Papers by Yagut Allahverdiyeva

Plant & cell physiology, Jan 10, 2015
The flavodiiron proteins (FDPs) are involved in the detoxification of oxidative compounds like NO... more The flavodiiron proteins (FDPs) are involved in the detoxification of oxidative compounds like NO or O2 in Archaea and Bacteria. In cyanobacteria, the FDPs Flv1 and Flv3 are essential in the light dependent reduction of O2 downstream of Photosystem I.Phylogenetic analysis revealed that two genes (flvA and flvB) in the genome of Chlamydomonas reinhardtii show high homology to flv1 and flv3 genes of the cyanobacterium Synechocystis sp. PCC 6803. The physiological roles of these FDPs in eukaryotic green algae is not known, but is of special interest since these phototrophic organisms perform oxygenic photosynthesis similar to higher plants, which do not possess FDP homologs.We have analyzed the levels of flvA and flvB transcripts in C. reinhardtii cells under various environmental conditions and showed that these genes are highly expressed under ambient CO2 levels and during the early phase of adaptation to sulfur-deprivation, just before the onset of anaerobiosis and the induction of ...

Applied and Environmental Microbiology, 2014
We have investigated two approaches to enhance and extend H 2 photoproduction yields in heterocys... more We have investigated two approaches to enhance and extend H 2 photoproduction yields in heterocystous, N 2 -fixing cyanobacteria entrapped in thin alginate films. In the first approach, periodic CO 2 supplementation was provided to alginate-entrapped, N-deprived cells. N deprivation led to the inhibition of photosynthetic activity in vegetative cells and the attenuation of H 2 production over time. Our results demonstrated that alginate-entrapped ⌬hupL cells were considerably more sensitive to high light intensity, N deficiency, and imbalances in C/N ratios than wild-type cells. In the second approach, Anabaena strain PCC 7120, its ⌬hupL mutant, and Calothrix strain 336/3 films were supplemented with N 2 by periodic treatments of air, or air plus CO 2 . These treatments restored the photosynthetic activity of the cells and led to a high level of H 2 production in Calothrix 336/3 and ⌬hupL cells (except for the treatment air plus CO 2 ) but not in the Anabaena PCC 7120 strain (for which H 2 yields did not change after air treatments). The highest H 2 yield was obtained by the air treatment of ⌬hupL cells. Notably, the supplementation of CO 2 under an air atmosphere led to prominent symptoms of N deficiency in the ⌬hupL strain but not in the wild-type strain. We propose that uptake hydrogenase activity in heterocystous cyanobacteria not only supports nitrogenase activity by removing excess O 2 from heterocysts but also indirectly protects the photosynthetic apparatus of vegetative cells from photoinhibition, especially under stressful conditions that cause an imbalance in the C/N ratio in cells.

Journal of Plant Physiology, 2011
The bloom-forming cyanobacterium Nodularia spumigena produces toxic compounds, including nodulari... more The bloom-forming cyanobacterium Nodularia spumigena produces toxic compounds, including nodularin, which is known to have adverse effects on various organisms. We monitored the primary effects of nodularin exposure on physiological parameters in Spinachia oleracea. We present the first evidence for the uptake of nodularin by a terrestrial plant, and show that the exposure of spinach to cyanobacterial crude water extract from nodularin-producing strain AV1 results in inhibition of growth and bleaching of the leaves. Despite drastic effects on phenotype and survival, nodularin did not disturb the photosynthetic performance of plants or the structure of the photosynthetic machinery in the chloroplast thylakoid membrane. Nevertheless, the nodularin-exposed plants suffered from oxidative stress, as evidenced by a high level of oxidative modifications targeted to various proteins, altered levels of enzymes involved in scavenging of reactive oxygen species (ROS), and increased levels of ␣-tocopherol, which is an important antioxidant. Moreover, the high level of cytochrome oxidase (COX II), a typical marker for mitochondrial respiratory protein complexes, suggests that the respiratory capacity is increased in the leaves of nodularin-exposed plants. Actively respiring plant mitochondria, in turn, may produce ROS at high rates. Although the accumulation of ROS and induction of the ROS scavenging network enable the survival of the plant upon toxin exposure, the upregulation of the enzymatic defense system is likely to increase energetic costs, reducing growth and the ultimate fitness of the plants.
International Journal of Hydrogen Energy, 2012

Plant, Cell & Environment, 2014
Screening of 55 different cyanobacterial strains revealed that an extract from Nostoc XPORK14A dr... more Screening of 55 different cyanobacterial strains revealed that an extract from Nostoc XPORK14A drastically modifies the amplitude and kinetics of chlorophyll a fluorescence induction of Synechocystis PCC6803 cells.After 2 d exposure to the Nostoc XPORK14A extract, Synechocystis PCC 6803 cells displayed reduced net photosynthetic activity and significantly modified electron transport properties of photosystem II under both light and dark conditions. However, the maximum oxidizable amount of P700 was not strongly affected. The extract also induced strong oxidative stress in Synechocystis PCC 6803 cells in both light and darkness. We identified the secondary metabolite of Nostoc XPORK14A causing these pronounced effects on Synechocystis cells. Mass spectrometry and nuclear magnetic resonance analyses revealed that this compound, designated as M22, has a non-peptide structure. We propose that M22 possesses a dualaction mechanism: firstly, by photogeneration of reactive oxygen species in the presence of light, which in turn affects the photosynthetic machinery of Synechocystis PCC 6803; and secondly, by altering the in vivo redox status of cells, possibly through inhibition of protein kinases.

Advances in Photosynthesis and Respiration, 2011
ABSTRACT Plants as sessile organisms must be capable of rapidly coping with changes in environmen... more ABSTRACT Plants as sessile organisms must be capable of rapidly coping with changes in environmental conditions. In nature light is the most variable environmental parameter. During the day, plants must deal with changes of several orders of magnitude in the light quantity but also changes in light quality take place. Light is an absolute prerequisite for photosynthesis as an energy source; however, excess light can also be harmful and lead to a destruction of the photosynthetic apparatus. Photoinhibition of photosynthesis has been defined as a light-dependent decline in photosynthetic efficiency as a result of absorption of light. However, a strong consensus is still missing concerning the term photoinhibition and whether it describes a decrease in photosynthetic efficiency due to photodamage and thereby a reduction in the population of functional photosystems or regulatory adjustments, like reduced energy transfer from the antenna to reaction centers or both of these processes. Diurnal photoinhibition is a common phenomenon in most plants exposed to direct sunlight. Depending on the season and also on the diurnal cycle, plants have developed various adaptation systems to cope with highly, as well as frequently, changing light intensity and quality. Although a number of mechanisms have evolved to dissipate excess absorbed light energy by harmless pathways, the photosynthetic apparatus still remains a fragile system and vulnerable to damage by light. This chapter describes briefly the mechanisms of photoinhibition and plant response to light stress. In this chapter, we have used the term photoinhibition to describe the process that finally leads to a photodamage and repair of the reaction centers, while the dissipative regulatory processes are regarded as sole photoprotective processes.

Life (Basel, Switzerland), 2015
Flavodiiron proteins (FDPs, also called flavoproteins, Flvs) are modular enzymes widely present i... more Flavodiiron proteins (FDPs, also called flavoproteins, Flvs) are modular enzymes widely present in Bacteria and Archaea. The evolution of cyanobacteria and oxygenic photosynthesis occurred in concert with the modulation of typical bacterial FDPs. Present cyanobacterial FDPs are composed of three domains, the β-lactamase-like, flavodoxin-like and flavin-reductase like domains. Cyanobacterial FDPs function as hetero- and homodimers and are involved in the regulation of photosynthetic electron transport. Whilst Flv2 and Flv4 proteins are limited to specific cyanobacterial species (β-cyanobacteria) and function in photoprotection of Photosystem II, Flv1 and Flv3 proteins, functioning in the "Mehler-like" reaction and safeguarding Photosystem I under fluctuating light conditions, occur in nearly all cyanobacteria and additionally in green algae, mosses and lycophytes. Filamentous cyanobacteria have additional FDPs in heterocyst cells, ensuring a microaerobic environment for the...

Journal of Experimental Botany, 2014
Oxygenic photosynthetic organisms experience strong fluctuations in light intensity in their natu... more Oxygenic photosynthetic organisms experience strong fluctuations in light intensity in their natural terrestrial and aquatic growth environments. Recent studies with both plants and cyanobacteria have revealed that Photosystem (PS) I is the potential target of damage upon abrupt changes in light intensity. Photosynthetic organisms have, however, developed powerful mechanisms in order to protect their photosynthetic apparatus against such potentially hazardous light conditions. Although the electron transfer chain has remained relatively unchanged in both plant chloroplasts and their cyanobacterial ancestors, the photoprotective and regulatory mechanisms of photosynthetic light reactions have experienced conspicuous evolutionary changes. In cyanobacteria, the specific flavodiiron proteins (Flv1 and Flv3) are responsible for safeguarding PSI under rapidly fluctuating light intensities, whilst the thylakoid located terminal oxidases are involved in the protection of PSII during 12h diurnal cycles involving abrupt, square-wave, changes from dark to high light. Higher plants such as Arabidopsis thaliana have evolved different protective mechanisms. In particular, the PGR5 protein controls electron flow during sudden changes in light intensity by allowing the regulation mostly via the Cytochrome b6f complex. Besides the function of PGR5, plants have also acquired other dynamic regulatory mechanisms, among them the STN7-related LHCII protein phosphorylation that is similarly responsible for protection against rapid changes in the light environment. The green alga Chlamydomonas reinhardtii, as an evolutionary intermediate between cyanobacteria and higher plants, probably possesses both protective mechanisms. In this review, evolutionarily different photoprotective mechanisms under fluctuating light conditions are described and their contributions to cyanobacterial and plant photosynthesis are discussed.

Applied and Environmental Microbiology, 2014
We have investigated two approaches to enhance and extend H 2 photoproduction yields in heterocys... more We have investigated two approaches to enhance and extend H 2 photoproduction yields in heterocystous, N 2 -fixing cyanobacteria entrapped in thin alginate films. In the first approach, periodic CO 2 supplementation was provided to alginate-entrapped, N-deprived cells. N deprivation led to the inhibition of photosynthetic activity in vegetative cells and the attenuation of H 2 production over time. Our results demonstrated that alginate-entrapped ⌬hupL cells were considerably more sensitive to high light intensity, N deficiency, and imbalances in C/N ratios than wild-type cells. In the second approach, Anabaena strain PCC 7120, its ⌬hupL mutant, and Calothrix strain 336/3 films were supplemented with N 2 by periodic treatments of air, or air plus CO 2 . These treatments restored the photosynthetic activity of the cells and led to a high level of H 2 production in Calothrix 336/3 and ⌬hupL cells (except for the treatment air plus CO 2 ) but not in the Anabaena PCC 7120 strain (for which H 2 yields did not change after air treatments). The highest H 2 yield was obtained by the air treatment of ⌬hupL cells. Notably, the supplementation of CO 2 under an air atmosphere led to prominent symptoms of N deficiency in the ⌬hupL strain but not in the wild-type strain. We propose that uptake hydrogenase activity in heterocystous cyanobacteria not only supports nitrogenase activity by removing excess O 2 from heterocysts but also indirectly protects the photosynthetic apparatus of vegetative cells from photoinhibition, especially under stressful conditions that cause an imbalance in the C/N ratio in cells.
Plant J, 2013
These authors contributed equally to this work.

The Plant cell, 2014
During oxygenic photosynthesis, metabolic reactions of CO2 fixation require more ATP than is supp... more During oxygenic photosynthesis, metabolic reactions of CO2 fixation require more ATP than is supplied by the linear electron flow operating from photosystem II to photosystem I (PSI). Different mechanisms, such as cyclic electron flow (CEF) around PSI, have been proposed to participate in reequilibrating the ATP/NADPH balance. To determine the contribution of CEF to microalgal biomass productivity, here, we studied photosynthesis and growth performances of a knockout Chlamydomonas reinhardtii mutant (pgrl1) deficient in PROTON GRADIENT REGULATION LIKE1 (PGRL1)-mediated CEF. Steady state biomass productivity of the pgrl1 mutant, measured in photobioreactors operated as turbidostats, was similar to its wild-type progenitor under a wide range of illumination and CO2 concentrations. Several changes were observed in pgrl1, including higher sensitivity of photosynthesis to mitochondrial inhibitors, increased light-dependent O2 uptake, and increased amounts of flavodiiron (FLV) proteins. W...
Genome announcements, 2015
We announce the draft genome sequence of Calothrix strain 336/3, an N2-fixing heterocystous filam... more We announce the draft genome sequence of Calothrix strain 336/3, an N2-fixing heterocystous filamentous cyanobacterium isolated from a natural habitat. Calothrix 336/3 produces higher levels of hydrogen than Nostoc punctiforme PCC 73102 and Anabaena strain PCC 7120 and, therefore, is of interest for potential technological applications.

The Plant Journal, 2009
Physiological roles of the two distinct chloroplast-targeted ferredoxin-NADP + oxidoreductase (FN... more Physiological roles of the two distinct chloroplast-targeted ferredoxin-NADP + oxidoreductase (FNR) isoforms in Arabidopsis thaliana were studied using T-DNA insertion line fnr1 and RNAi line fnr2. In fnr2 FNR1 was present both as a thylakoid membrane-bound form and as a soluble protein, whereas in fnr1 the FNR2 protein existed solely in soluble form in the stroma. The fnr2 plants resembled fnr1 in having downregulated photosynthetic properties, expressed as low chlorophyll content, low accumulation of photosynthetic thylakoid proteins and reduced carbon fixation rate when compared with wild type (WT). Under standard growth conditions the level of F 0 'rise' and the amplitude of the thermoluminescence afterglow (AG) band, shown to correlate with cyclic electron transfer (CET), were reduced in both fnr mutants. In contrast, when plants were grown under low temperatures, both fnr mutants showed an enhanced rate of CET when compared with the WT. These data exclude the possibility that distinct FNR isoforms feed electrons to specific CET pathways. Nevertheless, the fnr2 mutants had a distinct phenotype upon growth at low temperature. The fnr2 plants grown at low temperature were more tolerant against methyl viologen (MV)-induced cell death than fnr1 and WT. The unique tolerance of fnr2 plants grown at low temperature to oxidative stress correlated with an increased level of reduced ascorbate and reactive oxygen species (ROS) scavenging enzymes, as well as with a scarcity in the accumulation of thylakoid membrane protein complexes, as compared with fnr1 and WT. These results emphasize a critical role for FNR2 in the redistribution of electrons to various reducing pathways, upon conditions that modify the photosynthetic capacity of the plant.

European Journal of Biochemistry, 2004
The His332 residue of the D1 protein has been identified as the likely ligand of the catalytic Mn... more The His332 residue of the D1 protein has been identified as the likely ligand of the catalytic Mn ions in the water oxi-However, its function has not been fully clarified. Here we used thermoluminescence and flash-induced chlorophyll fluorescence measurements to characterize the effect of the D1-H333E, D1-H332D and D1-H332S mutations on the electron transport of Photosystem II in intact cells of the cyanobacterium Synechocystis 6803. Although the mutants are not photoautotrophic they all show flash-induced thermoluminescence and chlorophyll fluorescence, which originate from the S 2 Q A and S 2 Q B recombinations demonstrating that charge stabilization takes place in the water oxidizing complex. However, the conversion of S 2 to higher S states is inhibited and the energetic stability of the S 2 Q A charge pair is increased by 75, 50 and 7 mV in the D1-H332D, D1-H332E and D1-H332S mutants, respectively. This is most probably caused by a decrease of E m (S 2 /S 1 ). Concomitantly, the rate of electron donation from Mn to Tyr-Z • during the S 1 to S 2 transition is slowed down, relative to the wild type, 350-and 60-fold in the D1-H332E and D1-H332D mutants, respectively, but remains essentially unaffected in D1-H332S. A further effect of the D1-H332E and D1-H332D mutations is the retardation of the Q A to Q B electron transfer step as an indirect consequence of the donor side modification. Our data show that although the His residue in the D1-332 position can be substituted by other metal binding residues for binding photo-oxidisable Mn it is required for controlling the functional redox energetics of the Mn cluster.
Proceedings of the National Academy of Sciences, 2013

Plant Molecular Biology, 2006
The mobile part of the light-harvesting chlorophyll (chl) a/b protein complex (LHCII), composed o... more The mobile part of the light-harvesting chlorophyll (chl) a/b protein complex (LHCII), composed of the Lhcb1 and Lhcb2 proteins, is the basic unit of chloroplast state transitions-the short term tuning system in balancing the excitation energy between Photosystem (PS) II and PSI. State transitions are catalysed by the thylakoid associated STN7 kinase, and we show here that besides the phosphorylation of the Lhcb1 and Lhcb2 proteins, also the phosphorylation of Lhcb4.2 (CP29) is under the control of the STN7 kinase. Upon growth of Arabidopsis WT and stn7 mutant plants under low and moderate light conditions, the WT plants favoured state 2 whereas stn7 was locked in state 1. The lack of the STN7 kinase and state transitions in stn7 also modified the thylakoid protein contents upon long-term low light acclimation resulting, for example, in low Lhcb1 and in elevated Lhca1 and Lhca2 protein amounts as compared to WT. Adjustments of thylakoid protein contents probably occurred at post-transcriptional level since the DNA microarray experiments from each growth condition did not reveal any significant differences between stn7 and WT transcriptomes. The resulting high Lhcb2/ Lhcb1 ratio in stn7 upon growth at low light was accompanied by lower capacity for NPQ than in WT. On the contrary, higher amounts of PsbS in stn7 under moderate and high light growth conditions resulted in higher NPQ compared to WT and consequently also in a protection of PSII against photoinhibition. STN7 kinase and the state transitions are suggested to have a physiological significance for dynamic acclimation to low but fluctuating growth light conditions. They are shown to function as a buffering system upon short high light illumination peaks by shifting the thylakoids from state 2 to state 1 and thereby down regulating the induction of stress-responsive genes, a likely result from transient over-reduction of PSI acceptors. Keywords Arabidopsis AE Light acclimation AE STN7 kinase AE Thylakoid protein phosphorylation Abbreviations chl chlorophyll F v /F m photochemical efficiency of PSII HSP heat shock protein LHCII light harvesting chlorophyll a/b protein complex NPQ non-photochemical energy quenching PSI photosystem I PSII photosystem II Introduction Light harvesting antenna complexes absorb sunlight and transfer the excitation energy to PSII and PSI complexes in order to drive photosynthetic electron M. Tikkanen and M. Piippo contributed equally to this work.
Uploads
Papers by Yagut Allahverdiyeva