Xanthophyll Cycle Pigment Localization and Dynamics during Exposure to Low Temperatures and Light Stress inVinca major1

Abstract

The distribution of xanthophyll cycle pigments (violaxanthin plus antheraxanthin plus zeaxanthin [VAZ]) among photosynthetic pigment-protein complexes was examined in Vinca major before, during, and subsequent to a photoinhibitory treatment at low temperature. Four pigment-protein complexes were isolated: the core of photosystem (PS) II, the major light-harvesting complex (LHC) protein of PSII (LHCII), the minor light-harvesting proteins (CPs) of PSII (CP29, CP26, and CP24), and PSI with its LHC proteins (PSI-LHCI). In isolated thylakoids 80% of VAZ was bound to protein independently of the de-epoxidation state and was found in all complexes. Plants grown outside in natural sunlight had higher levels of VAZ (expressed per chlorophyll), compared with plants grown in low light in the laboratory, and the additional VAZ was mainly bound to the major LHCII complex, apparently in an acidlabile site. The extent of de-epoxidation of VAZ in high light and the rate of reconversion of Z plus A to V following 2.5 h of recovery were greatest in the free-pigment fraction and varied among the pigment-protein complexes. Photoinhibition caused increases in VAZ, particularly in low-light-acclimated leaves. The data suggest that the photoinhibitory treatment caused an enrichment in VAZ bound to the minor CPs caused by de novo synthesis of the pigments and/or a redistribution of VAZ from the major LHCII complex.Photoinhibition refers to a condition in which a persistent decrease in the efficiency of photosynthetic energy conversion in leaves is observed. Photoinhibition occurs in the field in plants exposed to conditions of high light in combination with environmental stress, such as cold temperatures, but can also be induced by exposure of shadeacclimated leaves to high light (Krause, 1994; Osmond, 1994).Under various photoinhibitory conditions large quantities of the xanthophyll cycle pigments Z and A have been found to be retained in leaves for extended periods after darkening (Demmig et al., 1988;Adams et al., 1995;Verhoeven et al., 1996;Demmig-Adams et al., 1998). The xanthophyll cycle pigments Z and A are formed from V when light is excessive, and they are involved in a photoprotective process whereby excess absorbed excitation energy is dissipated thermally in the light-harvesting antennae of PSII (Demmig-Adams and Adams, 1996; Eskling et al., 1997; Gilmore, 1997). The retention of Z plus A in photoinhibited leaves often correlates closely with sustained low PSII efficiencies measured as the F v /F m (Adams et al., 1995;Verhoeven et al., 1996; Demmig-Adams et al., 1998, and refs. therein). Such correlations have led to the suggestion that Z plus A may be engaged for thermal energy dissipation under these conditions and may therefore be involved in the reduced PSII efficiencies observed.To influence Chl fluorescence yield xanthophylls must be localized in close proximity to the pigment-protein complexes of the thylakoid membrane, and knowledge of their precise organization is important to understand the mechanism of (Z plus...

A Mechanism of Nonphotochemical Energy Dissipation, Independent from PsbS, Revealed by a Conformational Change in the Antenna Protein CP26

“…These characteristics are similar to those found in long term overwinter quenching (Verhoeven et al, 1999;Gilmore and Ball, 2000). Previous results demonstrated the existence of a form of sustained (Z þ A)-dependent energy dissipation, detected in cold-acclimated leaves and retained even upon warming; this mechanism is correlated with slow Z þ A to violaxanthin conversion and is not associated to nocturnal maintenance of low lumenal pH (Verhoeven et al, 1998).…”

“…Genetic analysis has identified PsbS as a gene product indispensable for qE, while zeaxanthin and lutein appear as modulators of qE amplitude Pogson et al, 1998). Zeaxanthin accumulation also has been involved in long term (overwinter) downregulation of photosynthesis (Verhoeven et al, 1999;Gilmore and Ball, 2000). Current understanding of energy dissipation suggests that PsbS catalyzes qE upon protonation of lumenal-exposed residues (Li et al, 2002b) and binding of zeaxanthin.…”

Role of the Reversible Xanthophyll Cycle in the Photosystem II Damage and Repair Cycle in Dunaliella salina

“…the lipid bilayer of the zea1 chloroplast thylakoids. Previous studies have shown that xanthophylls cycle Car are localized within the minor LHC (Bassi et al, 1993;Verhoeven et al, 1999) and/or may be found as free pigment in the lipid matrix of the thylakoid membrane (Tardy and Havaux, 1996;Bassi and Caffarri, 2000). Relevant in this respect are the findings of Havaux and Niyogi (1999) and Havaux et al (2000), who showed that the npq1 mutant of Arabidopsis, which cannot perform a de-epoxidation of V to Z, is subject to enhanced lipid peroxidation upon photooxidative stress.…”

The Functional Significance of the Monomeric and Trimeric States of the Photosystem II Light Harvesting Complexes

“…A peripheral binding site for xanthophyll cycle carotenoids has been identified on LHCII trimers (11,49). This site appears to be only partially occupied, the occupancy increasing under stress conditions when the xanthophyll cycle pool is enlarged (50). Genetic manipulation to increase the pool size similarly leads to increased occupancy of this site (51).…”