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State Transitions--a Question of Balance

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Science  07 Mar 2003:
Vol. 299, Issue 5612, pp. 1530-1532
DOI: 10.1126/science.1082833

Green plants and algae use a process of photochemical energy transduction called photosynthesis to harness light energy to make the energy-rich molecule ATP. Within their chloroplasts, light energy captured by chlorophyll photopigments is transformed into an electrochemical potential, which raises the energy of an electron; the subsequent “fall” of the electron back to its original state releases energy that is used to make ATP. Plants must tune photosynthesis to changing light conditions, and they do this with kinases that phosphorylate (add phosphate groups) to proteins of the photosynthetic machinery. The light-harvesting complex II (LHCII) is found in the chloroplasts of all plants and green algae, and accounts for about half of the chlorophyll molecules in nature. It tunes energy conversion to the wavelength of light in a balancing act known as state transitions. For over 20 years, the redox-controlled kinase that phosphorylates proteins in the LHCII and thus drives state transitions has been eagerly sought. Despite ingenious biochemical experiments, the results have invariably been ambiguous, yielding interesting new proteins but leaving the identity of the LHCII kinase shrouded in mystery (1). Enter Depège et al. (2) on page 1572 of this issue, with their report of a new LHCII kinase. Using a genetic approach to screen for mutants of the green alga Chlamydomonas reinhardtii, they identify a new serine-threonine protein kinase in the chloroplast thylakoid membranes. They call their kinase Stt7 (for state transition, thylakoid) and demonstrate that it is required for the phosphorylation of the LHCII protein complex.

Both light and dark reactions comprise the energy conversion steps of photosynthesis. During the former, light energy drives the movement of an electron from a reluctant donor to a reluctant acceptor. This is followed by dark reactions during which the electron is returned to its lowest energy state in order to make ATP and, eventually, to fix carbon dioxide. In the 1930s, experiments with short flashes of light of different intensities revealed that there is a surprising excess of chlorophyll molecules involved in the primary events of photosynthesis (3). In a “photosynthetic unit” of about 300 chlorophylls that work together to absorb each quantum of light energy, only one chlorophyll molecule converts energy into a stable chemical form in a protein complex called the “reaction center.” The remaining chlorophylls are “light-harvesting” pigments that keep the reaction center supplied with light energy quanta at a rate enabling one quantum to be converted about every 60 ms at normal light intensities. Subsequent experiments revealed that the wavelength dependency of photosynthetic yield is caused by two different but connected photosynthetic units—photosystem I and II (3). Photosystem II supplies electrons to photosystem I, and their serial connection means that the rate of electron transport between the two photosystems must be equal. Thus, for maximal photosynthetic efficiency, the rates of delivery of quanta to the two reaction centers must also be identical.

In 1969, using two experimental algae—Chlorella pyrenoidosa and Porphyridium cruentum—with different light-harvesting pigments, two laboratories reported independently that absorbed light energy is redistributed constantly between photosystems I and II by means of state transitions (4). Under light conditions that favor photosystem I (light 1), the fluorescence emission from chlorophyll increases over the course of a few minutes, indicating that the surplus energy of photosystem I has been redirected to the rate-limiting fluorescent photosystem II. In the resulting “light-1 state” (state 1), absorbed light energy is distributed equally between photosystems I and II. But under light conditions that favor photosystem II (light 2), there is a sharp rise in chlorophyll fluorescence as photosystem II becomes saturated with quanta. During the next few minutes, fluorescence falls as excess light 2 is used up by the now rate-limiting photosystem I. In the resulting “light-2 state” (state 2), an equal balance also is achieved, this time because a fraction of the light-harvesting chlorophylls of photosystem II are moonlighting—they have been redeployed to collect quanta for photosystem I.

What causes the transition between states 1 and 2? Plastoquinone is one of the electron carriers that connects photosystem I with photosystem II (see the figure). Under light 2 conditions, electrons enter the plastoquinone pool faster than they leave it and plastoquinone becomes reduced. Reduction of plastoquinone activates a thylakoid protein kinase that Depège et al. postulate may be Stt7. This enzyme catalyzes phosphorylation of LHCII proteins, which then leave photosystem II and join photosystem I (5). The imbalance in energy distribution is therefore corrected and plastoquinone is restored, in state 2, to a condition of redox poise. Conversely, light 1 causes photosystem I to extract electrons from plastoquinone faster than they arrive from photosystem II. When plastoquinone is thus oxidized, the kinase is switched off, LHCII becomes dephosphorylated by an LHCII phosphatase, and balance is restored in state I as LHCII returns to photosystem II.

Transitions between states.

During photosynthesis, the LHCII kinase phosphorylates the LHCII protein complex and is required for the transition from state 1 to state 2. The LHCII phosphatase dephosphorylates LHCII and is required for the transition from state 2 to state 1. The two photosynthetic units, photosystems I and II, have central reaction center domains (yellow) that drive electron transport (blue) into and out of the pool of plastoquinone (PQH2, reduced plastoquinone; PQ, oxidized plastoquinone). The reaction centers harness light energy, and each works optimally with different wavelengths of light (light 2; light 1). Each photosystem has its own light-harvesting protein pigment complexes (light green) to collect and distribute light energy to the reaction centers. There is also a mobile light-harvesting complex, LHCII (dark green), that serves to collect light for photosystem I in its phosphorylated form (P, phosphate group), and for photosystem II in its dephosphorylated form. The molecular basis of the transition from state 1 to state 2 is redox activation of the LHCII kinase, which could be Stt7 itself or a target of Stt7. This activation takes place when plastoquinone becomes reduced because photosystem II moves electrons slightly faster than photosystem I. Conversely, the molecular basis of the transition from state 2 to state 1 is redox inactivation of the LHCII kinase; this occurs when plastoquinone becomes oxidized because photosystem I moves electrons faster than photosystem II. In the state 1 transition, the LHCII phosphatase reaction restores the ability of LHCII to deliver light energy to photosystem II.

To screen a Chlamydomonas DNA library for state transition mutants, Depège et al. (2) measured the fluorescence emission of chlorophyll in the cell colonies. Rochaix's laboratory described such mutants a few years ago. Now, Depège and colleagues conclusively identify the stt7-1 and stt7-2 mutants as incapable of undergoing the state 2 transition with concomitant decreased phosphorylation of LHCII (2). Both mutants carry mutations in the nuclear gene encoding the Stt7 protein of chloroplast thylakoid membranes. From its sequence, this protein is predicted to be a serine-threonine kinase. The 754 amino acids of Stt7 include an amino-terminal 41-amino acid chloroplast transit peptide and a putative single membrane helix that is located between the transit sequence and the catalytic domain. There are two cysteines similar to the site of action of the redox regulatory protein thioredoxin. Stt7 has clear orthologs in the model plant Arabidopsis thaliana and a paralog Stl1 (state transition-like) in a Chlamydomonas expressed sequence tag collection (2). Further work is needed to confirm that Stt7 is required for state transitions in other species, and to characterize Stl1. Future investigations should be aided by the availability of Arabidopsis plants engineered to be deficient in Stt7 (2).

It may be that Stt7 forms just one link in the redox signaling pathway that underpins the state transitions of photosynthesis, perhaps working together with other thylakoid-associated kinases (5). The core event—occupancy of a binding site by reduced plastoquinone—probably occurs in the cytochrome b6f complex which, like plastoquinone, connects photosystem I with photosystem II (6). These initial steps in signal transduction may be common to both LHCII-containing cells and to cyanobacteria and red algae, which have a different kind of light-harvesting antenna. It is possible that Stt7 is specific to LHCII-containing organisms.

There is also a long-term balancing act in play because plastoquinone controls the relative rates of transcription of photosystem I and II reaction center genes (7). This mechanism serves to balance the absolute stoichiometry of photosystem I relative to photosystem II, not just their delivery of light quanta to preexisting reaction centers. This redox control of transcription may be the prime reason why the chloroplast genome retained the genes of its cyanobacterial ancestors.

Future prospects include better understanding of how LHCII phosphorylation affects the dynamic architecture of photosynthetic membranes: both local structural changes at atomic resolution (4) and supramolecular rearrangements of reaction center, light-harvesting, and electron-transfer elements (8-10). With mutants of signal transduction components such as Stt7 researchers can now dissect out the structural consequences for target proteins from an intriguing but mechanistically poorly resolved set of integrated responses. State transitions in photosynthesis may be a specialist evolutionary application of chloroplast redox signaling (7), guided molecular recognition (9-10), and membrane protein trafficking (6). With the characterization of the Chlamydomonas Stt7 mutant by Depège and colleagues, researchers now have another tool with which to take state transitions apart and see the stuff of which they are made.

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