Photoinhibition of PSII occurs at the same quantum efficiency from very low to very high light, which raises a question about how important is the rate of photosynthetic electron transfer in photoinhibition. We modulated electron transfer rate and light intensity independently of each other in lincomycin-treated pea leaves and in isolated thylakoids, in order to elucidate the specific effects of light and PSII electron transport on photoinhibition. Major changes in the rate of electron transport caused only small changes in the rate of photoinhibition, suggesting the existence of a significant photoinhibitory pathway that contains an electron-transfer-independent phase. We compared the action spectrum of photoinhibition with absorption spectra of PSII components that could function as photoreceptors of the electron-transfer-independent phase of photoinhibition and found that the absorption spectra of Mn(III) and Mn(IV) compounds resemble the action spectrum of photoinhibition, showing a steep decrease from UV-C to blue light and a low visible-light tail. Our results show that the release of a Mn ion to the thylakoid lumen is the earliest detectable step of both UV- and visible-light-induced photoinhibition. After Mn release from the oxygen-evolving complex, oxidative damage to the PSII reaction center occurs because the Mn-depleted oxygen-evolving complex cannot reduce P680+ normally.

The eubacterial RNA polymerase core, a transcription machinery performing DNA-dependent RNA polymerization, consists of two α subunits and β, β′ and ω subunits. An additional σ subunit is recruited for promoter recognition and transcription initiation. Cyanobacteria, a group of eubacteria characterized by oxygenic photosynthesis, have a unique composition of the RNA polymerase (RNAP) core due to splitting of the β′ subunit to N-terminal γ and C-terminal β′ subunits. The physiological roles of the small ω subunit of RNAP, encoded by the rpoZ gene, are not yet completely understood in any bacteria. We found that although ω is non-essential in cyanobacteria, it has a major impact on the overall gene expression pattern. In ΔrpoZ strain, recruitment of the primary σ factor into the RNAP holoenzyme is inefficient, which causes downregulation of highly expressed genes and upregulation of many low-expression genes. Especially, genes encoding proteins of photosynthetic carbon concentrating and carbon fixing complexes were down, and the ΔrpoZ mutant showed low light-saturated photosynthetic activity and accumulated photoprotective carotenoids and α-tocopherol. The results indicate that the ω subunit facilitates the association of the primary σ factor with the RNAP core, thereby allowing efficient transcription of highly expressed genes.

SummaryThe photosystem II reaction centre protein D1 is encoded by the psbA gene. The D1 protein is stable in darkness but undergoes rapid turnover in the light. Here, we show that, in cyanobacterium Synechocystis sp. PCC6803, the synthesis of the D1 protein is regulated at the level of translation elongation in addition to the previously known transcriptional regulation. When Synechocystis sp. PCC6803 cells were transferred from light to darkness, the psbA mRNA remained abundant for hours. Cytosolic ribosomes were attached to psbA transcripts in the dark, and translation continued up to a distinct pausing site. However, ribosome nascent D1 chain complexes were not targeted to the thylakoid membrane, and no full-length D1 protein was produced in darkness. The arrest in translation elongation was released in the light, concomitantly with targeting of ribosome D1 nascent-chain complexes to the thylakoid membrane, allowing the synthesis of the full-length D1 protein. Downregulation of membrane targeting of ribosome complexes was also observed in the light if damage to the D1 protein was slow. This novel type of regulation of prokaryotic translation functions to balance the synthesis and degradation of the rapidly turning over photosystem II D1 protein in Synechocystis sp. PCC6803.

Photoinhibition is light-induced inactivation of PSII. Hypotheses about the photoreceptor(s) of photoinhibition include the Chl antenna of PSII, manganese of the oxygen-evolving complex (OEC), uncoupled Chl and iron-sulfur centres. We measured the action spectrum of photoinhibition in vivo from wild-type Arabidopsis thaliana L. and from the npq1-2 and npq4-1 mutants defective in non-photochemical quenching (NPQ) of excitations of the PSII antenna. The in vivo action spectrum was found to resemble closely the in vitro action spectra published for photoinhibition. We compared the action spectrum with absorbance spectra of model compounds of the OEC complex and other potential photoreceptors of photoinhibition. The comparison suggests that both manganese and Chl function as photoreceptors in photoinhibition. In accordance with the function of two types of photoreceptors in photoinhibition, NPQ was found to offer only partial protection against photoinhibition at visible wavelengths. The low protective efficiency of NPQ supports the conclusion that the Chl antenna of PSII is not the only photoreceptor of photoinhibition. Comparison of the action spectrum of photoinhibition with the emission spectrum of sunlight shows that the UV part of sunlight is responsible for the major part of photoinhibition under natural conditions.