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

The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions

Jose I. García-Plazaola A , Shizue Matsubara B and C. Barry Osmond C D

A Department of Plant Biology and Ecology, UPV/EHU, Apdo. 644, 48080 Bilbao, Spain.

B Institut Phytosphäre (ICG3), Forschungszentrum Jülich, 52425 Jülich, Germany.

C School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia.

D Corresponding author. Email: barry.osmond@anu.edu.au

Functional Plant Biology 34(9) 759-773 http://dx.doi.org/10.1071/FP07095
Submitted: 18 April 2007  Accepted: 8 June 2007   Published: 30 August 2007

Abstract

Several xanthophyll cycles have been described in photosynthetic organisms. Among them, only two are present in higher plants: the ubiquitous violaxanthin (V) cycle, and the taxonomically restricted lutein epoxide (Lx) cycle, whereas four cycles seem to occur in algae. Although V is synthesised through the β-branch of the carotenoid biosynthetic pathway and Lx is the product of the α-branch; both are co-located in the same sites of the photosynthetic pigment-protein complexes isolated from thylakoids. Both xanthophylls are also de-epoxidised upon light exposure by the same enzyme, violaxanthin de-epoxidase (VDE) leading to the formation of zeaxanthin (Z) and lutein (L) at comparable rates. In contrast with VDE, the reverse reaction presumably catalysed by zeaxanthin epoxidase (ZE), is much slower (or even inactive) with L than with antheraxanthin (A) or Z. Consequently many species lack Lx altogether, and although the presence of Lx shows an irregular taxonomical distribution in unrelated taxa, it has a high fidelity at family level. In those plants which accumulate Lx, variations in ZE activity in vivo mean that a complete Lx-cycle occurs in some (with Lx pools being restored overnight), whereas in others a truncated cycle is observed in which VDE converts Lx into L, but regeneration of Lx by ZE is extremely slow. Accumulation of Lx to high concentrations is found most commonly in old leaves in deeply shaded canopies, and the Lx cycle in these leaves is usually truncated. This seemingly anomalous situation presumably arises because ZE has a low but finite affinity for L, and because deeply shaded leaves are not often exposed to light intensities strong enough to activate VDE. Notably, both in vitro and in vivo studies have recently shown that accumulation of Lx can increase the light harvesting efficiency in the antennae of PSII. We propose a model for the truncated Lx cycle in strong light in which VDE converts Lx to L which then occupies sites L2 and V1 in the light-harvesting antenna complex of PSII (Lhcb), displacing V and Z. There is correlative evidence that this photoconverted L facilitates energy dissipation via non-photochemical quenching and thereby converts a highly efficient light harvesting system to an energy dissipating system with improved capacity to engage photoprotection. Operation of the α- and β-xanthophyll cycles with different L and Z epoxidation kinetics thus allows a combination of rapidly and slowly reversible modulation of light harvesting and photoprotection, with each cycle having distinct effects. Based on the patchy taxonomical distribution of Lx, we propose that the presence of Lx (and the Lx cycle) could be the result of a recurrent mutation in the epoxidase gene that increases its affinity for L, which is conserved whenever it confers an evolutionary advantage.

Additional keywords: antheraxanthin, α-carotene, de-epoxidase, epoxidase, lutein, lutein epoxide, non-photochemical quenching, photoprotection, violaxanthin, xanthophyll cycles, zeaxanthin.


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