Connecting Chlorophyll Metabolism with Accumulation of the Photosynthetic Apparatus.

In plants, the chilling response involves decreased photosynthetic capacity and increased starch accumulation in chloroplasts. However, the mechanisms that modulate these processes remain unclear. We found that the SlWHY1 gene is significantly induced by chilling stress (4°C) in tomato. Three SlWHY1 overexpression (OE) lines grew better than the wild type (WT) under chilling stress; the OE plants retained intact photosynthetic grana lamellae and showed enhanced hydrolysis of starch. By contrast, RNAi lines that inhibited SlWHY1 were more affected than the corresponding WT cultivar. Their grana lamellae were damaged and starch content increased. The psbA gene encodes the key photosystem II (PSII) protein D1. We show that SlWHY1 binds to the upstream region (A/GTTACCCT/A) of SlpsbA and enhances the de novo synthesis of D1 in chloroplasts. Additionally, SlWHY1 regulates the expression of the starch-degrading enzyme α-amylase (SlAMY3-L) and the starch synthesis-related enzyme isoamylase gene (SlISA2) in the nucleus, thus modulating the starch content in chloroplasts. We demonstrate that SlWHY1 enhances the resistance of tomato to chilling stress by maintaining the function of PSII and degrading starch. Thus, overexpression of WHY1 may be an effective strategy for enhancing resistance to chilling stress of chilling-sensitive crops in agricultural production.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.15532

Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation.

Life on earth is sustained by oxygenic photosynthesis, a process that converts solar energy, carbon dioxide, and water into chemical energy and biomass. Sunlight is essential for growth and productivity of photosynthetic organisms. However, exposure to an excessive amount of light adversely affects fitness due to photooxidative damage to the photosynthetic machinery, primarily to the reaction center of the oxygen-evolving photosystem II (PSII). Photosynthetic organisms have evolved diverse photoprotective and adaptive strategies to avoid, alleviate, and repair PSII damage caused by high-irradiance or fluctuating light. Rapid and harmless dissipation of excess absorbed light within antenna as heat, which is measured by chlorophyll fluorescence as non-photochemical quenching (NPQ), constitutes one of the most efficient protective strategies. In parallel, an elaborate repair system represents another efficient strategy to maintain PSII reaction centers in active states. This article reviews both the reaction center-based strategy for robust repair of photodamaged PSII and the antenna-based strategy for swift control of PSII light-harvesting (NPQ). We discuss evolutionarily and mechanistically diverse strategies used by photosynthetic organisms to maintain PSII function for growth and productivity under static high-irradiance light or fluctuating light environments. Knowledge of mechanisms underlying PSII maintenance would facilitate bioengineering photosynthesis to enhance agricultural productivity and sustainability to feed a growing world population amidst climate change.

/pdf/a-new-light-on-photosystem-ii-maintenance-in-oxygenic-3xgzfixhtv.pdf

A New Light on Photosystem II Maintenance in Oxygenic Photosynthesis.

The reaction center (RC) of photosystem II (PSII), which is composed of D1, D2, PsbI, and cytochrome b559 subunits, forms at an early stage of PSII biogenesis. However, it is largely unclear how these components assemble to form a functional unit. In this work, we show that synthesis of the PSII core proteins D1/D2 and formation of the PSII RC is blocked specifically in the absence of ONE-HELIX PROTEIN1 (OHP1) and OHP2 proteins in Arabidopsis (Arabidopsis thaliana), indicating that OHP1 and OHP2 are essential for the formation of the PSII RC. Mutagenesis of the chlorophyll-binding residues in OHP proteins impairs their function and/or stability, suggesting that they may function in the binding of chlorophyll in vivo. We further show that OHP1, OHP2, and HIGH CHLOROPHYLL FLUORESCENCE244 (HCF244), together with D1, D2, PsbI, and cytochrome b559, form a complex. We designated this complex the PSII RC-like complex to distinguish it from the RC subcomplex in the intact PSII complex. Our data imply that OHP1, OHP2, and HCF244 are present in this PSII RC-like complex for a limited time at an early stage of PSII de novo assembly and of PSII repair under high-light conditions. In a subsequent stage of PSII biogenesis, OHP1, OHP2, and HCF244 are released from the PSII RC-like complex and replaced by the other PSII subunits. Together with previous reports on the cyanobacterium Synechocystis, our results demonstrate that the process of PSII RC assembly is highly conserved among photosynthetic species.

OHP1, OHP2, and HCF244 Form a Transient Functional Complex with the Photosystem II Reaction Center

LHC (light-harvesting complex) proteins of plants and algae are known to be involved both in collecting light energy for driving the primary photochemical reactions of photosynthesis and in photoprotection when the absorbed light energy exceeds the capacity of the photosynthetic apparatus. These proteins usually contain three transmembrane (TM) helices which span the thylakoid membranes and bind several chlorophyll, carotenoid and lipid molecules. In addition, the LHC protein family includes LHC-like proteins containing one, two, three or even four TM domains. One-helix proteins are not only present in eukaryotic photosynthetic organisms but also in cyanobacteria where they have been named high light-inducible proteins. These small proteins are probably the ancestors of the members of the extant LHC protein family which arouse through gene duplications, deletions and fusions. During evolution, some of these proteins have diverged and acquired novel functions. In most cases, LHC-like proteins are induced in response to various stress conditions including high light, high salinity, elevated temperature and nutrient limitation. Many of these proteins play key roles in photoprotection, notably in non-photochemical quenching of absorbed light energy. Moreover, some of these proteins appear to be involved in the regulation of chlorophyll synthesis and in the assembly and repair of Photosystem II and also of Photosystem I possibly by mediating the insertion of newly synthesized pigments into the photosynthetic reaction centers.

LHC-like proteins involved in stress responses and biogenesis/repair of the photosynthetic apparatus.

F-type ATP synthases produce nearly all of the ATP found in cells. The catalytic module F1 commonly comprises an α3β3 hexamer surrounding a γ/e stalk. However, it is unclear how these subunits assemble to form a catalytic motor. In this work, we identified and characterized a chloroplast protein that interacts with the CF1β, γ, and e subunits of the chloroplast ATP synthase and is required for assembly of its F1 module. We named this protein BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE1 (BFA1) and determined its crystal structure at 2.8-A resolution. BFA1 is comprised primarily of two interacting β-barrels that are oriented nearly perpendicularly to each other. The contact region between BFA1 and the CF1β and γ subunits was further mapped by yeast two-hybrid assays. An in silico molecular docking analysis was performed and revealed close fitting contact sites without steric conflicts between BFA1 and CF1β/γ. We propose that BFA1 acts mainly as a scaffold protein promoting the association of a CF1α/β heterodimer with CF1γ. The subsequent assembly of other CF1α/β heterodimers may shift the position of the CF1γ subunit to complete assembly of the CF1 module. This CF1 assembly process is likely to be valid for other F-type ATP synthases, as their structures are highly conserved.

/pdf/nucleus-encoded-protein-bfa1-promotes-efficient-assembly-of-2o7m1w3mm9.pdf

Nucleus-Encoded Protein BFA1 Promotes Efficient Assembly of the Chloroplast ATP Synthase Coupling Factor 1.

Chloroplast ribulose-5-phosphate-3-epimerase (RPE) is a critical enzyme involved in the Calvin-Benson cycle and oxidative pentose phosphate pathways in higher plants. Three Arabidopsis rpe mutants with reduced level of RPE were identified through their high NPQ (nonphotochemical quenching) phenotype upon illumination, and no significant difference of plant size was found between these rpe mutants and WT (wild type) plants under growth chamber conditions. A decrease in RPE expression to a certain extent leads to a decrease in CO2 fixation, V cmax and J max. Photosynthetic linear electron transport was partially inhibited and activity of ATP synthase was also decreased in the rpe mutants, but the levels of thylakoid protein complexes and other Calvin-Benson cycle enzymes in rpe mutants were not affected. These results demonstrate that some degree of reduction in RPE expression decreases carbon fixation in chloroplasts, which in turn feedback inhibits photosynthetic electron transport and ATP synthase activity due to the photosynthetic control. Taken together, this work provides evidence that RPE plays an important role in the Calvin-Benson cycle and influences the photosynthetic capacity of chloroplasts.

/pdf/reduction-in-chloroplastic-ribulose-5-phosphate-3-epimerase-rxx5xghg.pdf

Yonghong Li

Papers

OHP1, OHP2, and HCF244 Form a Transient Functional Complex with the Photosystem II Reaction Center

Nucleus-Encoded Protein BFA1 Promotes Efficient Assembly of the Chloroplast ATP Synthase Coupling Factor 1.

Reduction in chloroplastic ribulose-5-phosphate-3-epimerase decreases photosynthetic capacity in Arabidopsis