Involvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids

Santabarbara, Stefano; Neverov, K.V.; Garlaschi, Flavio M.; Zucchelli, Giuseppe; Jennings, Robert C.

doi:10.1016/s0014-5793(01)02174-3

Cited by 85 publications

(86 citation statements)

References 27 publications

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“…Because of its photodynamic properties, free chlorophyll is potentially hazardous and is believed to be involved in photoinhibition of the photosystems (31). By reacting with molecular O 2 , free chlorophyll in the excited triplet state can generate the toxic 1 O 2 , which in turn can damage thylakoid membrane components, causing leaf bleaching and tissue necrosis in chaos leaves.…”

Section: Resultsmentioning

confidence: 99%

Early light-induced proteins protect Arabidopsis from photooxidative stress

Hutin

Nussaume

Moise

et al. 2003

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

302

250

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The early light-induced proteins (ELIPs) belong to the multigenic family of light-harvesting complexes, which bind chlorophyll and absorb solar energy in green plants. ELIPs accumulate transiently in plants exposed to high light intensities. By using an Arabidopsis thaliana mutant (chaos) affected in the posttranslational targeting of light-harvesting complex-type proteins to the thylakoids, we succeeded in suppressing the rapid accumulation of ELIPs during high-light stress, resulting in leaf bleaching and extensive photooxidative damage. Constitutive expression of ELIP genes in chaos before light stress resulted in ELIP accumulation and restored the phototolerance of the plants to the wild-type level. Free chlorophyll, a generator of singlet oxygen in the light, was detected by chlorophyll fluorescence lifetime measurements in chaos leaves before the symptoms of oxidative stress appeared. Our findings indicate that ELIPs fulfill a photoprotective function that could involve either the binding of chlorophylls released during turnover of pigment-binding proteins or the stabilization of the proper assembly of those proteins during high-light stress.L ight is essential for plants through photosynthetic carbon assimilation. However, when absorbed light exceeds the photosynthetic capacities, reactive O 2 species are generated in the chloroplasts, causing oxidative damage to proteins, lipids, and photosynthetic pigments (1, 2). This effect is amplified by environmental stresses such as low temperature or drought, for example, that inhibit the photosynthetic activity, leading to strong yield reduction in crops. In green plants, solar energy is collected by chlorophyll-and carotenoid-binding lightharvesting complexes (LHCs), which are encoded by a multigene family of LHC genes. The expression of these genes is tightly regulated by light (2-4). High light intensities inhibit transcription of LHC genes and activate synthesis of the early lightinduced proteins (ELIPs), a class of proteins structurally related to the LHCs (5). The ELIPs are predicted to have three transmembrane helices, and they have sequence similarity to the LHCs in the central pair of helices (6, 7). The similarity is not only at the sequence level, however, because both LHCs and ELIPs bind chlorophyll and carotenoids (8). The ELIPs differ from the LHCs by their transient expression under high-light stress (5). Recently, a number of ELIP-type polypeptides, containing LHC motifs and inducible by high light, have been discovered in vascular plants: the one-helix high-light-induced proteins (9) and the two-helix stress-enhanced proteins (10).The physiological role of the ELIPs in vascular plants has not yet been elucidated, although there have been several suggestions (11)(12)(13)(14). The induction of ELIPs by high light intensities suggests a role in the acclimation to light stress rather than a light-harvesting function, but this has not yet been demonstrated. ELIP antisense transgenic tobacco plants did not exhibit any phenotype of sensitivity to high ...

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Section: Resultsmentioning

confidence: 99%

Early light-induced proteins protect Arabidopsis from photooxidative stress

Hutin

Nussaume

Moise

et al. 2003

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

302

250

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“…In principle, uncoupled chlorophylls are expected to have a high triplet yield and hence lead to photoinhibition via singlet oxygen formation (Santabarbara et al, 2001). Their presence may be experimentally demonstrated either by time resolved fluorescence decay measurements (Vasil'ev et al, 1998), due to their nanosecond lifetime, or by steady-state fluorescence measurements due to their blue-shifted emission (absorption) characteristics (Santabarbara and Jennings, 2005).…”

Section: Uncoupled Chlorophyll Moleculesmentioning

confidence: 99%

Suppression of Both ELIP1 and ELIP2 in Arabidopsis Does Not Affect Tolerance to Photoinhibition and Photooxidative Stress

et al. 2006

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ELIPs (early light-induced proteins) are thylakoid proteins transiently induced during greening of etiolated seedlings and during exposure to high light stress conditions. This expression pattern suggests that these proteins may be involved in the protection of the photosynthetic apparatus against photooxidative damage. To test this hypothesis, we have generated Arabidopsis (Arabidopsis thaliana) mutant plants null for both elip genes (Elip1 and Elip2) and have analyzed their sensitivity to light during greening of seedlings and to high light and cold in mature plants. In particular, we have evaluated the extent of damage to photosystem II, the level of lipid peroxidation, the presence of uncoupled chlorophyll molecules, and the nonphotochemical quenching of excitation energy. The absence of ELIPs during greening at moderate light intensities slightly reduced the rate of chlorophyll accumulation but did not modify the extent of photoinhibition. In mature plants, the absence of ELIP1 and ELIP2 did not modify the sensitivity to photoinhibition and photooxidation or the ability to recover from light stress. This raises questions about the photoprotective function of these proteins. Moreover, no compensatory accumulation of other ELIP-like proteins (SEPs, OHPs) was found in the elip1/elip2 double mutant during high light stress. elip1/elip2 mutant plants show only a slight reduction in the chlorophyll content in mature leaves and greening seedlings and a lower zeaxanthin accumulation in high light conditions, suggesting that ELIPs could somehow affect the stability or synthesis of these pigments. On the basis of these results, we make a number of suggestions concerning the biological function of ELIPs.

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“…Inspite of the large number of studies about the mechanisms of photoinhibition, there is no consensus about how much different molecular mechanisms contribute to inhibition under visible and ultraviolet light. The main hypotheses include the acceptor-side mechanism (Vass et al 1992), the donor-side mechanism (Chen et al 1992;Anderson et al 1998) and hypotheses based on damage caused by singlet oxygen ( 1 O 2 ) produced either by thylakoid components with no function in PSII (Jung and Kim, 1990;Santabarbara et al 2001) or produced by back reactions (Keren et al 1997). In addition, we have recently suggested that the Mn ions of the oxygen-evolving complex are involved in photoinhibition (Hakala et al 2004).…”

Section: Introductionmentioning

confidence: 99%

Mathematical modelling of the light response curve of photoinhibition of Photosystem II

2005

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The light response curves of the acceptor and donor side mechanisms of photoinhibition of Photosystem II were calculated, using Arabidopsis as a model organism. Acceptor-side photoinhibition was modelled as double reduction of QA, noting that non-photochemical quenching has the same effect on the quantum yield of QA double reduction in closed PSII centres as it has on the quantum yield of electron transport in open centres. The light response curve of acceptor-side photoinhibition in Arabidopsis shows very low efficiency under low intensity light and a relatively constant quantum yield above light saturation of photosynthesis. To calculate the light response curve of donor-side photoinhibition, we built a model describing the concentration of the oxidized primary donor P680 + during steady-state photosynthesis. The model is based on literature values of rate constants of electron transfer reactions of PSII, and it was fitted with fluorescence parameters measured in the steady state. The modelling analysis showed that the quantum yield of donor-side photoinhibition peaks under moderate light. The deviation of the acceptor and donor side mechanisms from the direct proportionality between photoinhibition and photon flux density suggests that these mechanisms cannot solely account for photoinhibition in vivo, but contribution of a reaction whose quantum yield is independent of light intensity is needed. Furthermore, a simple kinetic calculation suggests that the acceptor-side mechanism may not explain singlet oxygen production by photoinhibited leaves. The theoretical framework described here can be used to estimate the yields of different photoinhibition mechanisms under different wavelengths or light intensities.

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Involvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids

Cited by 85 publications

References 27 publications

Early light-induced proteins protect Arabidopsis from photooxidative stress

Early light-induced proteins protect Arabidopsis from photooxidative stress

Suppression of Both ELIP1 and ELIP2 in Arabidopsis Does Not Affect Tolerance to Photoinhibition and Photooxidative Stress

Mathematical modelling of the light response curve of photoinhibition of Photosystem II

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