In this review, we highlight recent research and current ideas on how to improve the efficiency of the light reactions of photosynthesis in crops. We note that the efficiency of photosynthesis is a balance between how much energy is used for growth and the energy wasted or spent protecting the photosynthetic machinery from photodamage. There are reasons to be optimistic about enhancing photosynthetic efficiency, but many appealing ideas are still on the drawing board. It is envisioned that the crops of the future will be extensively genetically modified to tailor them to specific natural or artificial environmental conditions.

Certain cyanobacteria synthesize chlorophyll (Chl) molecules (Chl d and Chl f) that absorb in the far-red region of the solar spectrum thereby extending the spectral range of photosynthetically active radiation 1,2. The synthesis and introduction of these far-red Chls into the photosynthetic apparatus of plants might improve the efficiency of oxygenic photosynthesis, especially in far-red enriched environments, such as in the lower regions of the canopy 3. Production of Chl f requires the ChlF subunit, also known as PsbA4 4 or super-rogue D1 5 , a paralog of the D1 subunit of photosystem II (PSII) which together with D2 binds co-factors involved in the light-driven oxidation of water. Current ideas suggest that ChlF oxidizes Chl a to Chl f in a homodimeric ChlF reaction center (RC) complex and represents a missing link in the evolution of the heterodimeric D1/D2 RC of PSII 4,6. However, unambiguous biochemical support for this proposal is lacking. Here we show that ChlF can substitute for D1 to form modified PSII complexes capable of producing Chl f. Remarkably mutation of just two residues in D1 converts oxygenevolving PSII into a Chl f synthase. Overall, we have identified a new class of PSII

The oxygen-evolving photosystem II (PSII) complex located in chloroplasts and cyanobacteria is sensitive to light-induced damage 1 which unless repaired causes reduction in photosynthetic capacity and growth. Although a potential target for crop improvement, the mechanism of PSII repair remains unclear. The D1 reaction center protein is the main target for photodamage 2 , with repair involving the selective degradation of the damaged protein by FtsH protease 3 . How a single damaged PSII subunit is recognised for replacement is unknown. Here, we have tested dark stability of PSII subunits in strains of the cyanobacterium Synechocystis PCC 6803 blocked at specific stages of assembly. We have found that when D1, which is normally shielded by the CP43 subunit, becomes exposed in a photochemically active PSII complex lacking CP43, it is selectively degraded by FtsH even in the dark. Removal of the CP47 subunit, which increases accessibility of FtsH to the D2 subunit, induced dark degradation of D2 at a faster rate than that of D1. In contrast CP47 and CP43 are resistant to degradation in the dark. Our results indicate that protease accessibility induced by PSII disassembly is an important determinant in the selection of the D1 and D2 subunits to be degraded by FtsH. 3The unusually high rate of synthesis and degradation, or turnover, of the D1 subunit of PSII, first observed over 40 years ago 4,5 , reflects the selective replacement of D1 during the repair of PSII in response to light damage. In the cyanobacterium Synechocystis sp. PCC 6803 (hereafter referred to as Synechocystis), degradation of D1 is mediated by a specific membrane-bound FtsH2/FtsH3 protease complex 3 . How FtsH complexes differentiate between damaged and undamaged D1 subunits is unclear 6 . Given that the D1 protein is shielded in PSII by the PSII inner antenna, CP43, several small transmembrane PSII subunits as well as extrinsic proteins on the lumenal side of the complex, one possibility is that at least partial disassembly of PSII, possibly triggered by photodamage, facilitates contacts between FtsH and D1. If selective degradation of D1 is primarily driven by accessibility, which does not need to be caused just by photo-oxidative damage to D1, one interesting prediction is that undamaged D1 might be preferentially degraded in the dark in PSII complexes that have been mutated to improve access.High resolution structures of cyanobacterial PSII have confirmed that the D1 and D2 reaction center subunits are shielded in the membrane by the intrinsic CP43 and CP47 subunits, and capped on the lumenal side of the membrane by three extrinsic subunits: PsbO, PsbU and PsbV (Fig. 1a) 7,8 . Synechocystis strains lacking the PsbO subunit still assemble oxygen-evolving PSII complexes but show a higher rate of D1 turnover than WT, possibly in response to an increase in the rate of photodamage to D1 due to perturbations on the donor side of PSII 9,10 . Enhanced D1 degradation in ΔPsbO might also be due to exposure of specific lumenal regions of D1 (normally hi...

Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

One strategy for enhancing photosynthesis in crop plants is to improve their ability to repair photosystem II (PSII) in response to irreversible damage by light. Despite the pivotal role of thylakoid-embedded FtsH protease complexes in the selective degradation of PSII subunits during repair, little is known about the factors involved in regulating FtsH expression. Here we show using the cyanobacterium Synechocystis sp. PCC 6803 that the Psb29 subunit, originally identified as a minor component of His-tagged PSII preparations, physically interacts with FtsH complexes in vivo and is required for normal accumulation of the FtsH2/FtsH3 hetero-oligomeric complex involved in PSII repair. We show using X-ray crystallography that Psb29 from Thermosynechococcus elongatus has a unique fold consisting of a helical bundle and an extended C-terminal helix and contains a highly conserved region that might be involved in binding to FtsH. A similar interaction is likely to occur in Arabidopsis chloroplasts between the Psb29 homologue, termed THF1, and the FTSH2/FTSH5 complex. The direct involvement of Psb29/THF1 in FtsH accumulation helps explain why THF1 is a target during the hypersensitive response in plants induced by pathogen infection. Downregulating FtsH function and the PSII repair cycle via THF1 would contribute to the production of reactive oxygen species, the loss of chloroplast function and cell death.This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’.