Chloroplasts respond to changes in the wavelengths and in tensities of ambient light (as a consequence of the time of day, cloudiness, etc.) by altering the relative outputs of PSI and PSII to maintain the appropriate balance of ATP and NADPH production. In order for PSII, which is preferentially located in the stacked grana, and PSI, which is preferentially located in the unstacked thylakoid membranes, to act in sequence during linear electron flow, the amount of light energy delivered to the two reaction centers must be controlled so that each center activates the same number of electrons. This balanced condition is called state 1 (Figure 1a). If the two photosystems are not equally excited, then cyclic electron flow occurs in PSI, and PSII becomes less active (state 2).
Fig1. Phosphorylation of LHCII and the regulation of linear versus cyclic electron flow. (a) (Top) In normal sunlight, PSI and PSII are equally activated, and the photosystems are organized in state 1. In this arrangement, light-harvesting complex II (LHCII) is not phosphorylated, and six copies of LHCII trimers, together with several other light harvesting proteins, encircle a dimeric PSII reaction center in a tightly associated supercomplex in the grana (for clarity, molecular details of the supercomplexes are not shown). As a result, PSII and PSI can function in parallel in linear electron flow. (Bottom) When light excitation of the two photosystems is unbalanced (e.g., too much light via PSII), LHCII becomes phosphorylated, dissociates from PSII, and diffuses into the unstacked membranes, where it associates with PSI and its permanently associated LHCI. In this alternative supramolecular organization (state 2), most of the absorbed light energy is transferred to PSI, supporting cyclic electron flow and ATP production, but no formation of NADPH and thus no CO2 fixation. (b) Model of a PSI “super-supercomplex” involved with PGRL1 dependent cyclic electron flow that was isolated from green algae in stage 2. The super-supercomplex contains multiple complexes, including the integral membrane protein PGRL1 (but not PGR5). See F. A. Wollman, 2001, EMBO J. 20:3623; and M. Iwai, et al., 2010, Nature 464:1210.
One mechanism underlying the regulation of the relative activities of PSI and PSII is the phosphorylation and dephosphorylation of thylakoid membrane proteins, including PSII and LHCII, mediated by several protein kinases and protein phosphatases. Changes in phosphorylation, particularly for LHCII, can alter the intra–thylakoid membrane distribution (grana vs. unstacked membranes) of this antenna complex and thus its differential interactions with PSI and PSII. The more LHCII is associated with a particular photosystem, the more efficiently that system will be activated by light, and the greater its contribution to electron flow.
Under certain conditions, LHCII’s nonphosphorylated form is preferentially associated with PSII, and the phosphorylated form diffuses in the thylakoid membrane from the grana to the unstacked region and associates with PSI more than the nonphosphorylated form does. Light conditions in which there is preferential absorption of light by PSII result in activation of an LHCII kinase, increased LHCII phosphorylation, compensatory increased activation of PSI relative to PSII, and thus an increase in cyclic electron flow in state 2 (see Figure 1a). When the green alga Chlamydomonas reinhardtii was forced into state 2, it was possible to isolate a “super-supercomplex” containing PSI, LHCI, LHCII, Cyt bf, ferredoxin (Fd), ferredoxin-NADP+ reductase (FNR), and the integral membrane protein PGRL1 that participates in cyclic electron flow—but not PGR5 (Figure 1b). Thus it appears that the efficient operation of electron-transport chains has involved the evolution of functional complexes of increasing size and complexity, from individual proteins to complexes to supercomplexes to super-supercomplexes.
Regulating the supramolecular organization of the photosystems in plants has the effect of directing them toward ATP production (state 2) or toward the generation of reducing equivalents (NADPH) and ATP (state 1), depending on ambient light conditions and the metabolic needs of the plant. Both NADPH and ATP are required to convert CO2 to sucrose or starch, the fourth stage in photosynthesis, which we cover in the last section of this chapter.
