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

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.

From ecophysiology to phenomics: some implications of photoprotection and shade–sun acclimation in situ for dynamics of thylakoids in vitro

“…(c) A small addition to the lutein pool (DL from de-epoxidation of Lx) replaces A 1 Z to 'lock-in' enhanced capacity for fast relaxing NPQ in avocado shade leaves De-epoxidation in the Lx-cycle in avocado, Mediterranean oak (Quercus rubra), I. sapindoides and several other species is only very slowly reversible [23], in marked contrast to that in parasitic Cuscuta reflexa [43] and Amyema miquelii [44] or in a Macaronesian evergreen tree Ocotea foetens [45]. Indeed, the rapid restoration of [Lx] in O. foetens after short (3 min) artificial sun flecks is evidence for the role of Lx as a 'perfect switch' in this species, supporting high photosynthetic efficiency in the shade as discussed earlier, and its de-epoxidation providing enhanced NPQ in a sun fleck [45].…”

“…Although discussion of these phenomena is usually focused on cost-benefit analyses and structural considerations, we have argued that there may be additional distinctive attributes of photosynthesis in these leaves that involve rather more than repayment of their construction costs [20]. For example, the distinctive pigment composition and de-epoxidation/ epoxidation kinetics in two xanthophyll cycles in woody plants of Mediterranean and tropical forests have attracted attention in this context [21][22][23][24]. This paper briefly reviews some properties of pigment dynamics in relation to photoprotection in two species, Inga sapindoides and Persea americana, especially those aspects encouraging further attention to the role of lutein (L).…”

Canopy conundrums: building on the Biosphere 2 experience to scale measurements of inner and outer canopy photoprotection from the leaf to the landscape

“…These old shade leaves of Inga spp. and avocado have permitted a direct approach to the enigmatic role of L in photoprotection (García-Plazoala et al 2007), providing 'economical insights' into the stabilisation of NPQ by DL, with distinctive functional implications for inner and outer canopy photosynthesis, as discussed below.…”

“…and avocado is presumably a product of metabolic pathways and leaf environment (Matsubara et al 2003;García-Plazoala et al 2007;Esteban et al 2008). In Inga, avocado and other plants (Matsubara et al 2009) a 'leaky' zeaxanthin epoxidase (ZE) with some affinity for L, evidently catalyses the slow production of Lx from L in the dark.…”

“…The biochemical relationships of the two cycles were summarised in fig. 1 of García-Plazoala et al (2007).…”