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Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae

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Abstract

The lutein-epoxide cycle (Lx cycle) is an auxiliary xanthophyll cycle known to operate only in some higher-plant species. It occurs in parallel with the common violaxanthin cycle (V cycle) and involves the same epoxidation and de-epoxidation reactions as in the V cycle. In this study, the occurrence of the Lx cycle was investigated in the two major families of mistletoe, the Loranthaceae and the Viscaceae. In an attempt to find the limiting factor(s) for the occurrence of the Lx cycle, pigment profiles of mistletoes with and without the Lx cycle were compared. The availability of lutein as a substrate for the zeaxanthin epoxidase appeared not to be critical. This was supported by the absence of the Lx cycle in the transgenic Arabidopsis plant lutOE, in which synthesis of lutein was increased at the expense of V by overexpression of ε-cyclase, a key enzyme for lutein synthesis. Furthermore, analysis of pigment distribution within the mistletoe thylakoids excluded the possibility of different localizations for the Lx- and V-cycle pigments. From these findings, together with previous reports on the substrate specificity of the two enzymes in the V cycle, we propose that mutation to zeaxanthin epoxidase could have resulted in altered regulation and/or substrate specificity of the enzyme that gave rise to the parallel operation of two xanthophyll cycles in some plants. The distribution pattern of Lx in the mistletoe phylogeny inferred from 18S rRNA gene sequences also suggested that the occurrence of the Lx cycle is determined genetically. Possible molecular evolutionary processes that may have led to the operation of the Lx cycle in some mistletoes are discussed.

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Abbreviations

A:

antheraxanthin

α- and β-Car:

α- and β-carotene

Chl:

chlorophyll

α-DM:

dodecyl-α-d-maltoside

DPS:

de-epoxidation state of the violaxanthin cycle (= [A+Z]/[V+A+Z])

Lut:

lutein

Lx:

lutein epoxide

Σ Caro:

total carotenoid concentration

V:

violaxanthin

VAZ:

pool size of the violaxanthin cycle (= V+A+Z)

VDE:

violaxanthin de-epoxidase

Z:

zeaxanthin

ZE:

zeaxanthin epoxidase

References

  • Adams WW III, Demmig-Adams B, Verhoeven AS, Barker DH (1995) 'Photoinhibition' during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Aust J Plant Physiol 22:261–276

    Google Scholar 

  • Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS, Smith SD (2002) Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species growing in the Mojave Desert. Plant Cell Environ 25:95–103

    Article  CAS  Google Scholar 

  • Barlow BA (1983) Biogeography of Loranthaceae and Viscaceae. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 19–46

  • Bassi R, Simpson DJ (1986) Differential expression of LHCII genes in mesophyll and bundle sheath cells of maize. Carlsberg Res Commun 51:363–370

    CAS  Google Scholar 

  • Bouvier F, d'Harlingue A, Hugueney P, Marin E, Marion-Poll A, Camara B (1996) Xanthophyll biosynthesis. Cloning, expression, functional reconstitution, and regulation of β-cyclohexenyl carotenoid epoxidase from pepper (Capsicum annuum). Proc Natl Acad Sci USA 271:28861–28867

    CAS  Google Scholar 

  • Bouvier F, d'Harlingue A, Backhaus RA, Kumagai MH, Camara B (2000) Identification of neoxanthin synthase as a carotenoid cyclase paralog. Eur J Biochem 267:6346–6352

    Article  CAS  PubMed  Google Scholar 

  • Bugos RC, Hieber AD, Yamamoto HY (1998) Xanthophyll cycle enzymes are members of the lipocalin family, the first identified from plants. J Biol Chem 273:15321–15324

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci USA 96:1135–1139

    Article  CAS  PubMed  Google Scholar 

  • Caffarri S, Croce R, Breton J, Bassi R (2001) The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. J Biol Chem 276:35924–35933

    Article  CAS  PubMed  Google Scholar 

  • Calder M (1997) The mistletoe plant. Victorian Nat 114:96–97

    Google Scholar 

  • Connelly JP, Müller MG, Bassi R, Croce R, Holzwarth AR (1997) Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. Biochemistry 36:281–287

    Article  CAS  PubMed  Google Scholar 

  • Cunningham FX Jr, Gantt E (2001) One ring or two? Determination of ring number in carotenoids by lycopene ε-cyclases. Proc Natl Acad Sci USA 98:2905–2910

    Article  CAS  PubMed  Google Scholar 

  • Dainese P, Bassi R (1991) Subunit stoichiometry of the chloroplast photosystem II antenna system and aggregation state of the component chlorophyll a/b binding proteins. J Biol Chem 266:8136–8142

    CAS  PubMed  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    CAS  Google Scholar 

  • Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482

    CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell Environ 15:411–419

    CAS  Google Scholar 

  • García-Plazaola J, Hernández A, Errasti E, Becerril JM (2002) Occurrences and operation of the lutein epoxide cycle in Quercus species. Funct Plant Biol 29:1075–1080

    Article  Google Scholar 

  • García-Plazaola J, Hernández A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Funct Plant Biol 30:319–324

    Google Scholar 

  • Gilmore AM, Govindjee (1999) How higher plants respond to excess light: energy dissipation in photosystem II. In: Singhal GS, Renger G, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa, New Delhi, pp 513–548

  • Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J Chromatogr 543:137–145

    Article  CAS  Google Scholar 

  • Green BR (2001) Was "molecular opportunism" a factor in the evolution of different photosynthetic light-harvesting pigment systems? Proc Natl Acad Sci USA 98:2119–2121

    Google Scholar 

  • Grotz B, Molnár P, Stransky H, Hager A (1999) Substrate specificity and functional aspects of violaxanthin-de-epoxidase, an enzyme of the xanthophyll cycle. J Plant Physiol 154:437–446

    CAS  Google Scholar 

  • Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218

    CAS  PubMed  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley,·Los Angeles, pp 13–80

  • Kumagai MH, Keller Y, Bouvier F, Clary D, Camara B (1998) Functional integration of non-native carotenoids into chloroplasts by viral-derived expression of capsanthin–capsorubin synthase in Nicotiana benthamiana. Plant J 14:305–315

    Article  CAS  PubMed  Google Scholar 

  • Maidak BL, Cole JR, Lilburn TG, Parker CTJr, Saxman PR, Farris RJ, Garrity GM, Olsen GJ, Schmidt TM, Tiedje JM (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29:173–174

    PubMed  Google Scholar 

  • Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Frey A, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15:2331–2342

    CAS  PubMed  Google Scholar 

  • Martin NJ (1983) Nuclear DNA variation in the Australian Loranthaceae. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 277–293

  • Matsubara S, Gilmore AM, Osmond CB (2001) Diurnal and acclimatory responses of violaxanthin and lutein epoxide in the Australian mistletoe Amyema miquelii. Aust J Plant Physiol 28:793–800

    Article  CAS  Google Scholar 

  • Matsubara S, Gilmore AM, Ball MC, Anderson JM, Osmond CB (2002) Sustained downregulation of photosystem II in mistletoes during winter depression of photosynthesis. Funct Plant Biol 29:1157–1169

    Article  CAS  Google Scholar 

  • Nickrent DL, Franchina CR (1990) Phylogenetic relationships of Santalales and relatives. J Mol Evol 31:294–301

    CAS  PubMed  Google Scholar 

  • Nickrent DL, Schuette KP, Starr EM (1994) A molecular phylogeny of Arceuthobium (Viscaceae) based on nuclear ribosomal DNA internal transcribed spacer sequences. Am J Bot 81:1149–1160

    CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    CAS  Google Scholar 

  • Niyogi KK, Björkman O, Grossman AR (1997) Chlamydomonas xanthophyll cycle mutants identified by video imaging of chlorophyll fluorescence quenching. Plant Cell 9:1369–1380

    CAS  Google Scholar 

  • Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    CAS  PubMed  Google Scholar 

  • Phillip D, Hobe S, Paulsen H, Molnar P, Hashimoto H, Young, AJ (2002) The binding of xanthophylls to the bulk light-harvesting complex of photosystem II of higher plants. A specific requirement for carotenoids with a 3-hydroxy-β-end group. J Biol Chem 277:25160–25169

    Article  CAS  PubMed  Google Scholar 

  • Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8:1627–1639

    Article  CAS  PubMed  Google Scholar 

  • Pogson BJ, Rissler HM (2000) Genetic manipulation of carotenoid biosynthesis and photoprotection. Phil Trans R Soc Lond B 355:1395–1403

    Article  CAS  Google Scholar 

  • Press MC, Gurney AL (2000) Plant eats plant: sap-feeding witchweeds and other parasitic angiosperms. Biologist 47:189–193

    CAS  PubMed  Google Scholar 

  • Rabinowitch HD, Budowski P, Kedar N (1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122:91–97

    CAS  Google Scholar 

  • Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Lee PJ, Wentworth M, Young AJ, Horton P (1999) Determination of the stoichiometry and strength of binding of xanthophylls to the photosystem II light harvesting complexes. Proc Natl Acad Sci USA 274:10458–10465

    Article  CAS  Google Scholar 

  • Siefermann D, Yamamoto HY (1975) Properties of NADPH and oxygen-dependent zeaxanthin epoxidation in isolated chloroplasts. Arch Biochem Biophys 171:70–77

    CAS  PubMed  Google Scholar 

  • Thayer SS, Björkman O (1990) Leaf Xanthophyll content and composition in sun and shade determined by HPLC. Photosynth Res 23:331–343

    CAS  Google Scholar 

  • Thompson AJ, Jackson AC, Parker RA, Morpeth DR, Burbidge A, Taylor IB (2000) Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol Biol 42:833–845

    Article  CAS  PubMed  Google Scholar 

  • Verhoeven AS, Adams WW III, Demmig-Adams B, Croce R, Bassi R (1999) Xanthophyll cycle pigment localization and dynamics during exposure to low temperatures and light stress in Vinca major. Plant Physiol 120:727–737

    CAS  PubMed  Google Scholar 

  • Watson DM (2001) Mistletoe — A keystone resource in forests and woodlands worldwide. Annu Rev Ecol Syst 32:219–249

    Article  Google Scholar 

  • **a X, **e Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  CAS  PubMed  Google Scholar 

  • **ong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto HY, Bassi R (1996) Carotenoids: localization and function. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer, Dordrecht, pp 539–563

  • Yamamoto HY, Higashi RM (1978) Violaxanthin de-epoxidase. Lipid composition and substrate specificity. Arch Biochem Biophys 190:514–522

    CAS  PubMed  Google Scholar 

  • Yamamoto HY, Nakayama TOM, Chichester CO (1962) Studies on the light and dark interconversions of leaf xanthophylls. Arch Biochem Biophys 97:168–173

    CAS  Google Scholar 

  • Young AJ (1993a) Carotenoids in pigment–protein complexes. In: Young AJ, Britton G (eds) Carotenoids in photosynthesis. Chapman & Hall, London, pp 72–95

  • Young AJ (1993b) Occurrence and distribution of carotenoids in photosynthetic systems. In: Young AJ, Britton G (eds) Carotenoids in photosynthesis. Chapman & Hall, London, pp 16–71

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Acknowledgements

S.M. is the recipient of an ANU PhD Graduate School Scholarship (Endowment for Excellence) and an Overseas Postgraduate Research Scholarship. Part of this study was supported by a Forschungspreis from the Alexander von Humboldt Stiftung to C.B.O. and PRONEX-CNPq Brazil to A.C.F.. We thank Dr. Georg Weiller (Canberra, Australia) for invaluable advice on the phylogenetic analyses and Dr. Marilyn C. Ball for helpful comments on the manuscript. Kind assistance for HPLC experiments by Prof. Carlos A. Schwartz and Dr. Osmindo R. Pires Jr. (Brasilía, Brazil) and the identification of species in Rio de Janeiro by Carlos H. R. de Paula (Rio de Janeiro, Brazil) are greatly acknowledged. Plant materials were collected with the help of Claudenir S. Caires and Vandelio C. Mendes (Brasília, Brazil), Dr. Cornelia Büchen-Osmond (Oracle, USA), Dr. Stephan Schneckenburger (Darmstadt, Germany), and Dr. John C.G. Banks and Dr. Torsten Jülich (Canberra, Australia), to whom we would like to extend the warmest thanks.

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Authors and Affiliations

  1. Research School of Biological Sciences, and School of Biochemistry and Molecular Biology, Australian National University, GPO Box 475, ACT 2601, Canberra, Australia

    Shizue Matsubara, Britta Förster & Barry J. Pogson

  2. Dipartimento Scientifico e Tecnologico, Università di Verona, Strada Le Grazie, 15-37234, Verona, Italy

    Tomas Morosinotto & Roberto Bassi

  3. Institut für Botanik, Technische Universität Darmstadt, Schnittspahnstrasse 3–5, 64287, Darmstadt, Germany

    Anna-Luise Christian, Elke Fischer-Schliebs & Ulrich Lüttge

  4. Departamento de Botânica, Universidade de Brasília, caixa postal 04457, 70919-970, Brasília, DF, Brazil

    Birgit Orthen & Augusto C. Franco

  5. Departamento de Ecologia, Universidade Federal do Rio de Janeiro, CCS, Ilha do Fundão, 21941-970, Rio de Janeiro, RJ, Brazil

    Fabio R. Scarano

  6. Biosphere 2 Center, Columbia University, Oracle, AZ 85623, USA

    C. Barry Osmond

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  1. Shizue Matsubara
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Correspondence to Shizue Matsubara.

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Matsubara, S., Morosinotto, T., Bassi, R. et al. Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217, 868–879 (2003). https://doi.org/10.1007/s00425-003-1059-7

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