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Thylakoids of land plants have a bipartite structure, consisting of cylindrical grana stacks, made of membranous discs piled one on top of the other, and stroma lamellae which are helically wound around the cylinders. Protein complexes predominantly located in the stroma lamellae and grana end membranes are either bulky [photosystem I (PSI) and the chloroplast ATP synthase (cpATPase)] or are involved in cyclic electron flow [the NAD(P)H dehydrogenase (NDH) and PGRL1–PGR5 heterodimers], whereas photosystem II (PSII) and its light-harvesting complex (LHCII) are found in the appressed membranes of the granum. Stacking of grana is thought to be due to adhesion between Lhcb proteins (LHCII or CP26) located in opposed thylakoid membranes. The grana margins contain oligomers of CURT1 proteins, which appear to control the size and number of grana discs in a dosage- and phosphorylation-dependent manner. Depending on light conditions, thylakoid membranes undergo dynamic structural changes that involve alterations in granum diameter and height, vertical unstacking of grana, and swelling of the thylakoid lumen. This plasticity is realized predominantly by reorganization of the supramolecular structure of protein complexes within grana stacks and by changes in multiprotein complex composition between appressed and non-appressed membrane domains. Reversible phosphorylation of LHC proteins (LHCPs) and PSII components appears to initiate most of the underlying regulatory mechanisms. An update on the roles of lipids, proteins, and protein complexes, as well as possible trafficking mechanisms, during thylakoid biogenesis and the de-etiolation process complements this review.

Diatoms constitute a major phylum of phytoplankton biodiversity in ocean water and freshwater ecosystems. They are known to respond to some chemical variations of the environment by the accumulation of triacylglycerol, but the relative changes occurring in membrane glycerolipids have not yet been studied. Our goal was first to define a reference for the glycerolipidome of the marine model diatom Phaeodactylum tricornutum, a necessary prerequisite to characterize and dissect the lipid metabolic routes that are orchestrated and regulated to build up each subcellular membrane compartment. By combining multiple analytical techniques, we determined the glycerolipid profile of P. tricornutum grown with various levels of nitrogen or phosphorus supplies. In different P. tricornutum accessions collected worldwide, a deprivation of either nutrient triggered an accumulation of triacylglycerol, but with different time scales and magnitudes. We investigated in depth the effect of nutrient starvation on the Pt1 strain (Culture Collection of Algae and Protozoa no. 1055/3). Nitrogen deprivation was the more severe stress, triggering thylakoid senescence and growth arrest. By contrast, phosphorus deprivation induced a stepwise adaptive response. The time scale of the glycerolipidome changes and the comparison with large-scale transcriptome studies were consistent with an exhaustion of unknown primary phosphorus-storage molecules (possibly polyphosphate) and a transcriptional control of some genes coding for specific lipid synthesis enzymes. We propose that phospholipids are secondary phosphorus-storage molecules broken down upon phosphorus deprivation, while nonphosphorus lipids are synthesized consistently with a phosphatidylglycerol-to-sulfolipid and a phosphatidycholine-to-betaine lipid replacement followed by a late accumulation of triacylglycerol.

The objective of this study was to investigate the response of light emitting diodes (LEDs) at different light intensities (70 and 80 for green LEDs, 88 and 238 for red LEDs and 80 and 238 μmol m−2 s−1 for blue LEDs) at three wavelengths in lettuce leaves. Lettuce leaves were exposed to (522 nm), red (639 nm) and blue (470 nm) LEDs of different light intensities. Thylakoid multiprotein complex proteins and photosynthetic metabolism were then investigated. Biomass and photosynthetic parameters increased with an increasing light intensity under blue LED illumination and decreased when illuminated with red and green LEDs with decreased light intensity. The expression of multiprotein complex proteins including PSII-core dimer and PSII-core monomer using blue LEDs illumination was higher at higher light intensity (238 μmol m−2 s−1) and was lowered with decreased light intensity (70–80 μmol m−2 s−1). The responses of chloroplast sub-compartment proteins, including those active in stomatal opening and closing, and leaf physiological responses at different light intensities, indicated induced growth enhancement upon illumination with blue LEDs. High intensity blue LEDs promote plant growth by controlling the integrity of chloroplast proteins that optimize photosynthetic performance in the natural environment.

Key message OsPPR6, a pentatricopeptide repeat protein involved in editing and splicing chloroplast RNA, is required for chloroplast biogenesis in rice. The chloroplast has its own genetic material and genetic system, but it is also regulated by nuclear-encoded genes. However, little is known about nuclear-plastid regulatory mechanisms underlying early chloroplast biogenesis in rice. In this study, we isolated and characterized a mutant, osppr6 , that showed early chloroplast developmental defects leading to albino leaves and seedling death. We found that the osppr6 mutant failed to form thylakoid membranes. Using map-based cloning and complementation tests, we determined that OsPPR6 encoded a new Pentatricopeptide Repeat (PPR) protein localized in plastids. In the osppr6 mutants, mRNA levels of plastidic genes transcribed by the plastid-encoded RNA polymerase decreased, while those of genes transcribed by the nuclear-encoded RNA polymerase increased. Western blot analyses validated these expression results. We further investigated plastidic RNA editing and splicing in the osppr6 mutants and found that the ndhB transcript was mis-edited and the ycf3 transcript was mis-spliced. Therefore, we demonstrate that OsPPR6, a PPR protein, regulates early chloroplast biogenesis and participates in editing of ndhB and splicing of ycf3 transcripts in rice.

The impact of water-stress on chloroplast development was studied by applying polyethylene glycol 6000 to the roots of 5-day-old etiolated rice ( Oryza sativa ) seedlings that were subsequently illuminated up to 72 h. Chloroplast development in drought environment led to down-regulation of light-harvesting Chl-proteins. Photosynthetic proteins of Photosystem II (PSII) and oxygen evolving complex i.e., Cytb559, OEC16, OEC23 and OEC33 as well as those of PSI such as PSI-III, PSI-V, and PSI-VI, decreased in abundance. Consequently, due to reduced light absorption by antennae, the electron transport rates of PSII and PSI decreased by 55% and 25% respectively. Further, seedling development in stress condition led to a decline in the ratio of variable (Fv) to maximum (Fm) Chl a fluorescence, as well in the quantum yield of PSII photochemistry. Addition of Mg 2+ to the thylakoid membranes suggested that Mg 2+ -induced grana stacking was not affected by water deficit. Proteomic analysis revealed the down-regulation of proteins involved in electron transport and in carbon reduction reactions, and up-regulation of antioxidative enzymes. Our results demonstrate that developing seedlings under water deficit could downsize their light-harvesting capacity and components of photosynthetic apparatus to prevent photo-oxidative stress, excess ROS generation and membrane lipid peroxidation.

The distinctive lateral organization of the protein complexes in the thylakoid membrane investigated by Jan Anderson and co-workers is dependent on the balance of various attractive and repulsive forces. Modulation of these forces allows critical physiological regulation of photosynthesis that provides efficient light-harvesting in limiting light but dissipation of excess potentially damaging radiation in saturating light. The light-harvesting complexes (LHCII) are central to this regulation, which is achieved by phosphorylation of stromal residues, protonation on the lumen surface and de-epoxidation of bound violaxanthin. The functional flexibility of LHCII derives from a remarkable pigment composition and configuration that not only allow efficient absorption of light and efficient energy transfer either to photosystem II or photosystem I core complexes, but through subtle configurational changes can also exhibit highly efficient dissipative reactions involving chlorophyll–xanthophyll and/or chlorophyll–chlorophyll interactions. These changes in function are determined at a macroscopic level by alterations in protein–protein interactions in the thylakoid membrane. The capacity and dynamics of this regulation are tuned to different physiological scenarios by the exact protein and pigment content of the light-harvesting system. Here, the molecular mechanisms involved will be reviewed, and the optimization of the light-harvesting system in different environmental conditions described.

Long-term acclimation of shade versus sun plants modulates the composition, function and structural organization of the architecture of the thylakoid membrane network. Significantly, these changes in the macroscopic structural organization of shade and sun plant chloroplasts during long-term acclimation are also mimicked following rapid transitions in irradiance: reversible ultrastructural changes in the entire thylakoid membrane network increase the number of grana per chloroplast, but decrease the number of stacked thylakoids per granum in seconds to minutes in leaves. It is proposed that these dynamic changes depend on reversible macro-reorganization of some light-harvesting complex IIb and photosystem II supracomplexes within the plant thylakoid network owing to differential phosphorylation cycles and other biochemical changes known to ensure flexibility in photosynthetic function in vivo. Some lingering grana enigmas remain: elucidation of the mechanisms involved in the dynamic architecture of the thylakoid membrane network under fluctuating irradiance and its implications for function merit extensive further studies.

A wheat stay-green mutant, tasg1, was previously generated via mutation breeding of HS2, a common wheat cultivar (Triticum aestivum L.). Compared with wild-type (WT) plants, tasg1 exhibited delayed senescence indicated by the slower degradation of chlorophyll. In this study, the stability of proteins in thylakoid membranes was evaluated in tasg1 under drought stress compared with WT plants in the field as well as in seedlings in the laboratory. Drought stress was imposed by controlling irrigation and sheltering the plants from rain in the field, and by polyethylene glycol (PEG)-6000 in the laboratory. The results indicated that tasg1 plants could maintain higher Hill activity, actual efficiency (ΦPSII), maximal photochemical efficiency of PSII (Fv/Fm), and Ca2+-ATPase and Mg2+-ATPase activities than the WT plants under drought stress. Furthermore, the abundance of some polypeptides in thylakoid membranes of tasg1 was greater than that in the WT under drought stress. Expression levels of TaLhcb4 and TaLhcb6 were higher in tasg1 compared with the WT. Under drought stress, the accumulation of superoxide radical (O2·–) and hydrogen peroxide (H2O2) was lower in tasg1 compared with the WT not only at the senescence stage but also at the seedling stages. These results suggest greater functional stability of thylakoid membrane proteins in tasg1 compared with the WT, and the higher antioxidant competence of tasg1 may play an important role in the enhanced drought tolerance of tasg1.

To maintain high photosynthetic rates, plants must adapt to their light environment on a timescale of seconds to minutes. Therefore, the light-harvesting antenna system of photosystem II in thylakoid membranes, light-harvesting complex II (LHCII), has a feedback mechanism, which determines the proportion of absorbed energy dissipated as heat: non-photochemical chlorophyll fluorescence quenching (NPQ). This is crucial to prevent photo-oxidative damage to photosystem II (PSII) and is controlled by the transmembrane pH differences (ΔpH). High ΔpH activates NPQ by protonation of the protein PsbS and the enzymatic de-epoxidation of LHCII-bound violaxanthin to zeaxanthin. But the precise role of PsbS and its interactions with different LHCII complexes remain uncertain. We have investigated PsbS–LHCII interactions in native thylakoid membranes using magnetic-bead-linked antibody pull-downs. The interaction of PsbS with the antenna system is affected by both ΔpH and the level of zeaxanthin. In the presence of ΔpH alone, PsbS is found to be mainly associated with the trimeric LHCII protein polypeptides, Lhcb1, Lhcb2 and Lhcb3. However, a combination of ΔpH and zeaxanthin increases the proportion of PsbS bound to the minor LHCII antenna complex proteins Lhcb4, Lhcb5 and Lhcb6. This pattern of interaction is not influenced by the presence of PSII reactions centres. Similar to LHCII particles in the photosynthetic membrane, PsbS protein forms clusters in the NPQ state. NPQ recovery in the dark requires uncoupling of PsbS. We suggest that PsbS acts as a ‘seeding’ centre for the LHCII antenna rearrangement that is involved in NPQ. The PsbS protein is essential in triggering non-photochemical quenching. Antibody pull-down assays show that a combination of ΔpH and zeaxanthin increases PsbS binding to specific minor proteins in the light-harvesting complex of photosystem II.

TAP38/STN7-dependent (de)phosphorylation of light-harvesting complex II (LHCII) regulates the relative excitation rates of photosystems I and II (PSI, PSII) (state transitions) and the size of the thylakoid grana stacks (dynamic thylakoid stacking). Yet, it remains unclear how changing grana size benefits photosynthesis and whether these two regulatory mechanisms function independently. Here, by comparing Arabidopsis wild-type, stn7 and tap38 plants with the psal mutant, which undergoes dynamic thylakoid stacking but lacks state transitions, we explain their distinct roles. Under low light, smaller grana increase the rate of PSI reduction and photosynthesis by reducing the diffusion distance for plastoquinol; however, this beneficial effect is only apparent when PSI/PSII excitation balance is maintained by state transitions or far-red light. Under high light, the larger grana slow plastoquinol diffusion and lower the equilibrium constant between plastocyanin and PSI, maximizing photosynthesis by avoiding PSI photoinhibition. Loss of state transitions in low light or maintenance of smaller grana in high light also both bring about a decrease in cyclic electron transfer and over-reduction of the PSI acceptor side. These results demonstrate that state transitions and dynamic thylakoid stacking work synergistically to regulate photosynthesis in variable light. The size of thylakoid stacks in chloroplasts changes depending on the light conditions. Studying mutants defective in biochemical adaptations showed that these dynamics work synergistically with state transitions to regulate photosynthesis in variable light.