RpaA Regulates the Accumulation of Monomeric Photosystem I and PsbA under High Light Conditions in Synechocystis sp. PCC 6803

Waqar Majeed,Ryan Nastashia Blue,Qingfang He,Yan Zhang,Qiang Wang,Saurabh Ranade,Yong Xue,Rajagopal Subramanyam

doi:10.1371/journal.pone.0045139

Abstract

The response regulator RpaA was examined by targeted mutagenesis under high light conditions in Synechocystis sp. PCC 6803. A significant reduction in chlorophyll fluorescence from photosystem I at 77 K was observed in the RpaA mutant cells under high light conditions. Interestingly, the chlorophyll fluorescence emission from the photosystem I trimers at 77 K are similar to that of the wild type, while the chlorophyll fluorescence from the photosystem I monomers was at a much lower level in the mutant than in the wild type under high light conditions. The RpaA inactivation resulted in a dramatic reduction in the monomeric photosystem I and the D1 protein but not the CP47 content. However, there is no significant difference in the transcript levels of psaA or psbA or other genes examined, most of which are involved in photosynthesis, pigment biosynthesis, or stress responses. Under high light conditions, the growth of the mutant was affected, and both the chlorophyll content and the whole-chain oxygen evolution capability of the mutant were found to be significantly lower than those of the wild type, respectively. We propose that RpaA regulates the accumulation of the monomeric photosystem I and the D1 protein under high light conditions. This is the first report demonstrating that inactivation of a stress response regulator has specifically reduced the monomeric photosystem I. It suggests that PS I monomers and PS I trimers can be regulated independently for acclimation of cells to high light stress.

Highlights

Light is the ultimate energy for photosynthesis; excess excitation energy as a result of high light (HL) illumination can damage photosynthetic cells [1,2,3,4,5]
It has been well documented that the transfer of cyanobacterial cells from low light (LL) to HL results in reduction of photosystem contents, the photosytem I (PS I) content [14]
The PS I to PS II ratio decrease when cells are transferred from LL to HL

Summary

Introduction

Light is the ultimate energy for photosynthesis; excess excitation energy as a result of high light (HL) illumination can damage photosynthetic cells [1,2,3,4,5]. Photosynthetic organisms have evolved various mechanisms to acclimate to HL stress through altering the photosynthetic apparatus These mechanisms include changes in the reaction center pigment-protein complexes [6], state transitions [7,8,9], and stabilization of photosynthetic membranes [5,10]. The regulation of the photosytem I (PS I) and/or PS II content or the PS I to PS II ratio in response to changing light conditions is arguably one of the most critical processes in HL acclimation [10,11,12,13,14,15]. The more prominent decrease in PS I content than the PS II results in a decrease of the PS I to PS II ratio under HL conditions This process is triggered by the energy coupling between phycobilisome (PBS) and photosystems in response to varying light conditions. PmgA has been reported to be responsible for the down-regulation of PS I under HL conditions [13,17]; and the DspA protein (or Hik 33) has been reported to be responsible for transcriptional regulation of stress response and photosynthetic genes including PS I [18]

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