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BIOENERGETICS AND PHOTOSYNTHESIS

Short- and Long-Term Operation of the Lutein-Epoxide Cycle in Light-Harvesting Antenna Complexes^1,[W],[OA]

Phytosphäre Institut (Institut für Chemie und Dynamik der Geosphäre-3), Forschungszentrum Jülich, 52425 Juelich, Germany (S.M., C.B.O.); Laboratoire de Génétique et Biophysique des Plantes, Université de la Méditerranée, Marseille, France (T.M., R.B.); Dipartimento Scientifico e Tecnologico, Università di Verona, 37134 Verona, Italy (R.B.); Dipartimento di Biologia, Università di Padova, 35131 Padova, Italy (T.M.); and School of Biochemistry and Molecular Biology, Australian National University, Canberra, Australian Capital Territories 0200, Australia (C.B.O.)

The lutein-5,6-epoxide (Lx) cycle operates in some plants between lutein (L) and its monoepoxide, Lx. Whereas recent studies have established the photoprotective roles of the analogous violaxanthin cycle, physiological functions of the Lx cycle are still unknown. In this article, we investigated the operation of the Lx cycle in light-harvesting antenna complexes (Lhcs) of Inga sapindoides Willd, a tropical tree legume accumulating substantial Lx in shade leaves, to identify the xanthophyll-binding sites involved in short- and long-term responses of the Lx cycle and to analyze the effects on light-harvesting efficiency. In shade leaves, Lx was converted into L upon light exposure, which then replaced Lx in the peripheral V1 site in trimeric Lhcs and the internal L2 site in both monomeric and trimeric Lhcs, leading to xanthophyll composition resembling sun-type Lhcs. Similar to the violaxanthin cycle, the Lx cycle was operating in both photosystems, yet the light-induced Lx L conversion was not reversible overnight. Interestingly, the experiments using recombinant Lhcb5 reconstituted with different Lx and/or L levels showed that reconstitution with Lx results in a significantly higher fluorescence yield due to higher energy transfer efficiencies among chlorophyll (Chl) a molecules, as well as from xanthophylls to Chl a. Furthermore, the spectroscopic analyses of photosystem I-LHCI from I. sapindoides revealed prominent red-most Chl forms, having the lowest energy level thus far reported for higher plants, along with reduced energy transfer efficiency from antenna pigments to Chl a. These results are discussed in the context of photoacclimation and shade adaptation.

² These authors contributed equally to the article.

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www.plantphysiol.org/cgi/doi/10.1104/pp.107.099077

^* Corresponding author; e-mail s.matsubara{at}fz-juelich.de; fax 49–2461–61–2492.

Received March 6, 2007; accepted March 16, 2007; published March 27, 2007.