Activation of Zeaxanthin Is an Obligatory Event in the Regulation of Photosynthetic Light Harvesting

Ruban, Alexander V.; Pascal, Andrew A.; Robert, Bruno; Horton, Peter

doi:10.1074/jbc.m110693200

Cited by 102 publications

(107 citation statements)

References 32 publications

(29 reference statements)

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“…In addition, the measurements of LHCII and thylakoids under the unquenched condition all lack a lifetime component of Ϸ10 ps, which supports the notion that one-photon excitation of Zea is also unlikely when it is bound in a protein environment. All of the results are consistent with the idea that an electronic modification of some Zea molecules during the induction of qE, most likely in PsbS itself, is responsible for our observations (37).…”

Section: Discussionsupporting

confidence: 81%

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Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting

Holt

et al. 2003

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

201

177

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Nonphotochemical quenching (NPQ) refers to a process that regulates photosynthetic light harvesting in plants as a response to changes in incident light intensity. By dissipating excess excitation energy of chlorophyll molecules as heat, NPQ balances the input and utilization of light energy in photosynthesis and protects the plant against photooxidative damage. To understand the physical mechanism of NPQ, we have performed femtosecond transient absorption experiments on intact thylakoid membranes isolated from spinach and transgenic Arabidopsis thaliana plants. These plants have well defined quenching capabilities and distinct contents of xanthophyll (Xan) cycle carotenoids. The kinetics probed in the spectral region of the S 1 3 S n transition of Xans (530 -580 nm) were found to be significantly different under the quenched and unquenched conditions, corresponding to maximum and no NPQ, respectively. The lifetime and the spectral characteristics indicate that the kinetic difference originated from the involvement of the S 1 state of a specific Xan, zeaxanthin, in the quenched case.G reen plants live with a continual paradox: They have evolved to both use and dissipate solar energy with high efficiency. Highly reactive, photooxidative intermediates are inevitable byproducts of photosynthesis. An excess photon flux can exacerbate the damage caused by these intermediates, leading to problems ranging from reversible decreases in photosynthetic efficiency, to, in the worst case, death of the plant. Nonphotochemical quenching (NPQ) is a process that thermally dissipates the absorbed light energy in photosystem (PS) II that exceeds a plant's capacity for CO 2 fixation, minimizing the deleterious effects of high light. Although NPQ has been phenomenologically documented for years, a fundamental understanding of its physical mechanism remains elusive (1-3).Feedback deexcitation or energy-dependent quenching (qE) (2, 3) is the major, rapidly reversible component of NPQ in a variety of plants, including spinach and Arabidopsis thaliana (4,5), and is the focus of this study. qE is characterized by a light-induced absorbance change at 535 nm (⌬A 535 ) (6) and the shortening of specific components of chlorophyll (Chl) fluorescence lifetimes, the exact numerical value for the shortened lifetime depending on the specific form of the photosynthetic system and the measurement conditions. For isolated thylakoid systems with closed reaction centers, a Chl lifetime component is reduced from Ϸ2.0 to Ϸ0.4 ns (4). It requires the buildup of a pH gradient (⌬pH) under high light conditions (2, 3), which triggers the enzymatic conversion of carotenoids, violaxanthin (Vio) to zeaxanthin (Zea), by means of the xanthophyll (Xan) cycle (Fig. 1a).Currently two hypotheses concerning the mechanism of qE exist, one in which the effect of Zea is solely structural (termed indirect quenching) and the other in which Zea acts as an energy acceptor for excitation transfer from the first Chl singlet excited state (termed direct quenching). The direct ...

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Section: Discussionsupporting

confidence: 81%

“…The first is that the probe wavelengths from 530 to 580 nm are located on the red side of the spectrally red-shifted Zea absorption (37). For a given probe wavelength, pr , and a symmetric S 0 3 S 2 absorption band with an absorption maximum m , a band shift ϽϷ2͉ pr Ϫ m ͉ will lead to increased absorption.…”

Section: Discussionmentioning

confidence: 99%

Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting

Holt

et al. 2003

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

201

177

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“…However, in vivo light absorption and resonant Raman experiments on quenched PSII in leaves and chloroplasts indicated that zeaxanthin undergoes dramatic spectroscopic changes upon induction of feedback deexcitation: its absorption maximum shifts to the red by at least 22 nm, and the molecule assumes a very specific, highly twisted conformation (35). To account for these phenomena, Ruban et al (35) proposed that zeaxanthin is bound in a highly polarizing local environment, possibly arising from a strong electric field of a dipole or charge in the zeaxanthin vicinity. It seems plausible that such an extensive change of local environment, combined with a distortion of the polyene backbone, may bring down ICT states of zeaxanthin to couple with S 1 , and thereby activate a quenching mechanism similar to that reported here for the model systems.…”

Section: Discussionmentioning

confidence: 99%

A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

Berera

Herrero

Stokkum

et al. 2006

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

125

176

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Under excess illumination, plant photosystem II dissipates excess energy through the quenching of chlorophyll fluorescence, a process known as nonphotochemical quenching. Activation of nonphotochemical quenching has been linked to the conversion of a carotenoid with a conjugation length of nine double bonds (violaxanthin) into an 11-double-bond carotenoid (zeaxanthin). It has been suggested that the increase in the conjugation length turns the carotenoid from a nonquencher into a quencher of chlorophyll singlet excited states, but unequivocal evidence is lacking. Here, we present a transient absorption spectroscopic study on a model system made up of a zinc phthalocyanine (Pc) molecule covalently linked to carotenoids with 9, 10, or 11 conjugated carbon-carbon double bonds. We show that a carotenoid can act as an acceptor of Pc excitation energy, thereby shortening its singlet excited-state lifetime. The conjugation length of the carotenoid is critical to the quenching process. Remarkably, the addition of only one double bond can turn the carotenoid from a nonquencher into a very strong quencher. By studying the solvent polarity dependence of the quenching using target analysis of the time-resolved data, we show that the quenching proceeds through energy transfer from the excited Pc to the optically forbidden S 1 state of the carotenoid, coupled to an intramolecular charge-transfer state. The mechanism for excess energy dissipation in photosystem II is discussed in view of the insights obtained on this simple model system. artificial photosynthesis ͉ carotenoid ͉ nonphotochemical quenching ͉ photoprotection ͉ xanthophyll cycle

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“…The light Ϫ dark recovery absorption difference spectrum is characterized by a series of positive and negative bands, the best-known of which is ⌬A535 (20). Using resonance Raman the origin of ⌬A535 was shown to be a sub-population of red-shifted zeaxanthin molecules (21). In the absence of zeaxanthin (and antheraxanthin) a proportion of NPQ remains and the ⌬A535 change is blue-shifted to 525 nm (⌬A525) (22).…”

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confidence: 99%

Photoprotection in Plants Involves a Change in Lutein 1 Binding Domain in the Major Light-harvesting Complex of Photosystem II

Ilioaia

Johnson

Liao

et al. 2011

Journal of Biological Chemistry

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Nonphotochemical quenching (NPQ) is the fundamental process by which plants exposed to high light intensities dissipate the potentially harmful excess energy as heat. Recently, it has been shown that efficient energy dissipation can be induced in the major light-harvesting complexes of photosystem II (LHCII) in the absence of protein-protein interactions. Spectroscopic measurements on these samples (LHCII gels) in the quenched state revealed specific alterations in the absorption and circular dichroism bands assigned to neoxanthin and lutein 1 molecules. In this work, we investigate the changes in conformation of the pigments involved in NPQ using resonance Raman spectroscopy. By selective excitation we show that, as well as the twisting of neoxanthin that has been reported previously, the lutein 1 pigment also undergoes a significant change in conformation when LHCII switches to the energy dissipative state. Selective two-photon excitation of carotenoid (Car) dark states (Car S 1 ) performed on LHCII gels shows that the extent of electronic interactions between Car S 1 and chlorophyll states correlates linearly with chlorophyll fluorescence quenching, as observed previously for isolated LHCII (aggregated versus trimeric) and whole plants (with versus without NPQ).The photosynthetic process starts with the absorption of incoming solar photons by specialized pigment-protein complexes. In plants, light energy is absorbed by the two multisubunit protein-cofactor complexes, photosystem I (PSI) 3 and photosystem II (PSII), and the excitation energy is efficiently transferred to their reaction centers where photochemistry takes place. When these organisms are in low light environments, the process of light energy collection is extremely efficient. However, this process is regulated when the incoming light energy is above that which can be used in electron transport. In these latter conditions, the light-harvesting antenna is able to switch into a photoprotective mode, dissipating the excess energy as heat (1-3). This regulatory mechanism is measured as nonphotochemical quenching of chlorophyll (Chl) fluorescence (NPQ). In higher plants NPQ is a multicomponent process whose major component is called qE (energy-dependent quenching) (4), dependent upon the formation of the proton gradient (⌬pH) across the thylakoid membrane (which itself results from photosynthetic activity) (5). qE is facilitated by the deepoxidation of violaxanthin to zeaxanthin in the xanthophyll cycle (6). The PsbS protein also plays a crucial role in this process, possibly acting as a pH sensor (7,8). A key characteristic of the qE process is that it is induced in seconds and thus cannot involve de novo protein synthesis, but rather corresponds to a reorganization of the existing photosynthetic architecture.In the past decade a large amount of work has been performed to gain insight in the molecular mechanism(s) underlying this process, and several hypotheses have been put forward (9 -12). Among these, it was in particular proposed that excitation e...

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Activation of Zeaxanthin Is an Obligatory Event in the Regulation of Photosynthetic Light Harvesting

Cited by 102 publications

References 32 publications

Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting

Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting

A simple artificial light-harvesting dyad as a model for excess energy dissipation in oxygenic photosynthesis

Photoprotection in Plants Involves a Change in Lutein 1 Binding Domain in the Major Light-harvesting Complex of Photosystem II

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