Energy-dependent quenching of excess absorbed light energy (qE) is a vital mechanism for regulating photosynthetic light harvesting in higher plants. All of the physiological characteristics of qE have been positively correlated with charge transfer between coupled chlorophyll and zeaxanthin molecules in the light-harvesting antenna of photosystem II (PSII). We found evidence for charge-transfer quenching in all three of the individual minor antenna complexes of PSII (CP29, CP26, and CP24), and we conclude that charge-transfer quenching in CP29 involves a delocalized state of an excitonically coupled chlorophyll dimer. We propose that reversible conformational changes in CP29 can “tune” the electronic coupling between the chlorophylls in this dimer, thereby modulating the energy of the chlorophyll-zeaxanthin charge-transfer state and switching on and off the charge-transfer quenching during qE.

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In higher plant chloroplasts, transthylakoid proton motive force serves both to drive the synthesis of ATP and to regulate light capture by the photosynthetic antenna to prevent photodamage. In vivo probes of the proton circuit in wild-type and a mutant strain of Arabidopsis thaliana show that regulation of light capture is modulated primarily by altering the resistance of proton efflux from the thylakoid lumen, whereas modulation of proton influx through cyclic electron flow around photosystem I is suggested to play a role in regulating the ATP͞NADPH output ratio of the light reactions.ATP synthase proton conductivity ͉ cyclic electron flow ͉ linear electron flow ͉ energy-dependent nonphotochemical quenching ͉ protein motive force P hotosynthesis converts light energy into chemical energy, ultimately powering the vast majority of our ecosystem (1). Higher plant photosynthesis is initiated through absorption of light by antennae complexes that funnel the energy to photosystem (PS) II and I. The photosystems operate in sequence with the plastoquinone pool, the cytochrome b 6 f complex, and plastocyanin to oxidize H 2 O and reduce NADP ϩ to NADPH in what is termed linear electron flow (LEF). LEF is coupled to proton translocation, establishing a transthylakoid electrochemical gradient of protons, termed the proton motive force (pmf ) (2), comprised of electric field (⌬ ) and pH (⌬pH) gradients (3). Dual Role of the pmfThe pmf plays two central roles in higher plant photosynthesis (4). First, pmf drives the normally endergonic synthesis of ATP through the CF 1 -CF 0 ATP synthase (ATP synthase) (5). Both the ⌬pH and ⌬ components of pmf contribute to ATP synthesis in a thermodynamically, and probably kinetically, equivalent fashion (6). Second, pmf is a key signal for initiating photoprotection of the photosynthetic reaction centers through energydependent nonphotochemical quenching (q E ), a process that harmlessly dissipates excessively absorbed light energy as heat (7-10). Only the ⌬pH component of pmf, through acidification of the lumen, is effective in initiating q E by activating violaxanthin de-epoxidase, a lumen-localized enzyme that converts violaxanthin to antheraxanthin and zeaxanthin, and by protonating lumen-exposed residues of PsbS, a pigment-binding protein of the PS II antenna complex (11). A Need for Flexibility in the Light ReactionsA major open question concerns how the light reactions achieve the flexibility required to meet regulatory needs and match downstream biochemical demands (12). In LEF to NADP ϩ , the synthesis of ATP and the production of NADPH are coupled, producing a fixed ATP͞NADPH output ratio. LEF alone is probably unable to satisfy the variable ATP͞NADPH output ratios required to power the sum of the Calvin-Benson cycle (13,14) and other metabolic processes (alternate electron and ATP sinks) that are variably engaged under different physiological conditions (12,15,16). Failure to match ATP͞NADPH output with demand will lead to buildup of products and depletion of substrates for the...