Redox Control of psbA Gene Expression in the Cyanobacterium Synechocystis PCC 6803. Involvement of the Cytochrome b6/fComplex

Abstract

We investigated the role of the redox state of the photosynthetic and respiratory electron transport chains on the regulation of psbA expression in Synechocystis PCC 6803. Different means to modify the redox state of the electron carriers were used: (a) dark to oxidize the whole electron transport chain; (b) a shift from dark to light to induce its reduction; (c) the chemical interruption of the electron flow at different points to change the redox state of specific electron carriers; and (d) the presence of glucose to maintain a high reducing power in darkness. We show that changes in the redox state of the intersystem electron transport chain induce modifications of psbA transcript production and psbA mRNA stability. Reduction of the intersystem electron carriers activates psbA transcription and destabilizes the mRNA, while their oxidation induces a decrease in transcription and a stabilization of the transcript. Furthermore, our data suggest that the redox state of one of the electron carriers between the plastoquinone pool and photosystem I influences not only the expression of the psbA gene, but also that of other two photosynthetic genes, psaE and cpcBA. As a working hypothesis, we propose that the occupancy of the Q 0 site in the cytochrome b 6 /f complex may be involved in this regulation.

Transcriptional Regulation of the Respiratory Genes in the CyanobacteriumSynechocystissp. PCC 6803 during the Early Response to Glucose Feeding

“…In contrast, Glc expression of group II genes was abolished by the electron transport inhibitor Hg 21 or CN 2 , which would maintain the PQ pool in an oxidized or a reduced state, respectively, indicating the involvement of decreased cytosolic NADPH content rather than changes in membrane redox state in group II gene expression. If membrane redox were involved, then differential effects of Hg 21 and CN 2 would be expected; for instance, if the redox state of the PQ is critical, as has been shown for the expression of photosynthesis-related (Alfonso et al, 2000;Li and Sherman, 2000) and RNA synthesisrelated genes (Kujat and Owttrim, 2000), Hg 21 treatment Figure 5. Effects of respiration inhibitors (6-AN, Hg 21 , and CN 2 ) and an uncoupler (CCCP) on Glc-induced accumulation of respiratory gene transcripts in the dark.…”

“…These results also rule out the possibility that the Glc transporter (or homologs) and the glucokinase have regulatory roles as they do in higher plants and yeast (Rolland et al, 2002). During respiration, changes in the cellular redox state [NAD(P)H to NAD(P) 1 ratio], the redox state of respiratory electron transport, cytosolic pH, and energy charge in terms of the ATP to ADP ratio occur sequentially, resulting in the transcriptional regulation of genes encoding enzymes involved in respiratory electron transport in Streptomyces coelicolor A3(2) (Brekasis and Paget, 2003), photosynthesis (Alfonso et al, 2000;Li and Sherman, 2000), RNA synthesis (Kujat and Owttrim, 2000), and pigment biosynthesis (Ryu et al, 2004) in Synechocystis, and Glc repression in yeast (Rolland et al, 2002). By analogy, these changes could be candidate signals for the Glc-induced expression of the respiratory genes observed in this study.…”

“…Glc treatment induces changes in cytosolic and membrane redox states, cellular energy charge (ATP to ADP ratio), and cytosolic pH, which affect metabolism and hormone signaling, and mediates Glc repression of yeast genes (Rolland et al, 2002) and Glc induction of cyanobacterial genes (Alfonso et al, 2000;Kujat and Owttrim, 2000;Li and Sherman, 2000;Ryu et al, 2004). To see if Glc induction of respiratory gene expression is also mediated by these changes, we investigated the expression levels of 18 genes in wildtype cells treated with chemical inhibitors of the OPP pathway and oxidative phosphorylation, such as 6-aminonicotinamide (6-AN, G6PDH inhibitor; Varnes, 1988), Hg 21 (NDH-1 inhibitor; Mi et al, 1992), CN 2 (CtaI inhibitor), and carbonylcyanide-3-chlorophenyl hydrazone (CCCP; an uncoupler; Schmetterer, 1994).…”

Chloroplast redox signals: how photosynthesis controls its own genes

“…As in chloroplasts, the transcription of many cyanobacterial photosynthesis genes is influenced by light and photosynthetic electron transport [37][38][39]. Under photoautotrophic conditions, DCMU and DBMIB can be used to manipulate the redox state of the PQ pool in the same way as in chloroplasts [40,41]. Furthermore, the sequencing of the Arabidopsis genome revealed that many genes of cyanobacterial origin have been maintained throughout evolution, suggesting that, at least in part, its gene products could still have their former function [42].…”

A Novel Mechanism, Linked to Cell Density, Largely Controls Cell Division in Synechocystis

“…S2). The lower pigment content observed under HL might lead to a lower redox state of the electron transport chain (Alfonso et al, 2000), which might be a strategy to avoid the production of reactive oxygen species and the inhibition of photosynthesis (Hihara et al, 2001;Muramatsu et al, 2009), particularly when photoassimilates cannot be used for cell division. Interestingly, Kopecná et al (2012) showed that, even with a lower cellular chlorophyll content under HL, the rate of chlorophyll synthesis was higher than at lower light intensity.…”