Photosynthesis and Chloroplast Regulation—Balancing Photosynthesis and Photoprotection under Changing Environments

Light has opposing effects on chloroplasts: while it is an essential energy source for photosynthesis, it can also be detrimental to the photosynthetic apparatus. Thus, photosynthetic organisms have acquired a dual mechanism to utilize and dissipate light energy (photosynthesis and photoprotection, respectively) and have developed chloroplast plasticity to help optimize the balance between photosynthesis and photoprotection under changing environments. Nonetheless, such optimization has not been sufficiently achieved in many plants and algae, resulting in growth being generally restricted to optimal environments only, while suppressed under adverse conditions. Current photosynthesis research is addressing how this balance is established and could be further optimized to improve photosynthetic efficiency by genetic engineering. This special issue includes five review articles and three research articles that not only highlight such cutting edge research but also present and propose new directions in this field. We are hoping that these articles will inform readers about the field and stimulate them to integrate these newly developed ideas into their research. Schematic model for the photosynthetic electron transfer and photophoshorylation; two types of light-harvesting complexes (LHCI and LHCII) are mainly associated with two photosystem complexes (PSI and PSII), respectively, to harvest light energy and transfer excitons to the photosystems, respectively. PSII and PSI operate to drive the linear electron flow, while the cytochrome b6f complex (Cyt b6f) as well as plastoquinone (PQ) and two soluble components, plastocyanin (Pc) or cytochrome c6 (Cyt c6), link PSII with PSI. This linear electron flow produces NADPH via ferredoxin (Fd) and ferredoxin-NADP-reductase (FNR), and generates PMF. In addition, the cyclic electron flow also occurs through PSI and Cyt b6f to generate only PMF. The resulting PMF is used to generate ATP (from ADP) and Pi by ATP synthase. The function and structure of the components remain unchanged under constant or optimal environments, whereas they are flexibly remodeled under variable natural conditions. For example, in nature, light environments change drastically, and so, LHCIIs translocate between PSI and PSII to redistribute light energy as state transitions, which is controlled by phosphorylation/de-phosphorylation of the proteins involved. Some subunits of PSI, PSII, Cyt b6 and LHCI complexes also undergo phosphorylation/de-phosphorylation. Under high-light conditions, part of the light energy not used for photosynthesis triggers the shifting from photosynthesis to dissipation via non-photochemical quenching (NPQ), alleviating over-reduction of PSI which produces toxic reactive oxygen species (ROS). Schematic model for the photosynthetic electron transfer and photophoshorylation; two types of light-harvesting complexes (LHCI and LHCII) are mainly associated with two photosystem complexes (PSI and PSII), respectively, to harvest light energy and transfer excitons to the photosystems, respectively. PSII and PSI operate to drive the linear electron flow, while the cytochrome b6f complex (Cyt b6f) as well as plastoquinone (PQ) and two soluble components, plastocyanin (Pc) or cytochrome c6 (Cyt c6), link PSII with PSI. This linear electron flow produces NADPH via ferredoxin (Fd) and ferredoxin-NADP-reductase (FNR), and generates PMF. In addition, the cyclic electron flow also occurs through PSI and Cyt b6f to generate only PMF. The resulting PMF is used to generate ATP (from ADP) and Pi by ATP synthase. The function and structure of the components remain unchanged under constant or optimal environments, whereas they are flexibly remodeled under variable natural conditions. For example, in nature, light environments change drastically, and so, LHCIIs translocate between PSI and PSII to redistribute light energy as state transitions, which is controlled by phosphorylation/de-phosphorylation of the proteins involved. Some subunits of PSI, PSII, Cyt b6 and LHCI complexes also undergo phosphorylation/de-phosphorylation. Under high-light conditions, part of the light energy not used for photosynthesis triggers the shifting from photosynthesis to dissipation via non-photochemical quenching (NPQ), alleviating over-reduction of PSI which produces toxic reactive oxygen species (ROS). As shown in Fig. 1, the three-dimensional structures of the major proteins, including Pc (Xue et al. 1998), Cyt c6 (Kerfeld et al. 1995), ferredoxin (Binda et al. 1998) and ferredoxin–NADP reductase (Bruns and Karplus 1995), and multi-protein complexes, including PSI–LHCI (Mazor et al. 2017, Su et al. 2019, Suga et al. 2019), PSI–LHCI–LHCII supercomplexes (Pan et al. 2018, 2021, Huang et al. 2021), PSII–LHCII supercomplex (Su et al. 2017, Sheng et al. 2019), Cyt b6f complex (Stroebel et al. 2003, Malone et al. 2019) and ATP synthase (Hahn et al. 2018), have been determined at high resolution. Such structural information has provided the basis for elucidating the molecular mechanism by which the efficient light-harvesting, excitation energy transfer, photochemical reactions, electron transfer reactions, generation of PMF and ATP synthesis occur. Although detailed biophysical and biochemical mechanisms within these complexes or between complexes have been proposed, a detailed mechanistic understanding of how overall efficiency of photosynthesis is optimized under natural conditions, where environmental factors affecting photosynthesis efficiency constantly vary, requires further profound research. Light, which is collected by LHCs, is essential for photosynthesis; yet, excess light is hazardous to the photosynthetic machinery as it may lead to the formation of reactive oxygen species. Thus, photosynthetic organisms evolved to optimize light utilization to maximize photosynthetic energy conversion efficiency while minimizing photo-oxidative damage. Facing this challenge, algae and vascular plants developed molecular mechanisms to control electron transfer and the partitioning between ΔΨ and ΔpH as well as to modulate light-harvesting and light-dissipation processes. In addition, variable post-translational modifications, such as phosphorylation/de-phosphorylation as well as acetylation/deacetylation of subunits of LHCI, LHCII, PSI, PSII and Cyt b6f complexes, contribute to the remodeling of these complexes in the thylakoid membranes. These control mechanisms are mirrored by a dynamic plasticity of the photosynthetic machinery. In this issue, Hippler and Nelson (2021) shed light on this plasticity in regard to the structure and function of PSI and its associated light-harvesting proteins. They also take a closer look at the evolution of electron transfer between PSI and Pc or Cyt c6 in cyanobacteria, green algae and vascular plants. Similarly, Castell et al. (2021) have investigated the dynamic properties of electron transfer between Cyt f and PSI in the green and red branches of photosynthetic eukaryotes. In slight contrast, Sheng et al. (2021) direct their focus on the architectures and assemblies of PSII-light harvesting complex II (LHCII) supercomplexes in plants and green algae. They discuss the plasticity of peripheral small PSII subunits and the organization of major LHCII and assess energy transfer pathways that define their light-harvesting and photoprotective properties. The photo-protective mechanism of non-photochemical quenching (NPQ) in LHCII is highlighted as a defense line against photo-oxidative stress by Ruban and Wilson (2020). They focus on NPQ in vascular plants and in particular discuss the site of energy dependent quenching, qE, the fastest component of NPQ, and the possible molecular mechanisms that transmit ΔpH into conformational changes in major LHCII. Notably, these major LHCII as well as PSII core subunits are dynamically phosphorylated and de-phosphorylated in response to light conditions and metabolic demands. Longoni and Goldschmidt-Clermont (2021) describe and discuss evolutionarily conserved thylakoid protein kinases and counteracting protein phosphatases. As the authors explain, the combined action of kinases and phosphatases is responsible for phosphorylation dynamics, which are, for example, involved in the control of a process called ‘state transitions’. State transitions represent a regulatory feedback mechanism that modulates the distribution of PSII light-harvesting protein complexes between PSII and PSI. The dynamic allocation of these light-harvesting antenna proteins to PSII or PSI also contributes to the regulation of the redox poise of the electron transfer chain. Nutrient availability is another critical factor determining photosynthetic efficiency. In N-deficient plants, photosynthetic electron transport and CO2 fixation activity are unbalanced, leading to photoinhibition. Takahashi et al. (2021) analyzed the PSI and PSII photochemistry in rice plants acclimated to different N-levels and report that these two photosystems show coordinated responses to alleviate excess light energy. Besides post-translational regulation, post-transcriptional mechanisms are also important for the expression of photosynthetic proteins and for the assembly of photosynthetic protein complexes. In this issue, Yamamoto et al. (2021) identified a chloroplast-localized P-class pentatricopeptide repeat (PPR) protein, which is responsible for splicing of the group II intron in the ndhA transcript. The ndhA gene encodes a subunit of the chloroplast NADH dehydrogenase-like (NDH) complex, which mediates ferredoxin-dependent plastoquinone reduction in the thylakoid membrane of vascular plants as a component in the cyclic electron transfer. In the manuscript, the roles of NdhA in the assembly and stability of the NDH complex were also analyzed. In a related study, Higashi et al. (2021) investigated the function of PGR3, another P-class PPR protein that is required for the stabilization of petL operon RNA and the translation of the petL gene in plastids, where PetL is a small subunit of the Cyt b6f complex. In summary, the articles in this special issue review the field and shed new light on the structure and function of photosynthetic complexes, they address the importance of plasticity in regulation of photosynthetic electron transfer and photo-protection, and emphasize post-translational mechanisms involved in light acclimation and post-transcriptional mechanisms that are required for successful translation and assembly of photosynthetic protein complexes. Japan Society for the Promotion of Science [Grant-in-Aid for Scientific Research on Innovative Areas (JP16H06553 to J.M., JP16H06554 to Y.T.) and German Science Foundation (DFG. HI739/13-2 to M.H.). We thank Professor Wataru Sakamoto, Editor-in-Chief, Plant and Cell Physiology, for providing the opportunity for this Special Issue on Photosynthesis and Chloroplast Regulation and Dr. Liliana M. Costa, Managing Editor, for helpful advice and assistance. We wish to acknowledge the authors and reviewers who have contributed to this issue. The authors have no conflicts of interest to declare.