Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

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
+ Author Affiliations
- Author Affiliations

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: raquel.esteban@ehu.es

Functional Plant Biology 37(9) 859-869 https://doi.org/10.1071/FP10014
Submitted: 19 January 2010  Accepted: 13 May 2010   Published: 24 August 2010

Abstract

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.


Acknowledgements

We acknowledge B. Olascoaga (Basque Country University) for help during sampling and analyses, J. M. Olano for statistical advice, and the anonymous referees for their valuable suggestions regarding the manuscript. R.E. and B.F.M. received a fellowship from the Basque Government. R.E. received a grant from the Basque Government to make a visit to the ICG-3 (EC-2008–1-6). This research was supported by research BFU 2007–62637 from the Ministry of Education and Science of Spain, and research project UPV/EHU-GV IT-299–07.


References


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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Adams WW, Demmig-Adams B, Rosentiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biology 4, 545–557.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant & Cell Physiology 39, 474–482. open url image1

Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Hernández A, Artetxe U, Becerril JM (2002a) Regulation of the xanthophyll cycle pool size in duckweed (Lemna minor) plants. Physiologia Plantarum 116, 121–126.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

García-Plazaola JI, Hernández A, Errasti E, Becerril JM (2002b) Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gilmore AM (1997) Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiologia Plantarum 99, 197–209.
Crossref | GoogleScholarGoogle Scholar | open url image1

Höllermann P (1981) Microenvironmental studies in the laurel forest of the Canary Islands. Mountain Research and Development 1, 193–207.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 | open url image1

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 | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333–359.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 | open url image1

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