# Photosynthesis Research

## Current research articles..

The journal Photosynthesis Research is an international journal dealing with both basic and applied aspects of photosynthesis. The journal publishes research at all levels of plant organization: molecular, subcellular, cellular, whole plant, canopy, ecosystem and global.

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## Photosynthesis Research - Abstracts

On the origin of the slow M–T chlorophyll a fluorescence decline in cyanobacteria: interplay of short-term light-responses

### Abstract

The slow kinetic phases of the chlorophyll a fluorescence transient (induction) are valuable tools in studying dynamic regulation of light harvesting, light energy distribution between photosystems, and heat dissipation in photosynthetic organisms. However, the origin of these phases are not yet fully understood. This is especially true in the case of prokaryotic oxygenic photoautotrophs, the cyanobacteria. To understand the origin of the slowest (tens of minutes) kinetic phase, the M–T fluorescence decline, in the context of light acclimation of these globally important microorganisms, we have compared spectrally resolved fluorescence induction data from the wild type Synechocystis sp. PCC 6803 cells, using orange (λ = 593 nm) actinic light, with those of mutants, ΔapcD and ΔOCP, that are unable to perform either state transition or fluorescence quenching by orange carotenoid protein (OCP), respectively. Our results suggest a multiple origin of the M–T decline and reveal a complex interplay of various known regulatory processes in maintaining the redox homeostasis of a cyanobacterial cell. In addition, they lead us to suggest that a new type of regulatory process, operating on the timescale of minutes to hours, is involved in dissipating excess light energy in cyanobacteria.

Datum: 01.05.2018

Toward Escherichia coli bacteria machine for water oxidation

### Abstract

Nature uses a Mn oxide-based catalyst for water oxidation in plants, algae, and cyanobacteria. Mn oxides are among major candidates to be used as water-oxidizing catalysts. Herein, we used two straightforward and promising methods to form Escherichia coli bacteria/Mn oxide compounds. In one of the methods, the bacteria template was intact after the reaction. The catalysts were characterized by X-ray photoelectron spectroscopy, visible spectroscopy, scanning electron microscopy, high-resolution transmission electron microscopy, diffuse reflectance infrared Fourier transform spectroscopy, Raman spectroscopy, and X-ray diffraction spectrometry. Electrochemical properties of the catalysts were studied, and attributed redox potentials were assigned. The water oxidation of the compounds was examined under electrochemical condition. Linear sweep voltammetry showed that the onsets of water oxidation in our experimental condition for bacteria and Escherichia coli bacteria/Mn oxide were 1.68 and 1.56 V versus the normal hydrogen electrode (NHE), respectively. Thus, the presence of Mn oxide in the catalyst significantly decreased (~ 120 mV) the overpotential needed for water oxidation.

Datum: 01.05.2018

Engineering a carotenoid-binding site in Dokdonia sp. PRO95 Na + -translocating rhodopsin by a single amino acid substitution

### Abstract

Light-driven H+, Cl and Na+ rhodopsin pumps all use a covalently bound retinal molecule to capture light energy. Some H+-pumping rhodopsins (xanthorhodopsins; XRs) additionally contain a carotenoid antenna for light absorption. Comparison of the available primary and tertiary structures of rhodopsins pinpointed a single Thr residue (Thr216) that presumably prevents carotenoid binding to Na+-pumping rhodopsins (NaRs). We replaced this residue in Dokdonia sp. PRO95 NaR with Gly, which is found in the corresponding position in XRs, and produced a variant rhodopsin in a ketocarotenoid-synthesising Escherichia coli strain. Unlike wild-type NaR, the isolated variant protein contained the tightly bound carotenoids canthaxanthin and echinenone. These carotenoids were visible in the absorption, circular dichroism and fluorescence excitation spectra of the Thr216Gly-substituted NaR, which indicates their function as a light-harvesting antenna. The amino acid substitution and the bound carotenoids did not affect the NaR photocycle. Our findings suggest that the antenna function was recently lost during NaR evolution but can be easily restored by site-directed mutagenesis.

Datum: 01.05.2018

The effect of light quality on the pro-/antioxidant balance, activity of photosystem II, and expression of light-dependent genes in Eutrema salsugineum callus cells

### Abstract

The antioxidant balance, photochemical activity of photosystem II (PSII), and photosynthetic pigment content, as well as the expression of genes involved in the light signalling of callus lines of Eutrema salsugineum plants (earlier Thellungiella salsuginea) under different spectral light compositions were studied. Growth of callus in red light (RL, maximum 660 nm), in contrast to blue light (BL, maximum 450 nm), resulted in a lower H2O2 content and thiobarbituric acid reactive substances (TBARS). The BL increased the activities of key antioxidant enzymes in comparison with the white light (WL) and RL and demonstrated the minimum level of PSII photochemical activity. The activities of catalase (CAT) and peroxidase (POD) had the highest values in BL, which, along with the increased H2O2 and TBARS content, indicate a higher level of oxidative stress in the cells. The expression levels of the main chloroplast protein genes of PSII (PSBA and PSBD), the NADPH-dependent oxidase gene of the plasma membrane (RbohD), the protochlorophyllide oxidoreductase genes (POR B, C) involved in the biosynthesis of chlorophyll, and the key photoreceptor signalling genes (CIB1, CRY2, PhyB, PhyA, and PIF3) were determined. Possible mechanisms of light quality effects on the physiological parameters of callus cells are discussed.

Datum: 01.05.2018

Faster photosynthetic induction in tobacco by expressing cyanobacterial flavodiiron proteins in chloroplasts

### Abstract

Plants grown in the field experience sharp changes in irradiation due to shading effects caused by clouds, other leaves, etc. The excess of absorbed light energy is dissipated by a number of mechanisms including cyclic electron transport, photorespiration, and Mehler-type reactions. This protection is essential for survival but decreases photosynthetic efficiency. All phototrophs except angiosperms harbor flavodiiron proteins (Flvs) which relieve the excess of excitation energy on the photosynthetic electron transport chain by reducing oxygen directly to water. Introduction of cyanobacterial Flv1/Flv3 in tobacco chloroplasts resulted in transgenic plants that showed similar photosynthetic performance under steady-state illumination, but displayed faster recovery of various photosynthetic parameters, including electron transport and non-photochemical quenching during dark–light transitions. They also kept the electron transport chain in a more oxidized state and enhanced the proton motive force of dark-adapted leaves. The results indicate that, by acting as electron sinks during light transitions, Flvs contribute to increase photosynthesis protection and efficiency under changing environmental conditions as those found by plants in the field.

Datum: 01.05.2018

Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions

### Abstract

Assessment of photosynthetic traits and temperature tolerance was performed on field-grown modern genotype (MG), and the local landrace (LR) of wheat (Triticum aestivum L.) as well as the wild relative species (Aegilops cylindrica Host.). The comparison was based on measurements of the gas exchange (A/ci, light and temperature response curves), slow and fast chlorophyll fluorescence kinetics, and some growth and leaf parameters. In MG, we observed the highest CO2 assimilation rate $$\left( {{A_{{\text{C}}{{\text{O}}_2}}}} \right),$$ electron transport rate (Jmax) and maximum carboxylation rate $$\left( {{V_{{{\text{C}}_{\hbox{max} }}}}} \right)$$ . The Aegilops leaves had substantially lower values of all photosynthetic parameters; this fact correlated with its lower biomass production. The mesophyll conductance was almost the same in Aegilops and MG, despite the significant differences in leaf phenotype. In contrary, in LR with a higher dry mass per leaf area, the half mesophyll conductance (gm) values indicated more limited CO2 diffusion. In Aegilops, we found much lower carboxylation capacity; this can be attributed mainly to thin leaves and lower Rubisco activity. The difference in CO2 assimilation rate between MG and others was diminished because of its higher mitochondrial respiration activity indicating more intense metabolism. Assessment of temperature response showed lower temperature optimum and a narrow ecological valence (i.e., the range determining the tolerance limits of a species to an environmental factor) in Aegilops. In addition, analysis of photosynthetic thermostability identified the LR as the most sensitive. Our results support the idea that the selection for high yields was accompanied by the increase of photosynthetic productivity through unintentional improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions.

Datum: 01.05.2018

Influence of the variation potential on photosynthetic flows of light energy and electrons in pea

### Abstract

Local damage (mainly burning, heating, and mechanical wounding) induces propagation of electrical signals, namely, variation potentials, which are important signals during the life of plants that regulate different physiological processes, including photosynthesis. It is known that the variation potential decreases the rate of CO2 assimilation by the Calvin–Benson cycle; however, its influence on light reactions has been poorly investigated. The aim of our work was to investigate the influence of the variation potential on the light energy flow that is absorbed, trapped and dissipated per active reaction centre in photosystem II and on the flow of electrons through the chloroplast electron transport chain. We analysed chlorophyll fluorescence in pea leaves using JIP-test and PAM-fluorometry; we also investigated delayed fluorescence. The electrical signals were registered using extracellular electrodes. We showed that the burning-induced variation potential stimulated a nonphotochemical loss of energy in photosystem II under dark conditions. It was also shown that the variation potential gradually increased the flow of light energy absorbed, trapped and dissipated by photosystem II. These changes were likely caused by an increase in the fraction of absorbed light distributed to photosystem II. In addition, the variation potential induced a transient increase in electron flow through the photosynthetic electron transport chain. Some probable mechanisms for the influence of the variation potential on the light reactions of photosynthesis (including the potential role of intracellular pH decrease) are discussed in the work.

Datum: 01.05.2018

Acceleration of the excitation decay in Photosystem I immobilized on glass surface

### Abstract

Femtosecond transient absorption was used to study excitation decay in monomeric and trimeric cyanobacterial Photosystem I (PSI) being prepared in three states: (1) in aqueous solution, (2) deposited and dried on glass surface (either conducting or non-conducting), and (3) deposited on glass (conducting) surface but being in contact with aqueous solvent. The main goal of this contribution was to determine the reason of the acceleration of the excitation decay in dried PSI deposited on the conducting surface relative to PSI in solution observed previously using time-resolved fluorescence (Szewczyk et al., Photysnth Res 132(2):111–126, 2017). We formulated two alternative working hypotheses: (1) the acceleration results from electron injection from PSI to the conducting surface; (2) the acceleration is caused by dehydration and/or crowding of PSI proteins deposited on the glass substrate. Excitation dynamics of PSI in all three types of samples can be described by three main components of subpicosecond, 3–5, and 20–26 ps lifetimes of different relative contributions in solution than in PSI-substrate systems. The presence of similar kinetic components for all the samples indicates intactness of PSI proteins after their deposition onto the substrates. The kinetic traces for all systems with PSI deposited on substrates are almost identical and they decay significantly faster than the kinetic traces of PSI in solution. We conclude that the accelerated excitation decay in PSI-substrate systems is caused mostly by dense packing of proteins.

Datum: 01.05.2018

Red shift in the spectrum of a chlorophyll species is essential for the drought-induced dissipation of excess light energy in a poikilohydric moss, Bryum argenteum

### Abstract

Some mosses are extremely tolerant of drought stress. Their high drought tolerance relies on their ability to effectively dissipate absorbed light energy to heat under dry conditions. The energy dissipation mechanism in a drought-tolerant moss, Bryum argenteum, has been investigated using low-temperature picosecond time-resolved fluorescence spectroscopy. The results are compared between moss thalli samples harvested in Antarctica and in Japan. Both samples show almost the same quenching properties, suggesting an identical drought tolerance mechanism for the same species with two completely different habitats. A global target analysis was applied to a large set of data on the fluorescence-quenching dynamics for the 430-nm (chlorophyll-a selective) and 460-nm (chlorophyll-b and carotenoid selective) excitations in the temperature region from 5 to 77 K. This analysis strongly suggested that the quencher is formed in the major peripheral antenna of photosystem II, whose emission spectrum is significantly broadened and red-shifted in its quenched form. Two emission components at around 717 and 725 nm were assigned to photosystem I (PS I). The former component at around 717 nm is mildly quenched and probably bound to the PS I core complex, while the latter at around 725 nm is probably bound to the light-harvesting complex. The dehydration treatment caused a blue shift of the PS I emission peak via reduction of the exciton energy flow to the pigment responsible for the 725 nm band.

Datum: 01.05.2018

Crystal structure of Psb27 from Arabidopsis thaliana determined at a resolution of 1.85 Å

### Abstract

Proper biogenesis and maintenance of photosynthetic thylakoid membrane complexes are essential for the photosynthetic light reactions. A thylakoid lumenal protein, Psb27, plays a vital role in assembly or/and maintenance of photosystem II (PSII). In cyanobacteria, it is a small lipoprotein docked to the lumenal side of PSII, and functions in the assembly of the Mn4Ca cluster and in the PSII repair cycle. However, Psb27 from Arabidopsis thaliana is not a lipoprotein, and it is involved in PSII repair and acclimation to fluctuating light stress, suggesting a functional divergence between Arabidopsis Psb27 and cyanobacterial Psb27s. To gain a better understanding of Psb27 from higher plants, we determined the crystal structure of Arabidopsis Psb27 by X-ray crystallography at a resolution of 1.85 Å. The structure of Arabidopsis Psb27 is a four-helix bundle, similar to its orthologues from cyanobacteria. However, there are several structural differences between Arabidopsis Psb27 and cyanobacterial Psb27s concerning the overall molecular shape, the N- and C-terminal structures, and the surface charge. These differences suggest that Psb27 from higher plants and cyanobacteria may function differently.

Datum: 01.05.2018

Low oxygen affects photophysiology and the level of expression of two-carbon metabolism genes in the seagrass Zostera muelleri

### Abstract

Seagrasses are a diverse group of angiosperms that evolved to live in shallow coastal waters, an environment regularly subjected to changes in oxygen, carbon dioxide and irradiance. Zostera muelleri is the dominant species in south-eastern Australia, and is critical for healthy coastal ecosystems. Despite its ecological importance, little is known about the pathways of carbon fixation in Z. muelleri and their regulation in response to environmental changes. In this study, the response of Z. muelleri exposed to control and very low oxygen conditions was investigated by using (i) oxygen microsensors combined with a custom-made flow chamber to measure changes in photosynthesis and respiration, and (ii) reverse transcription quantitative real-time PCR to measure changes in expression levels of key genes involved in C4 metabolism. We found that very low levels of oxygen (i) altered the photophysiology of Z. muelleri, a characteristic of C3 mechanism of carbon assimilation, and (ii) decreased the expression levels of phosphoenolpyruvate carboxylase and carbonic anhydrase. These molecular-physiological results suggest that regulation of the photophysiology of Z. muelleri might involve a close integration between the C3 and C4, or other CO2 concentrating mechanisms metabolic pathways. Overall, this study highlights that the photophysiological response of Z. muelleri to changing oxygen in water is capable of rapid acclimation and the dynamic modulation of pathways should be considered when assessing seagrass primary production.

Datum: 01.05.2018

Properties and structure of a low-potential, penta-heme cytochrome c 552 from a thermophilic purple sulfur photosynthetic bacterium Thermochromatium tepidum

### Abstract

The thermophilic purple sulfur bacterium Thermochromatium tepidum possesses four main water-soluble redox proteins involved in the electron transfer behavior. Crystal structures have been reported for three of them: a high potential iron–sulfur protein, cytochrome c′, and one of two low-potential cytochrome c552 (which is a flavocytochrome c) have been determined. In this study, we purified another low-potential cytochrome c552 (LPC), determined its N-terminal amino acid sequence and the whole gene sequence, characterized it with absorption and electron paramagnetic spectroscopy, and solved its high-resolution crystal structure. This novel cytochrome was found to contain five c-type hemes. The overall fold of LPC consists of two distinct domains, one is the five heme-containing domain and the other one is an Ig-like domain. This provides a representative example for the structures of multiheme cytochromes containing an odd number of hemes, although the structures of multiheme cytochromes with an even number of hemes are frequently seen in the PDB database. Comparison of the sequence and structure of LPC with other proteins in the databases revealed several characteristic features which may be important for its functioning. Based on the results obtained, we discuss the possible intracellular function of this LPC in Tch. tepidum.

Datum: 24.04.2018

Correction to: Site, trigger, quenching mechanism and recovery of non-photochemical quenching in cyanobacteria: recent updates

In the original publication, under the subtitle Recovery: fluorescence recovery protein (FRP), paragraph 4 the text section enclosed in quotation marks does not occur in one of the original publications cited (Sluchanko et al. 2017a, b).

Datum: 23.04.2018

Time-dependent upregulation of electron transport with concomitant induction of regulated excitation dissipation in Haslea diatoms

### Abstract

Photoacclimation by strains of Haslea “blue” diatom species H. ostrearia and H. silbo sp. nov. ined. was investigated with rapid light curves and induction–recovery curves using fast repetition rate fluorescence. Cultures were grown to exponential phase under 50 µmol m−2 s−1 photosynthetic available radiation (PAR) and then exposed to non-sequential rapid light curves where, once electron transport rate (ETR) had reached saturation, light intensity was decreased and then further increased prior to returning to near growth light intensity. The non-sequential rapid light curve revealed that ETR was not proportional to the instantaneously applied light intensity, due to rapid photoacclimation. Changes in the effective absorption cross sections for open PSII reaction centres (σPSII′) or reaction centre connectivity (ρ) did not account for the observed increases in ETR under extended high light. σPSII′ in fact decreased as a function of a time-dependent induction of regulated excitation dissipation Y(NPQ), once cells were at or above a PAR coinciding with saturation of ETR. Instead, the observed increases in ETR under extended high light were explained by an increase in the rate of PSII reopening, i.e. QA oxidation. This acceleration of electron transport was strictly light dependent and relaxed within seconds after a return to low light or darkness. The time-dependent nature of ETR upregulation and regulated NPQ induction was verified using induction–recovery curves. Our findings show a time-dependent induction of excitation dissipation, in parallel with very rapid photoacclimation of electron transport, which combine to make ETR independent of short-term changes in PAR. This supports a selective advantage for these diatoms when exposed to fluctuating light in their environment.

Datum: 16.04.2018

Uphill energy transfer in photosystem I from Chlamydomonas reinhardtii . Time-resolved fluorescence measurements at 77 K

### Abstract

Energetic properties of chlorophylls in photosynthetic complexes are strongly modulated by their interaction with the protein matrix and by inter-pigment coupling. This spectral tuning is especially striking in photosystem I (PSI) complexes that contain low-energy chlorophylls emitting above 700 nm. Such low-energy chlorophylls have been observed in cyanobacterial PSI, algal and plant PSI–LHCI complexes, and individual light-harvesting complex I (LHCI) proteins. However, there has been no direct evidence of their presence in algal PSI core complexes lacking LHCI. In order to determine the lowest-energy states of chlorophylls and their dynamics in algal PSI antenna systems, we performed time-resolved fluorescence measurements at 77 K for PSI core and PSI–LHCI complexes isolated from the green alga Chlamydomonas reinhardtii. The pool of low-energy chlorophylls observed in PSI cores is generally smaller and less red-shifted than that observed in PSI–LHCI complexes. Excitation energy equilibration between bulk and low-energy chlorophylls in the PSI–LHCI complexes at 77 K leads to population of excited states that are less red-shifted (by ~ 12 nm) than at room temperature. On the other hand, analysis of the detection wavelength dependence of the effective trapping time of bulk excitations in the PSI core at 77 K provided evidence for an energy threshold at ~ 675 nm, above which trapping slows down. Based on these observations, we postulate that excitation energy transfer from bulk to low-energy chlorophylls and from bulk to reaction center chlorophylls are thermally activated uphill processes that likely occur via higher excitonic states of energy accepting chlorophylls.

Datum: 04.04.2018

Correction to: Photosystem I-LHCII megacomplexes respond to high light and aging in plants

### Abstract

The funding statement in the last sentence of the Acknowledgements section in the original publication is incorrect. The corrected Acknowledgements section is printed below.

Datum: 01.04.2018

Correction to: Arctic Micromonas uses protein pools and non-photochemical quenching to cope with temperature restrictions on Photosystem II protein turnover

In Table 2 of the original publication, all instances of krec in the Parameter and Equation columns should read krecinact.

Datum: 01.04.2018

Photoprotection in intact cells of photosynthetic bacteria: quenching of bacteriochlorophyll fluorescence by carotenoid triplets

### Abstract

Upon high light excitation in photosynthetic bacteria, various triplet states of pigments can accumulate leading to harmful effects. Here, the generation and lifetime of flash-induced carotenoid triplets (3Car) have been studied by observation of the quenching of bacteriochlorophyll (BChl) fluorescence in different strains of photosynthetic bacteria including Rvx. gelatinosus (anaerobic and semianaerobic), Rsp. rubrum, Thio. roseopersicina, Rba. sphaeroides 2.4.1 and carotenoid- and cytochrome-deficient mutants Rba. sphaeroides Ga, R-26, and cycA, respectively. The following results were obtained: (1) 3Car quenching is observed during and not exclusively after the photochemical rise of the fluorescence yield of BChl indicating that the charge separation in the reaction center (RC) and the carotenoid triplet formation are not consecutive but parallel processes. (2) The photoprotective function of 3Car is not limited to the RC only and can be described by a model in which the carotenoids are distributed in the lake of the BChl pigments. (3) The observed lifetime of 3Car in intact cells is the weighted average of the lifetimes of the carotenoids with various numbers of conjugated double bonds in the bacterial strain. (4) The lifetime of 3Car measured in the light is significantly shorter (1–2 μs) than that measured in the dark (2–10 μs). The difference reveals the importance of the dynamics of 3Car before relaxation. The results will be discussed not only in terms of energy levels of the 3Car but also in terms of the kinetics of transitions among different sublevels in the excited triplet state of the carotenoid.

Datum: 01.04.2018

Kinetics of photosystem II electron transport: a mathematical analysis based on chlorophyll fluorescence induction

### Abstract

The OJDIP rise in chlorophyll fluorescence during induction at different light intensities was mathematically modeled using 24 master equations describing electron transport through photosystem II (PSII) plus ordinary differential equations for electron budgets in plastoquinone, cytochrome f, plastocyanin, photosystem I, and ferredoxin. A novel feature of the model is consideration of electron in- and outflow budgets resulting in changes in redox states of Tyrosine Z, P680, and QA as sole bases for changes in fluorescence yield during the transient. Ad hoc contributions by transmembrane electric fields, protein conformational changes, or other putative quenching species were unnecessary to account for primary features of the phenomenon, except a peculiar slowdown of intra-PSII electron transport during induction at low light intensities. The lower than F m post-flash fluorescence yield F f was related to oxidized tyrosine Z. The transient J peak was associated with equal rates of electron arrival to and departure from QA and requires that electron transfer from QA to QB be slower than that from QA to QB. Strong quenching by oxidized P680 caused the dip D. Reduced plastoquinone, a competitive product inhibitor of PSII, blocked electron transport proportionally with its concentration. Electron transport rate indicated by fluorescence quenching was faster than the rate indicated by O2 evolution, because oxidized donor side carriers quench fluorescence but do not transport electrons. The thermal phase of the fluorescence rise beyond the J phase was caused by a progressive increase in the fraction of PSII with reduced QA and reduced donor side.

Datum: 01.04.2018

Effect of different methods of Ca 2+ extraction from PSII oxygen-evolving complex on the Q A − oxidation kinetics

### Abstract

Lumenal extrinsic proteins PsbO, PsbP, and PsbQ of photosystem II (PSII) protect the catalytic cluster Mn4CaO5 of oxygen-evolving complex (OEC) from the bulk solution and from soluble compounds in the surrounding medium. Extraction of PsbP and PsbQ proteins by NaCl-washing together with chelator EGTA is followed also by the depletion of Ca2+ cation from OEC. In this study, the effects of PsbP and PsbQ proteins, as well as Ca2+ extraction from OEC on the kinetics of the reduced primary electron acceptor (QA) oxidation, have been studied by fluorescence decay kinetics measurements in PSII membrane fragments. We found that in addition to the impairment of OEC, removal of PsbP and PsbQ significantly slows the rate of electron transfer from QA to the secondary quinone acceptor QB. Electron transfer from QA to QB in photosystem II membranes with an occupied QB site was slowed down by a factor of 8. However, addition of EGTA or CaCl2 to NaCl-washed PSII did not change the kinetics of fluorescence decay. Moreover, the kinetics of QA oxidation by QB in Ca-depleted PSII membranes obtained by treatment with citrate buffer at pH 3.0 (such treatment keeps all extrinsic proteins in PSII but extracts Ca2+ from OEC) was not changed. The results obtained indicate that the effect of NaCl-washing on the QA to QB electron transport is due to PsbP and PsbQ extrinsic proteins extraction, but not due to Ca2+ depletion.

Datum: 01.04.2018

Category: Current Chemistry Research

Last update: 28.03.2018.