The protective function of the xanthophyll cycle in photosynthesis

Sarry, Jean-Emmanuel; Montillet, Jean‐Luc; Sauvaire, Yves; Havaux, Michel

doi:10.1016/0014-5793(94)01028-5

Cited by 67 publications

(50 citation statements)

References 32 publications

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“…It must be noted, however, that the protective function of the V cycle is probably not restricted to PSII, because the cycle takes place in both PSII and PSI (15). Inhibition of the V cycle by DTT, a potent (though nonspecific) inhibitor of the V deepoxidase, was associated with only a slight increase in the level of PSII photoinhibition in strong light whereas, concomitantly, pronounced lipid peroxidation monitored by the production of ethane was induced (16). This suggests that the V cycle could be involved in a general protection of the photosynthetic apparatus against photooxidation.…”

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The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism

Havaux

Niyogi

1999

Proc. Natl. Acad. Sci. U.S.A.

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627

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When light energy absorbed by plants becomes excessive relative to the capacity of photosynthesis, the xanthophyll violaxanthin is reversibly deepoxidized to zeaxanthin (violaxanthin cycle). The protective function of this phenomenon was investigated in a mutant of Arabidopsis thaliana, npq1, that has no functional violaxanthin deepoxidase. Two major consequences of the npq1 mutation are the absence of zeaxanthin formation in strong light and the partial inhibition of the quenching of singlet excited chlorophylls in the photosystem II light-harvesting complexes. Prolonged exposure of whole plants to bright light resulted in a limited photoinhibition of photosystem II in both npq1 and wild-type leaves, although CO 2 fixation and the linear electron transport in npq1 plants were reduced substantially. Lipid peroxidation was more pronounced in npq1 compared with the wild type, as measured by chlorophyll thermoluminescence, ethane production, and the total hydroperoxy fatty acids content. Lipid peroxidation was amplified markedly under chilling stress, and photooxidative damage ultimately resulted in leaf bleaching and tissue necrosis in npq1. The npq4 mutant, which possesses a normal violaxanthin cycle but has a limited capacity of quenching singlet excited chlorophylls, was rather tolerant to lipid peroxidation. The double mutant, npq4 npq1, which differs from npq4 only by the absence of the violaxanthin cycle, exhibited an increased susceptibility to photooxidative damage, similar to that of npq1. Our results demonstrate that the violaxanthin cycle specifically protects thylakoid membrane lipids against photooxidation. Part of this protection involves a mechanism other than quenching of singlet excited chlorophylls.

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“…In situ decomposition of -3 unsaturated hydroperoxy fatty acids into ethane was accelerated by a brief heat treatment (90 s) of the samples in a microwave oven. After cooling the flask, 1 ml of the gas phase was withdrawn and injected in a gas chromatograph for ethane determination (16).…”

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confidence: 99%

The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism

Havaux

Niyogi

1999

Proc. Natl. Acad. Sci. U.S.A.

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627

480

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“…Zeaxanthin synthesis in high light was also found to prevent photooxidative stress and lipid peroxidation (Sarry et al, 1994;Havaux et al, 2000) by a mechanism that seems to be different from NPQ (Havaux and Niyogi, 1999). In a number of cases, accumulation of zeaxanthin was shown to increase tolerance to photooxidative stress while NPQ was not substantially modified (Davison et al, 2002;Havaux et al, 2004;Johnson et al, 2007).…”

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Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions Independent of Binding to PSII Antennae

2007

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The ch1 mutant of Arabidopsis (Arabidopsis thaliana) lacks chlorophyll (Chl) b. Leaves of this mutant are devoid of photosystem II (PSII) Chl-protein antenna complexes and have a very low capacity of nonphotochemical quenching (NPQ) of Chl fluorescence. Lhcb5 was the only PSII antenna protein that accumulated to a significant level in ch1 mutant leaves, but the apoprotein did not assemble in vivo with Chls to form a functional antenna. The abundance of Lhca proteins was also reduced to approximately 20% of the wild-type level. ch1 was crossed with various xanthophyll mutants to analyze the antioxidant activity of carotenoids unbound to PSII antenna. Suppression of zeaxanthin by crossing ch1 with npq1 resulted in oxidative stress in high light, while removing other xanthophylls or the PSII protein PsbS had no such effect. The tocopherol-deficient ch1 vte1 double mutant was as sensitive to high light as ch1 npq1, and the triple mutant ch1 npq1 vte1 exhibited an extreme sensitivity to photooxidative stress, indicating that zeaxanthin and tocopherols have cumulative effects. Conversely, constitutive accumulation of zeaxanthin in the ch1 npq2 double mutant led to an increased phototolerance relative to ch1. Comparison of ch1 npq2 with another zeaxanthinaccumulating mutant (ch1 lut2) that lacks lutein suggests that protection of polyunsaturated lipids by zeaxanthin is enhanced when lutein is also present. During photooxidative stress, a-tocopherol noticeably decreased in ch1 npq1 and increased in ch1 npq2 relative to ch1, suggesting protection of vitamin E by high zeaxanthin levels. Our results indicate that the antioxidant activity of zeaxanthin, distinct from NPQ, can occur in the absence of PSII light-harvesting complexes. The capacity of zeaxanthin to protect thylakoid membrane lipids is comparable to that of vitamin E but noticeably higher than that of all other xanthophylls of Arabidopsis leaves.

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“…Zeaxanthin also appears to have a role in establishing tolerance to photooxidative stress by an NPQ-independent process, which protects the lipids of the thylakoid membrane from oxidative damage (14). Havaux and Niyogi (15) found that the Arabidopsis npq4 mutant, devoid of the PsbS protein, and so lacking the rapidly reversible component of NPQ, was still able to protect itself from lipid peroxidation, whereas the npq1 mutant, lacking a functional violaxanthin de-epoxidase enzyme and so devoid of zeaxanthin, suffered extensive oxidative lipid damage upon exposure to specific conditions of high light and low temperature.…”

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Elevated Zeaxanthin Bound to Oligomeric LHCII Enhances the Resistance of Arabidopsis to Photooxidative Stress by a Lipid-protective, Antioxidant Mechanism

Johnson

Havaux

Triantaphylidès

et al. 2007

Journal of Biological Chemistry

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174

140

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The xanthophyll cycle has a major role in protecting plants from photooxidative stress, although the mechanism of its action is unclear. Here, we have investigated Arabidopsis plants overexpressing a gene encoding ␤-carotene hydroxylase, containing nearly three times the amount of xanthophyll cycle carotenoids present in the wild-type. In high light at low temperature wild-type plants exhibited symptoms of severe oxidative stress: lipid peroxidation, chlorophyll bleaching, and photoinhibition. In transformed plants, which accumulate over twice as much zeaxanthin as the wild-type, these symptoms were significantly ameliorated. The capacity of non-photochemical quenching is not significantly different in transformed plants compared with wild-type and therefore an enhancement of this process cannot be the cause of the stress tolerant phenotype. Rather, it is concluded that it results from the antioxidant effect of zeaxanthin. 80 -90% of violaxanthin and zeaxanthin in wildtype and transformed plants was localized to an oligomeric LHCII fraction prepared from thylakoid membranes. The binding of these pigments in intact membranes was confirmed by resonance Raman spectroscopy. Based on the structural model of LHCII, we suggest that the protein/lipid interface is the active site for the antioxidant activity of zeaxanthin, which mediates stress tolerance by the protection of bound lipids.

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The protective function of the xanthophyll cycle in photosynthesis

Cited by 67 publications

References 32 publications

The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism

The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism

Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions Independent of Binding to PSII Antennae

Elevated Zeaxanthin Bound to Oligomeric LHCII Enhances the Resistance of Arabidopsis to Photooxidative Stress by a Lipid-protective, Antioxidant Mechanism

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