Reversible protein phosphorylation in higher plants: focus on state transitions.

Reversible protein phosphorylation is one of the comprehensive mechanisms of cell metabolism regulation in eukaryotic organisms. The review describes the impact of the reversible protein phosphorylation on the regulation of growth and development as well as in adaptation pathways and signaling network in higher plant cells. The main part of the review is devoted to the role of the reversible phosphorylation of light-harvesting proteins of photosystem II and the state transition process in fine-tuning the photosynthetic activity of chloroplasts. A separate section of the review is dedicated to comparing the mechanisms and functional significance of state transitions in higher plants, algae, and cyanobacteria that allows the evolution aspects of state transitions meaning in various organisms to be discussed. Environmental factors affecting the state transitions are also considered. Additionally, we gain insight into the possible influence of STN7-dependent phosphorylation of the target proteins on the global network of reversible protein phosphorylation in plant cells as well as into the probable effect of the STN7 kinase inhibition on long-term acclimation pathways in higher plants.

Comparison of State Transitions of the Photosynthetic Antennae in Arabidopsis and Barley Plants upon Illumination with Light of Various Intensity.

Changes in the light energy distribution between the photosystems 1 and 2 (PS1 and PS2, respectively) due to the reversible migration of a part of the light-harvesting complex (LHC2) between the photosystems (state transitions, ST) have been studied in leaves of barley (Hordeum vulgare) and Arabidopsis thaliana plants upon short-term illumination with light of various intensity that excited predominantly PS2. Changes in the ratio of fluorescence maxima at 745 and 685 nm in the low-temperature (77 K) fluorescence spectrum of chlorophyll a (Chl a) characterizing energy absorption by the PS1 and PS2, respectively, were insufficient for revealing the differences in the STs in barley and Arabidopsis plants at various light intensities, because they were not associated with STs at high-intensity illumination. Light-induced accumulation of the LHC2 phosphorylated proteins Lhcb1 and Lhcb2 involved in the relocation of a part of the LHC2 from PS2 to PS1 in the leaves of both plants decreased with the increase in the light intensity and was more pronounced in barley than in Arabidopsis at the same light intensity. Relaxation of the non-photochemical quenching (NPQ) of Chl a fluorescence after illumination corresponding to the return of the part of LHC2 from PS1 to PS2 was observed in barley leaves in a wider range of increasing light intensities than in Arabidopsis leaves. The differences in the accumulation of phosphorylated Lhcb1 and Lhcb2, as well as in the parameters of NPQ relaxation after illumination, revealed that STs in barley leaves could occur not only at low-but also at high-intensity light, when it is absent in Arabidopsis leaves.

Effect of Light Intensity under Different Photoperiods on Expression Level of Carbonic Anhydrase Genes of the α- and ß-Families in Arabidopsis thaliana Leaves.

Changes in expression levels of genes encoding carbonic anhydrases α-CA1, α-CA2, α-CA4, ß-CA1, ß-CA2, ß-CA3, ß-CA4, ß-CA5, and ß-CA6 in Arabidopsis thaliana leaves after light increase from 80 to 400 µmol PAR quanta·m-2·s-1 were investigated under short day (8 h) and long day (16 h) photoperiods. The expression of two forms of the gene, At3g01500.2 and At3g01500.3, encoding the most abundant carbonic anhydrase of leaves, ß-CA1, situated in chloroplast stroma, was found. The content of At3g01500.3 transcripts was higher by approximately an order of magnitude compared to the content of At3g01500.2 transcripts. When plants were adapted to high light intensity under short day photoperiod, the expression level of both forms increased, whereas under long day photoperiod, the content of At3g01500.3 transcripts increased, and the content of transcripts of At3g01500.2 decreased. The expression levels of the At3g01500.3 gene and of genes encoding chloroplast carbonic anhydrases α-CA1, α-CA4, α-CA2 and cytoplasmic carbonic anhydrase ß-CA2 increased significantly in response to increase in light intensity under short day, and these of the first three genes increased under long day as well. The expression level of the gene encoding α-CA2 under long day photoperiod as well as of genes of chloroplast ß-CA5 and ß-CA4 from plasma membranes and mitochondrial ß-CA6 under both photoperiods depended insignificantly on light intensity. Hypotheses about the roles in higher plant metabolism of the studied carbonic anhydrases are discussed considering the effects of light intensity on expression levels of the correspondent genes.

Participation of Two Carbonic Anhydrases of the Alpha Family in Photosynthetic Reactions in Arabidopsis thaliana.

The expression of genes of two carbonic anhydrases (CA) belonging to the α-family, α-CA2 and α-CA4 (according to the nomenclature in N. Fabre et al. (2007) Plant Cell Environ., 30, 617-629), was studied in arabidopsis (Arabidopsis thaliana, var. Columbia) leaves. The expression of the At2g28210 gene coding α-CA2 decreased under increase in plant illumination, while the expression of the At4g20990 gene coding α-CA4 increased. Under conditions close to optimal for photosynthesis, in plants with gene At2g28210 knockout, the effective quantum yield of photosystem 2 and the light-induced accumulation of hydrogen peroxide in leaves were lower than in wild type plants, while the coefficient of non-photochemical quenching of leaf chlorophyll a fluorescence and the rate of CO2 assimilation in leaves were higher. In plants with At4g20990 gene knockout, the same characteristics changed in opposite ways relative to wild type. Possible mechanisms of the participation of α-CA2 and α-CA4 in photosynthetic reactions are discussed, taking into account that protons can be either consumed or released in the reactions they catalyze.

The size of the light-harvesting antenna of higher plant photosystem II is regulated by illumination intensity through transcription of antenna protein genes.

In arabidopsis plants, with an increase in illumination intensity during growth the extent of reduction of the plastoquinone pool in the photosynthetic electron transport chain increased, whereas the effective quantum yield of photosynthesis decreased. After 5 days of growth under high illumination intensity, these parameters in high light returned to values observed in "shade-adapted" plants in low light. During the same period, the size of the antenna decreased, correlating with a decrease in the amounts of proteins of peripheral pigment-protein complexes. It was found that the decrease in the amounts of these proteins occurred due to suppression of transcription of their genes.