Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages

Complex I is the first and largest enzyme of the respiratory chain, playing a central role in cellular energy production by coupling electron transfer between NADH and ubiquinone to proton translocation. It is implicated in many common human neurodegenerative diseases. Here we report the first crystal structure of the entire, intact complex I (from T. thermophilus) at 3.3 Å resolution. The structure of the 536 kDa complex comprises 16 different subunits with 64 transmembrane helices and 9 Fe-S clusters. The core fold of subunit Nqo8 (NuoH/ND1) is, unexpectedly, similar to a half-channel of the antiporter-like subunits. Small subunits nearby form a linked second half-channel, thus completing the fourth proton translocation pathway, in addition to the channels in three antiporter-like subunits. The quinone-binding site is unusually long, narrow and enclosed. The quinone headgroup binds at the deep end of this chamber, near cluster N2. Strikingly, the chamber is linked to the fourth channel by a “funnel” of charged residues. The link continues over the entire membrane domain as a remarkable flexible central axis of charged and polar residues. It likely plays a leading role in the propagation of conformational changes, aided by coupling elements. The structure suggests that a unique, out-of-the-membrane quinone reaction chamber allows the redox energy to drive concerted long-range conformational changes in the four antiporter-like domains, resulting in translocation of four protons per cycle.

Photosynthesis provides at least two routes through which light energy can be used to generate a proton gradient across the thylakoid membrane of chloroplasts, which is subsequently used to synthesize ATP. In the first route, electrons released from water in photosystem II (PSII) are eventually transferred to NADP+ by way of photosystem I (PSI). This linear electron flow is driven by two photochemical reactions that function in series. The cytochrome b6f complex mediates electron transport between the two photosystems and generates the proton gradient (DeltapH). In the second route, driven solely by PSI, electrons can be recycled from either reduced ferredoxin or NADPH to plastoquinone, and subsequently to the cytochrome b6f complex. Such cyclic flow generates DeltapH and thus ATP without the accumulation of reduced species. Whereas linear flow from water to NADP+ is commonly used to explain the function of the light-dependent reactions of photosynthesis, the role of cyclic flow is less clear. In higher plants cyclic flow consists of two partially redundant pathways. Here we have constructed mutants in Arabidopsis thaliana in which both PSI cyclic pathways are impaired, and present evidence that cyclic flow is essential for efficient photosynthesis.

In this review we focus on photosynthetic behavior of overwintering evergreens with an emphasis on both the acclimative responses of photosynthesis to cold and the winter behavior of photosynthesis in conifers. Photosynthetic acclimation is discussed in terms of the requirement for a balance between the energy absorbed through largely temperature-insensitive photochemical processes and the energy used for temperature-sensitive biochemical processes and growth. Cold acclimation transforms the xanthophyll-mediated nonphotochemical antenna quenching of absorbed light from a short-term dynamic response to a long-term sustained quenching for the whole winter period. This acclimative response helps protect the evergreen foliage from photooxidative damage during the winter when photosynthesis is restricted or prevented by low temperatures. Although the molecular mechanisms behind the sustained winter excitation quenching are largely unknown, it does involve major alterations in the organization and composition of the photosystem II antenna. In addition, photosystem I may play an important role in overwintering evergreens not only by quenching absorbed light photochemically via its support of cyclic electron transport at low temperatures, but also by nonphotochemical quenching of absorbed light irrespective of temperature. The possible role of photosystem II reaction centers in nonphotochemical quenching of absorbed energy in overwintering evergreens is also discussed. Processes like chlororespiration and cyclic electron transport may also be important for maintaining the functional integrity of the photosynthetic apparatus of overwintering evergreens both during periods of thawing in winter and during recovery from winter stress in spring. We suggest that the photosynthetic acclimation responses of overwintering evergreens represent specific evolutionary adaptations for plant species that invest in the long-term maintenance of leaf structure in cold climatic zones as exemplified by the boreal forests of the Northern Hemisphere.