A Redox-Responsive Regulator of Photosynthesis Gene Expression in the Cyanobacterium Synechocystis sp. Strain PCC 6803

Abstract

We have identified genes in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 that are involved with redox control of photosynthesis and pigment-related genes. The genes, rppA (sll0797) and rppB (sll0798), represent a two-component regulatory system that controls the synthesis of photosystem II (PSII) and PSI genes, in addition to photopigment-related genes. rppA (regulator of photosynthesis-and photopigment-related gene expression) and rppB exhibit strong sequence similarity to prokaryotic response regulators and histidine kinases, respectively. In the wild type, the steady-state mRNA levels of PSII reaction center genes increased when the plastoquinone (PQ) pool was oxidized and decreased when the PQ pool was reduced, whereas transcription of the PSI reaction center genes was affected in an opposite fashion. Such results suggested that the redox poise of the PQ pool is critical for regulation of the photosystem reaction center genes. In ⌬rppA, an insertion mutation of rppA, the PSII gene transcripts were highly up-regulated relative to the wild type under all redox conditions, whereas transcription of phycobilisome-related genes and PSI genes was decreased. The higher transcription of the psbA gene in ⌬rppA was manifest by higher translation of the D1 protein and a concomitant increase in O 2 evolution. The results demonstrated that RppA is a regulator of photosynthesis-and photopigment-related gene expression, is involved in the establishment of the appropriate stoichiometry between the photosystems, and can sense changes in the PQ redox poise.

Chloroplast redox signals: how photosynthesis controls its own genes

“…When the PQ pool is oxidized by PSI -light or 3-(3 0 ,4 0 -dichlorophenyl)-1,1 0 -dimethyl urea (DCMU), the opposite is the case. This has been shown for the cyanobacterial genes psbA, psbD, psaA and psaB, which encode the reaction-centre proteins D1, D2, PsaA and PsaB (light-blue boxes) [41] and the chloroplast genes psbA and psaAB (green oval insets) [36,74]. Data from another study in Synechocystis also show that the redox state of a photosynthetic electron carrier activates psbA in its oxidized state and psaE in its reduced state, supporting this model of opposite redox regulation of PSI and PSII genes [89].…”

“…In addition, it activates phycobilicyanin (PBC) transcription and inactivates phycobilisome (PBS) degradation. However, its detailed functions still needs to be resolved [41]. Abbreviations: Asp, aspartate; e 2 , electrons; Fd, ferredoxin; GSH, reduced glutathione; GSSG, oxidized glutathione; His, histidine; PC, plastocyanin; PSI, photosystem I; PSII, photosystem II; ROS, reactive oxygen species; Trx, thioredoxin.…”

“…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].…”

“…Experimental support for this came from a study in Synechocystis PCC 6803 that revealed a redox control pathway for reaction-centre genes with striking similarities to the chloroplast pathway described above. A reduced PQ pool, like in chloroplasts, activates the transcription of PSI reaction-centre genes whereas an oxidized PQ pool activates the transcription of PSII reaction centre genes [41] (Fig. 3).…”

“…Additional mutant analyses uncovered components responsible for the transduction of the signal: a twocomponent system consisting of a sensor kinase (RppB) and a response regulator (RppA) [41] (Fig. 3).…”