella squamata (Prasinophyceae). Planta 217, 801–812.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kull D, Pfander H
(1995) Isolation and identification of carotenoids from the petals of rape (Brassica napus). Journal of Agricultural and Food Chemistry 43, 2854–2857.
Larbi A,
Abadía A,
Morales F, Abadía J
(2003) Fe resupply to Fe-deficient sugar beet plants leads to rapid changes in the violaxanthin cycle and other photosynthetic characteristics without significant de novo chlorophyll synthesis. Photosynthesis Research 79, 56–69.
Latowski D,
Kruk J,
Burda K,
Skrzynecka-Jaskier M,
Kostecka-Gugala A, Strzalka K
(2002) Kinetics of violaxanthin de-epoxidation by violaxanthin de-epoxidase, a xanthophyll cycle enzyme, is regulated by membrane fluidity in model lipid bilayers. European Journal of Biochemistry 269, 4656–4665.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Llorens L,
Aranda X,
Abadía A, Fleck I
(2002) Variations in Quercus ilex chloroplast pigment content during summer stress: involvement in photoprotection according to principal component analysis. Functional Plant Biology 29, 81–88.
| Crossref | GoogleScholarGoogle Scholar |
Matsubara S,
Gilmore AM, Osmond CB
(2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii.
Australian Journal of Plant Physiology 28, 793–800.
| Crossref | GoogleScholarGoogle Scholar |
Matsubara S,
Gilmore AM,
Ball MC,
Anderson JM, Osmond CB
(2002) Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Functional Plant Biology 29, 1157–1169.
| Crossref | GoogleScholarGoogle Scholar |
Matsubara S,
Morosinotto Y,
Bassi R,
Christian AL, Fischer-Schliebs E ,
et al
.
(2003) Occurrence of the lutein–epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217, 868–879.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matus Z,
Molnár P, Szabó LG
(1993) Main carotenoids in pressed seeds (Cucurbitae semen) of oil pumkin (Cucurbita pepo convar. pepo var. styriaca). Acta Pharmaceutica Hungarica 63, 247–256.
| PubMed |
Müller-Moulé P,
Conklin PL, Niyogi KK
(2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiology 128, 970–977.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pogson BJ,
Niyogi KK,
Björkman O, dellaPenna D
(1998) Altered xanthophyll composition adversely affect chlorophyll accumulation and non-photochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences USA 95, 13 324–13 329..
| Crossref | GoogleScholarGoogle Scholar |
Rabinowitch HD,
Budowski P, Kedar N
(1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122, 91–97.
Razungles AJ,
Babic I,
Sapisd JC, Bayonove CL
(1996) Particular behaviour of epoxy xanthophylls during veraison and maturation of grape. Journal of Agricultural and Food Chemistry 44, 3821–3825.
| Crossref | GoogleScholarGoogle Scholar |
Savolainen V,
Fay MF,
Albach DC,
Backlund A, van der Bank M
(2000) Phylogeny of the eudicots: a nearly complete familial analysis based on rbcl gene sequences. Kew Bulletin 55, 257–309.
Smirnoff N
(2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology 3, 229–235.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Soltis DE,
Soltis PS,
Chase MW,
Mort ME, Albach DC ,
et al
.
(2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL and atpB sequences. Botanical Journal of the Linnean Society 133, 381–461.
| Crossref | GoogleScholarGoogle Scholar |
Tai CY, Chen BH
(2000) Analysis and stability of carotenoids in the flowers of daylily (Hemerocallis disticha) as affected by various treatments. Journal of Agricultural and Food Chemistry 48, 5962–5968.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tausz M,
Wonisch A,
Grill D,
Morales D, Jiménez MS
(2003) Measuring antioxidants in tree species in the natural environment: from sampling to data evaluation. Journal of Experimental Botany 54, 1505–1510.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Werner C,
Correia O, Beyschlag W
(2002) Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. Functional Plant Biology 29, 999–1011.
| Crossref | GoogleScholarGoogle Scholar |
Young AJ, Phillip D, Savill J
(1997) Carotenoids in higher plant photosynthesis. ‘Handbook of photosynthesis’.
edn(Ed. M Pessaraki)
pp. 575–596. (Marcel Dekker Inc.: New York, NY)