Effect of water stress on the photosynthetic apparatus of plants and the protective role of cytokinins: a review

Characteristics of photosynthetic apparatus (the pool of pigments and proteins; the activity of photosystems; the intensities of in vivo photoassimilation of carbon dioxide and in vitro activity of enzymes of carbon metabolism; leaf structure; chloroplast structure), undergoing changes under the conditions of water deficiency, have been reviewed. The protective role of cytokinins is due to their regulatory effects on the renewal of disrupted cellular structures, the condition of the stomata, and de novo synthesis and activation of proteins that are required for increasing plant resistance to water stress.     

Heat stress: an overview of molecular responses in photosynthesis

The primary targets of thermal damage in plants are the oxygen evolving complex along with the associated cofactors in photosystem II (PSII), carbon fixation by Rubisco and the ATP generating system. Recent investigations on the combined action of moderate light intensity and heat stress suggest that moderately high temperatures do not cause serious PSII damage but inhibit the repair of PSII. The latter largely involves de novo synthesis of proteins, particularly the D1 protein of the photosynthetic machinery that is damaged due to generation of reactive oxygen species (ROS), resulting in the reduction of carbon fixation and oxygen evolution, as well as disruption of the linear electron flow. The attack of ROS during moderate heat stress principally affects the repair system of PSII, but not directly the PSII reaction center (RC). Heat stress additionally induces cleavage and aggregation of RC proteins; the mechanisms of such processes are as yet unclear. On the other hand, membrane linked sensors seem to trigger the accumulation of compatible solutes like glycinebetaine in the neighborhood of PSII membranes. They also induce the expression of stress proteins that alleviate the ROS-mediated inhibition of repair of the stress damaged photosynthetic machinery and are required for the acclimation process. In this review we summarize the recent progress in the studies of molecular mechanisms involved during moderate heat stress on the photosynthetic machinery, especially in PSII.     

Molecular mechanisms of stress resistance of the photosynthetic apparatus

The mechanisms of action of environmental stress-inducing factors on the photosynthetic apparatus (PA) of plants are considered. The basic targets for stress produced by heat, cold, salinity, osmotic imbalance, and high irradiance are analyzed. It is suggested that stress factors have an influence on the composition of thylakoid membranes and inhibit photosynthetic processes. However, recent studies demonstrated that strong light induces the photodamage to photosystem II (PS II) due to direct action of light on the oxygen-evolving complex. Stress-induced accumulation of reactive oxygen species (ROS) leads to inhibition of the recovery of the PSII by suppressing thede novo synthesis of photosynthetic proteins. In addition, stress stimulates the synthesis of protective low-molecular weight compounds (e.g., glycine betaine) and stress proteins. The major mechanisms of acclimation and protection of the PA against damaging effects of environmental stress-inducing factors are analyzed with special reference to cyanobacterial cells and mutants with high or low stress resistance.     

Evolution of cytokinin biosynthesis and degradation

Cytokinin hormones are important regulators of development and environmental responses of plants that execute their action via the molecular machinery of signal perception and transduction. The limiting step of the whole process is the availability of the hormone in suitable concentrations in the right place and at the right time to interact with the specific receptor. Hence, the hormone concentrations in individual tissues, cells, and organelles must be properly maintained by biosynthetic and metabolic enzymes. Although there are merely two active cytokinins, isopentenyladenine and its hydroxylated derivative zeatin, a variety of conjugates they may form and the number of enzymes/isozymes with varying substrate specificity involved in their biosynthesis and conversion gives the plant a variety of tools for fine tuning of the hormone level. Recent genome-wide studies revealed the existence of the respective coding genes and gene families in plants and in some bacteria. This review summarizes present knowledge on the enzymes that synthesize cytokinins, form cytokinin conjugates, and carry out irreversible elimination of the hormones, including their phylogenetic analysis and possible variations in different organisms.     

Effects of cytokinin preparations on the stability of the photosynthetic apparatus of two wheat cultivars under water deficiency

Carboxylase activities of the key enzyme of carbon metabolism, ribulose-bisphosphate carboxylase/oxygenase (RuBisCO; EC 4.1.1.39), and phosphoenolpyruvate carboxylase (PEPC; EC 4.1.1.31), as well as intensities of carbon dioxide photosynthetic assimilation in young seedlings and adult leaves of the wheat Triticum aestivum L. cultivars Mironovskaya 808 (a more tolerant) and Lyutestsens 758 (a less tolerant), were compared under conditions of progressive water deficiency. The water stress had more pronounced negative effects on all the studied characteristics of photosynthetic apparatus of cultivar Lyutestsens 758 photosynthetic machinery of the cultivar Lyutestsens 758. Its seedlings were more sensitive to water stress. Compounds with a cytokinin activity (6-benzylaminopurine, thidiazuron, cartolin 2, and cartolin 4) played a protective role, increasing the stability of the photosynthetic machinery under conditions of water deficiency. Preparations of cartolins displayed the maximum protective effect.     

Bioregulators protected photosynthetic machinery by inducing expression of photorespiratory genes under water stress in chickpea

Globally, water deficit is one of the major constraints in chickpea (Cicer arietinum L.) production due to substantial reduction in photosynthesis. Photorespiration often enhances under stress thereby protecting the photosynthetic apparatus from photoinhibition. Application of bioregulators is an alternative to counter adverse effects of water stress. Thus, in order to analyze the role of bioregulators in protecting the photosynthetic machinery under water stress, we performed an experiment with two contrasting chickpea varieties, i.e., Pusa 362 (Desi type) and Pusa 1108 (Kabuli type). Water deficit stress was imposed at the vegetative stage by withholding water. Just prior to exposure to water stress, plants were pretreated with thiourea (1,000 mg L^?1), benzyladenine (40 mg L^?1), and thidiazuron (10 mg L^?1). Imposed water deficit decreased relative water content (RWC), photosynthetic rate (P_N), quantum efficiency of PSII (F_v/F_m), and enhanced lipid peroxidation (LPO). However, bioregulator application maintained higher RWC, P_N, F_v/F_m, and lowered LPO under water stress. Expression of Rubisco large subunit gene (RbcL) was low under water stress both in the Kabuli and Desi type. However, bioregulators strongly induced its expression. Although poor expression of two important photorespiratory genes, i.e., glycolate oxidase and glycine decarboxylase H subunit, was observed in Desi chickpea under imposed stress, bioregulators in general and cytokinins in particular strongly induced their expression. This depicts that the application of bioregulators protected the photosynthetic machinery by inducing the expression of RbcL and photorespiratory genes during water deficit stress.     

Effect of water stress on the photosynthetic apparatus of plants and the protective role of cytokinins: A review

Characteristics of photosynthetic apparatus (the pool of pigments and proteins; the activity of photosystems; the intensities of in vivo photoassimilation of carbon dioxide and in vitro activity of enzymes of carbon metabolism; leaf structure; chloroplast structure), undergoing changes under the conditions of water deficiency, have been reviewed. The protective role of cytokinins is due to their regulatory effects on the renewal of disrupted cellular structures, the condition of the stomata, and de novo synthesis and activation of proteins that are required for increasing plant resistance to water stress.Translated from Prikladnaya Biokhimiya i Mikrobiologiya, Vol. 41, No. 2, 2005, pp. 133–147.Original Russian Text Copyright © 2005 by Chernyadev.     

Molecular events following perception of ultraviolet-B radiation by plants

Exposure of plants to UV-B radiation (280–320 nm) results in changes in expression of a large number of genes. Before UV-B radiation or light of other wavelengths can give rise to a cellular response, it has to be perceived by some kind of receptor, and the information transduced via a signalling pathway to the target molecules, be it proteins in the cytoplasm or the genetic material in the nucleus. The perception of low levels of UV-B probably occurs via a UV-B photoreceptor followed by several different signalling pathways. These pathways include second messengers such as calcium, kinases and the catalytic formation of reactive oxygen species. High levels of UV-B, on the other hand, probably cause cellular damage and oxidative stress, thus activating a general stress signal transduction pathway which leads to a response similar to that which occurs after pathogen attack and other stresses. Some of the genes identified so far as being regulated by UV-B encode proteins involved in the biosynthesis of protective pigments, DNA repair and antioxidative enzymes, photosynthetic genes, cell cycle genes, and stress genes induced by other types of stimuli (i.e. pathogenesis-related proteins and senescence-induced genes). In the light of the information obtained on components necessary for UV-B-induced changes in gene expression, we propose in this mini-review a working model for UV-B perception and signal transduction. This model also takes into account dosage differences for the observations, which imply a separation into UV-B-specific and more general stress signal transduction.     

Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts

In Arabidopsis thaliana, the Toc34 receptor component of the chloroplast import machinery is encoded by two independent but highly homologous genes, atToc33 and atToc34. We have isolated a T-DNA insertion mutant of atToc33 which is characterized by a pale phenotype, due to reductions in the levels of photosynthetic pigments, and alterations in protein composition. The latter involve not only chloroplast proteins but also some cytosolic polypeptides, including 14-3-3 proteins which, among other functions, have been proposed to be cytosolic targeting factors for nucleus-encoded chloroplast proteins. Within the chloroplast, many, though not all, proteins of the photosynthetic apparatus, as well as proteins not directly involved in photosynthesis, are found in significantly reduced amounts in the mutant. However, the accumulation of other chloroplast proteins is unaffected. This suggests that the atToc33 receptor is responsible for the import of a specific subset of nucleus-encoded chloroplast proteins. Supporting evidence for this conclusion was obtained by antisense repression of the atToc34 gene in the atToc33 mutant, which results in an exacerbation of the phenotype.Communicated by R. Hagemann     

Gene expression study of the flavodi-iron proteins from the cyanobacterium Synechocystis sp. PCC6803

The flavodi-iron proteins, also named FDPs, are an extensive family of enzymes able to reduce dioxygen to water and/or nitric oxide to nitrous oxide. These proteins are formed by a metallo-β-lactamase-like module with a di-iron catalytic site fused to a flavodoxin-like module bearing an FMN. However, in cyanobacteria, which are oxygenic photosynthetic organisms widespread in Nature, FDPs have an extra NAD(P)H:flavin reductase-like domain as a C-terminal extension. Interestingly, cyanobacteria contain more than one gene encoding FDP-like proteins, with the genome of Synechocystis sp. PCC6803 containing four genes coding for putative FDPs. However, the function of those proteins remains unclear. In the present study, we have analysed the expression profile of these genes under oxidative and nitrosative stress conditions. The results indicate that one of the flavodi-iron genes, the so-called flv1, is induced in cells exposed to nitrosative stress. By conducting a broad analysis on the primary sequences of FDPs, we have identified that the FDPs of cyanobacteria and oxygenic photosynthetic eukaryotes may be divided into multiple types (1-12), according to the amino acid residues of the di-iron catalytic site.     

Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery

When photosynthetic organisms are exposed to abiotic stress, their photosynthetic activity is significantly depressed. In particular, photosystem II (PSII) in the photosynthetic machinery is readily inactivated under strong light and this phenomenon is referred to as photoinhibition of PSII. Other types of abiotic stress act synergistically with light stress to accelerate photoinhibition. Recent studies of photoinhibition have revealed that light stress damages PSII directly, whereas other abiotic stresses act exclusively to inhibit the repair of PSII after light-induced damage (photodamage). Such inhibition of repair is associated with suppression, by reactive oxygen species (ROS), of the synthesis of proteins de novo and, in particular, of the D1 protein, and also with the reduced efficiency of repair under stress conditions. Gene-technological improvements in the tolerance of photosynthetic organisms to various abiotic stresses have been achieved via protection of the repair system from ROS and, also, by enhancing the efficiency of repair via facilitation of the turnover of the D1 protein in PSII. In this review, we summarize the current status of research on photoinhibition as it relates to the effects of abiotic stress and we discuss successful strategies that enhance the activity of the repair machinery. In addition, we propose several potential methods for activating the repair system by gene-technological methods.     

Regulatory role of membrane fluidity in gene expression and physiological functions

Plants, algae, and photosynthetic bacteria experience frequent changes in environment. The ability to survive depends on their capacity to acclimate to such changes. In particular, fluctuations in temperature affect the fluidity of cytoplasmic and thylakoid membranes. The molecular mechanisms responsible for the perception of changes in membrane fluidity have not been fully characterized. However, the understanding of the functions of the individual genes for fatty acid desaturases in cyanobacteria and plants led to the directed mutagenesis of such genes that altered the membrane fluidity of cytoplasmic and thylakoid membranes. Characterization of the photosynthetic properties of the transformed cyanobacteria and higher plants revealed that lipid unsaturation is essential for protection of the photosynthetic machinery against environmental stresses, such as strong light, salt stress, and high and low temperatures. The unsaturation of fatty acids enhances the repair of the damaged photosystem II complex under stress conditions. In this review, we summarize the knowledge on the mechanisms that regulate membrane fluidity, on putative sensors that perceive changes in membrane fluidity, on genes that are involved in acclimation to new sets of environmental conditions, and on the influence of membrane properties on photosynthetic functions.     

Mitochondrial DNA replication and repair defects: Clinical phenotypes and therapeutic interventions

Mitochondria is a unique cellular organelle involved in multiple cellular processes and is critical for maintaining cellular homeostasis. This semi-autonomous organelle contains its circular genome – mtDNA (mitochondrial DNA), that undergoes continuous cycles of replication and repair to maintain the mitochondrial genome integrity. The majority of the mitochondrial genes, including mitochondrial replisome and repair genes, are nuclear-encoded. Although the repair machinery of mitochondria is quite efficient, the mitochondrial genome is highly susceptible to oxidative damage and other types of exogenous and endogenous agent-induced DNA damage, due to the absence of protective histones and their proximity to the main ROS production sites. Mutations in replication and repair genes of mitochondria can result in mtDNA depletion and deletions subsequently leading to mitochondrial genome instability. The combined action of mutations and deletions can result in compromised mitochondrial genome maintenance and lead to various mitochondrial disorders. Here, we review the mechanism of mitochondrial DNA replication and repair process, key proteins involved, and their altered function in mitochondrial disorders. The focus of this review will be on the key genes of mitochondrial DNA replication and repair machinery and the clinical phenotypes associated with mutations in these genes.     

Reactive oxygen species and antioxidants: Relationships in green cells

The imposition of oxidative stress leads to increased production of reactive oxygen species (ROS) in plant cells. Orchestrated defense processes ensue that have much in common between stresses, yet are also particular to the site of action of the stress and its concentration. Possible functional roles of these responses include, but are not restricted to, the protection of the photosynthetic machinery, the preservation of membrane integrity and the protection of DNA and proteins. Superimposed upon our understanding of cellular mechanisms for protection against abiotic stress is a newly discovered role of ROS in signalling and defense response to pathogens (J. L. Dangl, R. A. Dietrich and M. S. Richberg. 1996. Plant Cell 8: 1793–1807). Evidence to date suggests a coordinated response to ROS among different members of the superoxide dismutase (SOD) gene families. A further layer of complexity is afforded by reports of coordination of expression between ascorbate peroxidase and SOD genes. Our understanding of the signalling mechanisms that underlie these coordinated events is in its infancy. An exciting future lies ahead in which the orchestration of successful antioxidant stress responses will be gradually revealed. Current data suggest that complex regulatory mechanisms function at both the gene and protein level to coordinate antioxidant responses and that a critical role is played by organellar localization and inter-compartment coordination.     

Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria

Using a bioinformatic approach, we analyzed the correspondence in genetic distance matrices between all possible pairwise combinations of 82 photosynthetic genes in 10 species of cyanobacteria. Our analysis reveals significant correlations between proteins linked in a conserved gene order and between structurally identified interacting protein scaffolds that coordinate the binding of cofactors involved in photosynthetic electron transport. Analyses of amino acid substitution rates suggest that the tempo of evolution of genes encoding core metabolic processes in the photosynthetic apparatus is highly constrained by protein-protein, protein-lipid, and protein-cofactor interactions (collectively called "protein interactions"). These interactions are critical for energy transduction, primary charge separation, and electron transport and effectively act as an internal selection pressure governing the conservation of clusters of photosynthetic genes in oxygenic prokaryotic photoautotrophs. Consequently, although several proteins within the photosynthetic apparatus are biophysically and physiologically inefficient, selection has not significantly altered the genes encoding these essential proteins over billions of years of evolution. In effect, these core proteins have become "frozen metabolic accidents."