As we’ve seen, electrons from reduced ferredoxin in PSI are transferred to NADP+ during linear electron flow, resulting in production of NADPH (see Figure 1). In some circumstances, however, especially when plants are stressed by conditions such as drought, high light intensity, or low carbon dioxide levels, cells must generate greater amounts of ATP relative to NADPH than they can produce by linear electron flow. To do this, they photosynthetically produce ATP from PSI without concomitant NADPH production. This is accomplished by a PSI-dependent and PSII- independent process called cyclic photophosphorylation, or cyclic electron flow (Figure 2). In this process, electrons cycle between PSI, ferredoxin, plastoquinone (Q), and the cytochrome bf complex, bypassing the ferredoxin-NADP+ reductase at PSI that normally generates NADPH. Thus, during cyclic electron flow, proton pumping permits additional ATP synthesis, but no net NADPH is generated, and there is no oxidization of H2O to produce O2.
Fig1. Linear electron flow in plants, which requires both chloroplast photosystems, PSI and PSII. Blue arrows indicate flow of electrons; red arrows indicate proton movement. LHCs are not shown. (Left) In the PSII reaction center, two sequential light-induced excitations of the same special-pair P680 chlorophyll result in a two-step reduction of the primary electron acceptor QB to QH2. On the luminal side of PSII, electrons removed from H2O by the oxygen-evolving complex are transferred to P680 +, restoring the reaction-center chlorophylls to the ground state after each excitation. The oxygen-evolving complex contains a cluster of four manganese ions (Mn, violet), a Ca2+ ion (green), and a Cl− ion (teal). These bound ions function in the split ting of H2O and maintain the environment essential for high rates of O2 evolution. Four sequential light-induced excitations of the P680 (double the number illustrated here) are required to oxidize two water molecules and release four protons and one molecule of molecular oxygen (O2). A tyrosine on the protein helps conducts electrons from the Mn ions to the oxidized reaction-center chlorophyll (P680 +), reducing it to the ground state (P680) after excitation by each photon. (Center) The cytochrome bf complex then accepts electrons from QH2 and transports two protons into the lumen. Operation of a Q cycle in the cytochrome bf complex translocates additional protons across the membrane to the thylakoid lumen, increasing the proton-motive force. (Right) In the PSI reaction center, each electron released from light-excited P700 chlorophylls moves via a series of carriers in the reaction center to the stromal surface, where soluble ferredoxin (an Fe-S protein) transfers the electron to ferredoxin-NADP+ reductase (FNR). This enzyme uses the prosthetic group flavin adenine dinucleotide (FAD) and a proton to reduce NADP+, forming NADPH. P700 + is restored to its ground state by addition of an electron carried from PSII via the cytochrome bf complex and plastocyanin, a soluble electron carrier.
Fig2. Cyclic electron flow in plants, which generates a proton-motive force and ATP but no oxygen or NADPH. In cyclic electron flow, light energy is used by PSI to transport electrons in a cycle to generate a proton-motive force and ATP without oxidizing water or generating NADPH. High-energy electrons are transferred via the ferredoxin of PSI either to a PGR5-PGRL1 heterodimer (red, left path way) or to the NADH dehydrogenase–like complex (blue, right path way), where they then reduce plastoquinone (Q) to QH2. Each of these two electron acceptors forms independent supercomplexes with PSI via light harvesting complex (LHC) subunits (yellow). (The PGR5-PGRL1 heterodimer and NADH dehydrogenase–like complex are not found together in the same supercomplex, but here are drawn together with only one PSI to emphasize the similarities of the two mechanisms of cyclic electron flow.) QH2 then transfers the electrons to the cytochrome bf complex, then to plastocyanin, and finally back to PSI, as is the case for the linear electron flow pathway (see Figure 1).
In higher plants, there are two cyclic electron flow path ways that control the ATP:NADPH ratio (see Figure 2). The major pathway is the PGR5-PGRL1-dependent path way, which we shall describe shortly; this pathway ensures efficient photosynthesis and protects against stress. The minor pathway is the NADH dehydrogenase–like complex dependent pathway, which appears to respond to stress and to be a target of H2O2-mediated regulation. The NADH dehydrogenase–like complex is a very large multiprotein complex that is very similar in shape and composition to mitochondrial complex I, which oxidizes NADPH or NADH while reducing Q to QH2. The NADH dehydrogenase–like complex, however, appears to lack the subunit necessary for NADPH oxidation.
During cyclic electron flow, high-energy electrons generated by light absorption and photoelectric transport in PSI are transferred either to the PGR5-PGRL1 heterodimer or to the NADH dehydrogenase–like complex from the ferredoxin subunit of PSI. Indeed, there is evidence that each of these two electron acceptors independently associates with PSI in supercomplexes mediated by LHC subunits. Both of these electron acceptors then reduce Q to QH2, which then delivers protons and electrons to the cytochrome bf complex via a Q cycle, as we described earlier for linear electron flow (see Figure 1). Protons are transported across the thylakoid membrane into the lumen by the cytochrome bf complex and possibly by the NADH dehydrogenase–like complex. Finally, plastocyanin returns the electrons from the cyto chrome bf complex to PSI to complete the cycle. This cyclic electron flow is similar to the cyclical process that occurs in the single photosystem of purple bacteria. The proton-motive force generated by cyclic electron flow drives ATP synthesis by the F0F1 complex (ATP synthase) and thus increases the ATP:NADPH ratio.
