Mechanism of Photosynthetic State Transitions

Green plants carry out photosynthesis using two photosystems: PSI and PSII. The two photosystems convert light energy (photons) into redox* potential so that at the end of the electron transfers, carbon dioxide is reduced to glucose. PSI and PSII occur in two different locations in chloroplast thylakoids. PSI is in the stroma lamellae and PSII is within the thylakoid membrane of the grana stacks. Both PSI and PSII are present in the grana margins. Each photosystem has a characteristic optimal activation wavelength range – for PSI, illumination of wavelength less than 700 nm; for PSII, wavelengths less than or equal to 680 nm. Both photosystems pass on electrons along a series of electron carriers in redox reactions.

Plants are capable of responding to illumination conditions by differentially distributing light energy between PSI and PSII. These redistributions are called state transitions and are short-term responses, occurring within minutes. State transitions are thought to occur when light-harvesting complex II (LHCII) relocates from PSII to PSI. The mechanism for this has been proposed to involve phosphorylation of LHCII subunits in a manner regulated by redox state of plastoquinone. The effect of the state transition is to redistribute excitation energy to PSII or PSI, whichever is favored by the conditions at hand.

In a review article in the July, 2001 issue of Trends in Plant Science (6:301-305), Henrik V. Scheller and his associates at the Royal Veterinary and Agriculture University (Copenhagen, Denmark) present the current state of knowledge about the regulation of photosynthetic state transitions. In the beginning of the article, the authors show with the help of a figure how state transitions can be analyzed by fluorescence measurements in intact dark-adapted leaves by exposing them to wavelengths that activate PSI or PSII. By these manipulations, the changes in fluorescence that occur during transition states can be measured.

When both photosystems harvest the same amount of light energy, a balanced electron flow is established. In state 1, units of unphosphorylated LHCII are bound to PSII. If conditions favor light energy harvesting by PSII, PSI cannot function as efficiently and electrons accumulate between the two systems. In state 2, a fraction of LHCII subunits become phosphorylated and dissociate from PSII to associate with PSI. Standard models of the mechanism of LHCII dissociation involve the activation of a thylakoid LHCII kinase, which phosphorylates the LHCII subunits. The kinase has been suggested to be sensitive to the redox state of plastoquinone (PQ), an electron carrier. The PQ pool is reduced when PSII runs faster than PSI.

While the authors describe this current working model of the mechanism of state transition regulation, they feel that more current research indicates a need to change the existing paradigm. In particular, they advocate a re-evaluation of the relationship between the redox state of the PQ pool and the phosphorylation state of LHCII. They also interpret recent data as supporting a more active role of PSI in the state transition establishment process.

Though in vitro experiments have indicated a correlation between PQ redox state and LHCII phosphorylation levels, results from in vivo studies do not support a simple relationship. In the in vivo experiments, high light conditions resulted in a reduction of PQ molecules, but little of the LHCII pool was phosphorylated. The authors suggest that stromal components, which are absent in the in vitro experiments, regulate LHCII phosphorylation. They also propose that the inhibition of LHCII phosphorylation in high light results from the reduction of thiol groups in LHCII kinase. Although the authors do not rule out the possibility of the involvement of LHCII phosphorylation in regulating state transitions, they do not think it is a causal relationship. To support this position, they cite experiments with pumpkin and Arabidopsis in which the phosphorylation status of LHCII and the level of state transitions was not directly correlated. Highest LHCII phosphorylation occurred at low light intensities. State transitions did not show a direct relationship with the level of irradiance in the low- to moderate-irradiance range, although both state transitions and LHCII phosphorylation were decreased in high light. Analogous conclusions were made in a study on barley. Based on these observations, the authors proposed that the kinase may act upon a substrate other than LHCII. Although the kinase has not been unambiguously identified, a candidate has been described in Arabidopsis.

Previously, PSI has been thought to play a passive role in state transitions. Opinions vary as to whether LHCII actually adheres to PSI in state 2. According to some reports, a fraction of the LHCII pool is associated with PSI in normally grown plants. The authors determined the relative antenna size of PSI in states 1 and 2, noting a 33% increase after the transition to state 2. They calculated that one LHCII trimer associates with each PSI in state 2. To further investigate the role of PSI in state transitions, the authors produced a series of transgenic Arabidopsis plants lacking subunits of PSI. From the study of these transgenic plants, they found that the PSI-H subunit plays an essential role in state transitions. PSI in plants lacking PSI-H cannot associate with LHCII, although the LHCII pool was highly phosphorylated. These transgenic plants were deficient in state transitions. The three-dimensional nature of these interactions is beginning to emerge from other studies which have shown that the PSI subunits PSI-F and PSI-J associate with light harvesting complex I and that they are on the other side of the complex from PSI-H, PSI-I and PSI-L. The transgenic plants lacking PSI-H also have higher phosphorylation of LHCII than in wild type and a more reduced PQ pool, indicating that LHCII phosphorylation alone cannot promote the dissociation of LHCII from PSII. The authors propose that, in contrast to previous models, the distribution of LHCII occurs due to a binding equilibrium between it and the two photosystems. In this mechanism, LHCII-PSI binding is promoted during state 2, and alterations in binding affinities regulate state transitions.

In conclusion, the authors propose that factors other than LHCII phosphorylation status regulate state transitions. They further propose that a functional attachment site on PSI is essential for both detachment of LHCII from PSII and its binding to PSI, thus advocating an active role for PSI in this process. In order to further evaluate this model, the authors stress the need for mutant or transgenic plants that are permanently “locked” in state 2, so that binding constants can be determined and other regulatory factors can be identified.

*The redox potential is a measure (in volts) of the affinity of a substance for electrons – its electronegativity – compared with hydrogen (which is set at 0).


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