Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

Operation and regulation of the lutein epoxide cycle in seedlings of Ocotea foetens

Raquel Esteban A D , Shizue Matsubara B , María Soledad Jiménez C , Domingo Morales C , Patricia Brito C , Roberto Lorenzo C , Beatriz Fernández-Marín A , José María Becerril A and José Ignacio García-Plazaola A

A Departamento de Biología Vegetal y Ecología, Universidad del País Vasco EHU, Apdo. 644, E-48080 Bilbao, Spain.

B Institut für Phytosphäre (ICG-3), Forschungszentrum Jülich, 52425 Jülich, Germany.

C Departamento de Biología Vegetal, Universidad de La Laguna, 38207 La Laguna, Tenerife, Spain.

D Corresponding author. Email:

Functional Plant Biology 37(9) 859-869
Submitted: 19 January 2010  Accepted: 13 May 2010   Published: 24 August 2010


Two xanthophyll cycles are present in higher plants: the ubiquitous violaxanthin (V) cycle and the taxonomically restricted lutein epoxide (Lx) cycle. Conversions of V to zeaxanthin (Z) in the first and Lx to lutein (L) in the second happen in parallel under illumination. Unlike the V cycle, in which full epoxidation is completed overnight, in the Lx cycle, this reaction has been described as irreversible on a daily basis in most species (the ‘truncated’ Lx cycle). However, there are some species that display complete restoration of Lx overnight (‘true’ Lx cycle). So far, little is known about the physiological meaning of these two versions of the Lx cycle. Therefore, in the present work, the ‘true’ Lx cycle operation was studied in seedlings of Ocotea foetens (Aiton) Benth. under controlled and field conditions. Complete overnight recovery of the Lx pool in the presence of norfluorazon suggested that the inter-conversions between Lx and L represent a true cycle in this species. Furthermore, Lx responded dynamically to environmental conditions during long-term acclimation. Our data demonstrate the operation of a ‘true’ Lx cycle and, for the first time, its potential involvement in the regulation of non-photochemical quenching in situ. We propose dual regulation of Lx cycle in O. foetens, in which the extent of Lx restoration depends on the intensity and duration of illumination.

Additional keywords: de-epoxidation, epoxidation, laurel forest, xanthophyll cycles, violaxanthin.


Adams WW III Demmig-Adams B 1995 The xanthophyll cycle and sustained thermal energy dissipation activity in Vinca minor and Euonymus kiautschovicus in winter. Plant, Cell & Environment 18 117 127 doi:10.1111/j.1365-3040.1995.tb00345.x

Adams WW Demmig-Adams B Rosentiel TN Brightwell AK Ebbert V 2002 Photosynthesis and photoprotection in overwintering plants. Plant Biology 4 545 557 doi:10.1055/s-2002-35434

Bramwell D , Bramwell Z (2001) Flora. In ‘Flores silvestres de las Islas Canarias’. (Ed. Rueda) pp. 130–131. (Editorial Rueda SL: Madrid, Spain)

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 of the United States of America 96 1135 1139 doi:10.1073/pnas.96.3.1135

Dall’Osto L Lico C Alric J Giuliano G Havaux M Bassi R 2006 Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biology 6 32 doi:10.1186/1471-2229-6-32

Demmig-Adams B 1998 Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant & Cell Physiology 39 474 482

Demmig-Adams B Adams WW III 2006 Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172 11 21

Demmig-Adams B Moeller DL Logan BA Adams WW 1998 Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill. Planta 205 367 374 doi:10.1007/s004250050332

Esteban R Jiménez ET Jiménez MS Morales D Hormaetxe K Becerril JM García-Plazaola JI 2007 Dynamics of violaxanthin and lutein epoxide xanthophyll cycles in Lauraceae tree species under field conditions. Tree Physiology 27 1407 1414

Esteban R Jiménez MS Morales D Jiménez ET Hormaetxe K Becerril JM Osmond B García-Plazaola JI 2008 Short- and long-term modulation of the lutein epoxide and violaxanthin cycles in two species of the Lauraceae: sweet bay laurel (Laurus nobilis L.) and avocado (Persea americana Mill.). Plant Biology 10 288 297

Esteban R Olano JM Castresana J Fernández-Marín B Hernández A Becerril JM García-Plazaola JI 2009 Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom. Physiologia Plantarum 135 379 389 doi:10.1111/j.1399-3054.2008.01196.x

Förster B Osmond CB Pogson BJ 2009 De novo synthesis and degradation of Lx and V cycle pigments during shade and sun acclimation in avocado leaves. Plant Physiology 149 1179 1195 doi:10.1104/pp.108.131417

García-Plazaola JI Becerril JM 1999 A rapid high performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochemical Analysis 10 307 313 doi:10.1002/(SICI)1099-1565(199911/12)10:6<307::AID-PCA477>3.0.CO;2-L

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 doi:10.1071/PP00119

García-Plazaola JI Hernández A Artetxe U Becerril JM 2002 a Regulation of the xanthophyll cycle pool size in duckweed (Lemna minor) plants. Physiologia Plantarum 116 121 126 doi:10.1034/j.1399-3054.2002.1160115.x

García-Plazaola JI Hernández A Errasti E Becerril JM 2002 b Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29 1075 1080 doi:10.1071/FP02002

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 doi:10.1071/FP02224

García-Plazaola JI Matsubara S Osmond B 2007 The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Functional Plant Biology 34 759 773 doi:10.1071/FP07095

Gilmore AM 1997 Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99 197 209 doi:10.1111/j.1399-3054.1997.tb03449.x

Höllermann P 1981 Microenvironmental studies in the laurel forest of the Canary Islands. Mountain Research and Development 1 193 207 doi:10.2307/3673057

Johnson MP Davison P Ruban A Horton P 2008 The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Letters 582 262 266 doi:10.1016/j.febslet.2007.12.016

Johnson MP Pérez-Bueno M Zia A Horton P Ruban AV 2009 The zeaxanthin-independent and zeaxanthin-dependent qE components of nonphotoquemical quenching involve common conformational changes within the photosystem II antenna in Arabidopsis. Plant Physiology 149 1061 1075 doi:10.1104/pp.108.129957

Jung S Kim JS Cho KY Tae GS Kang BG 2000 Antioxidant responses of cucumber (Cucumis sativus) to photoinhibition and oxidative stress induced by norflurazon under high and low PPFDs. Plant Science 153 145 154 doi:10.1016/S0168-9452(99)00259-9

Li Z Ahn TK Avenson JT Ballotari M Cruz JA Kramer DM Bassi R Fleming GR Keasling JD Niyogi KK 2009 Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. The Plant Cell 21 1798 1812 doi:10.1105/tpc.109.066571

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 doi:10.1071/PP01031

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 doi:10.1071/FP02014

Matsubara S Morosinotto T 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 doi:10.1007/s00425-003-1059-7

Matsubara S Naumann M Martin R Nichol C Rascher U Morosinotto T Bassi R Osmond B 2005 Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may “lock in” lutein-based photoprotection during acclimation to strong light. Journal of Experimental Botany 56 461 468 doi:10.1093/jxb/eri012

Matsubara S Morisinotto T Osmond CB Bassi R 2007 Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144 926 941 doi:10.1104/pp.107.099077

Matsubara S Krause GH Seltmann M Virgo A Kursar TA Jahns P Winter K 2008 Lutein epoxide cycle, light harvesting and photoprotection in species of the tropical tree genus Inga. Plant, Cell & Environment 31 548 561 doi:10.1111/j.1365-3040.2008.01788.x

Matsubara S Krause GH Aranda J Virgo A Beisel KG Jahns P Winter K 2009 Sun–shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Functional Plant Biology 36 20 36 doi:10.1071/FP08214

Morales F Abadía A Abadía J 1990 Characterization of the xanthophyll cycle and other photosynthetic pigment changes induced by iron deficiency in sugar beet (Beta vulgaris L.). Plant Physiology 94 607 613 doi:10.1104/pp.94.2.607

Niyogi KK 1999 Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50 333 359 doi:10.1146/annurev.arplant.50.1.333

Pogson BJ Niyogi KK Björkman O DellaPenna D 1998 Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences of the United States of America 95 13 324 13 329 doi:10.1073/pnas.95.22.13324

Snyder AM Clark BM Bungard RA 2005 Light-dependent conversion of carotenoids in the parasitic angiosperm Cuscuta reflexa L. Plant, Cell & Environment 28 1326 1333 doi:10.1111/j.1365-3040.2005.01379.x

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 doi:10.1093/jxb/erg175

Winer BJ , Brown DR , Michels KM (1991) ‘Statistical principles in experimental design.’ (McGraw-Hill: New York, NY)

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