The Response Regulator RpaB Binds to the Upstream Element of Photosystem I Genes To Work for Positive Regulation under Low-Light Conditions in Synechocystis sp. Strain PCC 6803

Abstract

The coordinated high-light response of genes encoding subunits of photosystem I (PSI) is achieved by the AT-rich region located just upstream of the core promoter in Synechocystis sp. strain PCC 6803. The upstream element enhances the basal promoter activity under low-light conditions, whereas this positive regulation is lost immediately after the shift to high-light conditions. In this study, we focused on a high-light regulatory 1 (HLR1) sequence included in the upstream element of every PSI gene examined. A gel mobility shift assay revealed that a response regulator RpaB binds to the HLR1 sequence in PSI promoters. Base substitution in the HLR1 sequence or decrease in copy number of the rpaB gene resulted in decrease in the promoter activity of PSI genes under low-light conditions. These observations suggest that RpaB acts as a transcriptional activator for PSI genes. It is likely that RpaB binds to the HLR1 sequence under low-light conditions and works for positive regulation of PSI genes and for negative regulation of high-light-inducible genes depending on the location of the HLR1 sequence within target promoters.In photosynthesis, light energy is absorbed by the light-harvesting antennae pigments and converted into chemical energy by the reaction centers. However, when the supply of light energy exceeds its consumption, elevated excitation pressure results in excess production of reactive oxygen species, leading to severe damage to many cellular processes (3,8,20). Thus, the absorption of excess light energy must be avoided under light-saturated conditions by decreasing the amount of lightharvesting antenna complexes per reaction center or the amount of reaction center complexes itself.In cyanobacteria, the decrease of photosystem (PS) content, as well as phycobilisome content, is typically observed under high-light (HL) conditions, and the main component to be downregulated is not PSII but PSI (14,22). The physiological significance of the selective repression of PSI content during HL acclimation has been demonstrated by the characterization of the two mutants of Synechocystis sp. strain PCC 6803, disruptants of pmgA (sll1968) and sll1961, both of which have defect in keeping their PSI content at low level under HL conditions (9, 14). They grew better than the wild-type cells during a short-term exposure (e.g., 24 h) to HL because a higher amount of PSI accelerated the rate of photosynthetic electron transport (14). Under prolonged HL conditions, however, the growth of the mutants was severely inhibited (9, 14, 30), presumably due to the generation of reactive oxygen species at the acceptor side of PSI. These observations strongly suggest that the repression of PSI content is indispensable for growth under continuous HL conditions.In Synechocystis sp. strain PCC 6803, the PSI complex is comprised of 11 subunits and genes encoding these subunits (PSI genes) are dispersed throughout the genome (11, 17). PSI genes are actively transcribed under low-light (LL) conditions, whereas their transcription is coord...

The Small Regulatory RNA SyR1/PsrR1 Controls Photosynthetic Functions in Cyanobacteria

“…The response regulator RpaB was shown to be a transcriptional activator of PSI genes (Seino et al, 2009) and a repressor of hliB under low-light conditions (Kappell and van Waasbergen, 2007) by binding to the HLR1 sequence. Hanaoka and Tanaka (2008) suggested that the upregulation of such high light-inducible genes as hliB (another potential target of PsrR1) and the downregulation of PSI genes are induced upon the release of RpaB from the HLR1 sequence directly after high-light shift.…”

“…As psaL is part of the RpaB regulon (Seino et al, 2009), a general disturbed transcriptional regulation of further photosynthesis components may be assumed. RpaA, another response regulator, was recently shown to regulate the accumulation of monomeric PSI under high-light conditions by an as yet unknown The model for the activity of transcription factors and their targets explains most of the physiological observations during acclimation to high light.…”

An Rrf2-Type Transcriptional Regulator Is Required for Expression of psaAB Genes in the Cyanobacterium Synechocystis sp. PCC 6803

“…Regarding the PSI genes, RpaB binds to promoter sequences of other PSI genes (i.e. psaC, psaD, psaE, psaF, psaK1, and psaL; Seino et al, 2008). On the other hand, the microarray analysis revealed that Slr0846 does not regulate these genes but only psaAB (Supplemental Table S1).…”

“…The high-light-induced down-regulation of psaAB can be accounted for by a transcriptional regulator RpaB (Rre26), since it binds to a high-light-responsive element1 just upstream of the P1 promoter of psaA (Eriksson et al, 2000;Seino et al, 2008). RpaB is an OmpR-type response regulator, of which DNA binding may be activated by phosphorylation from the stress-responsive His kinase Hik33 under the normal light conditions (Tu et al, 2004;Kappell and van Waasbergen, 2007), and suppressed by dephosphorylation under high-light conditions (Seki et al, 2007).…”

“…In addition, gel-shift assay suggested that the psaAB promoters have some putative protein binding sites. The psaAB gene expression may be regulated by several transcription factors that are activated individually; however, there was no report to specify the factors for psaAB except recent report of RpaB (Seino et al, 2008).…”