Abstract
Absorption of excess light energy by the photosynthetic machinery results in the generation of reactive oxygen species (ROS), such as H2O2. We investigated the effects in vivo of ROS to clarify the nature of the damage caused by such excess light energy to the photosynthetic machinery in the cyanobacterium Synechocystis sp. PCC 6803. Treatments of cyanobacterial cells that supposedly increased intracellular concentrations of ROS apparently stimulated the photodamage to photosystem II by inhibiting the repair of the damage to photosystem II and not by accelerating the photodamage directly. This conclusion was confirmed by the effects of the mutation of genes for H2O2-scavenging enzymes on the recovery of photosystem II. Pulse labeling experiments revealed that ROS inhibited the synthesis of proteins de novo. In particular, ROS inhibited synthesis of the D1 protein, a component of the reaction center of photosystem II. Northern and western blot analyses suggested that ROS might influence the outcome of photodamage primarily via inhibition of translation of the psbA gene, which encodes the precursor to D1 protein.
MeSH Terms
Bacterial Proteins/biosynthesis,genetics
Blotting, Northern
Blotting, Western
Cyanobacteria/drug effects,genetics,metabolism,radiation effects
Gene Expression Regulation, Bacterial/radiation effects
Genes, Bacterial
Hydrogen Peroxide/metabolism,toxicity
Light/adverse effects
Oxidative Stress
Paraquat/toxicity
Peptide Chain Elongation, Translational/radiation effects
Peptide Chain Initiation, Translational/radiation effects
Photosynthesis/radiation effects
Photosynthetic Reaction Center Complex Proteins/biosynthesis,genetics,metabolism,radiation effects
Photosystem II Protein Complex
RNA, Bacterial/biosynthesis,genetics
RNA, Messenger/biosynthesis,genetics
Radiation-Sensitizing Agents/toxicity
Reactive Oxygen Species/metabolism
Chemicals
Bacterial Proteins
Photosynthetic Reaction Center Complex Proteins
Photosystem II Protein Complex
RNA, Bacterial
RNA, Messenger
Radiation-Sensitizing Agents
Reactive Oxygen Species
photosystem II, psbA subunit
Hydrogen Peroxide
Paraquat
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nishiyama Y
Department of Regulation Biology, National Institute for Basic Biology, Myodaiji, Okazaki 444-8585, Japan.
Yamamoto H
Allakhverdiev S I
Inaba M
Yokota A
Murata N
References (24)
24 references, click to expand
-
Regulation of translation elongation in cyanobacteria: membrane targeting of the ribosome nascent-chain complexes controls the synthesis of D1 protein.
Mol Microbiol. 2001 Apr;40(2):476-84
PMID: 11309129
-
THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons.
Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:601-639
PMID: 15012221
-
Chilling-enhanced photooxidation: The production, action and study of reactive oxygen species produced during chilling in the light.
Photosynth Res. 1995 Aug;45(2):79-97
PMID: 24301474
-
Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique.
J Biol Chem. 1994 May 6;269(18):13244-53
PMID: 8175754
-
Too much of a good thing: light can be bad for photosynthesis.
Trends Biochem Sci. 1992 Feb;17(2):61-6
PMID: 1566330
-
Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803.
Mol Microbiol. 1997 Sep;25(6):1167-75
PMID: 9350872
-
Thioredoxin peroxidase in the Cyanobacterium Synechocystis sp. PCC 6803.
FEBS Lett. 1999 Mar 26;447(2-3):269-73
PMID: 10214959
-
Exposure of Synechocystis 6803 cells to series of single turnover flashes increases the psbA transcript level by activating transcription and down-regulating psbA mRNA degradation.
FEBS Lett. 1998 Oct 9;436(3):483-7
PMID: 9801173
-
In vivo role of catalase-peroxidase in synechocystis sp. strain PCC 6803.
J Bacteriol. 1999 Mar;181(6):1875-82
PMID: 10074082
-
Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities.
Mol Cell Biol. 2000 Feb;20(4):1116-23
PMID: 10648596
-
Photoinhibition of Photosystem II. Inactivation, protein damage and turnover.
Biochim Biophys Acta. 1993 Jul 5;1143(2):113-34
PMID: 8318516
-
Specific degradation of the D1 protein of photosystem II by treatment with hydrogen peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination.
Biochemistry. 1995 Aug 8;34(31):10019-26
PMID: 7632674
-
Altered mRNA binding activity and decreased translational initiation in a nuclear mutant lacking translation of the chloroplast psbA mRNA.
Mol Cell Biol. 1996 Jul;16(7):3560-6
PMID: 8668172
-
Effect of oxidative stress, produced by cumene hydroperoxide, on the various steps of protein synthesis. Modifications of elongation factor-2.
J Biol Chem. 1996 Sep 20;271(38):23105-10
PMID: 8798501
-
Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism.
Biochemistry. 1992 Nov 17;31(45):11072-83
PMID: 1332749
-
The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance.
Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8787-91
PMID: 8090724
-
Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress.
J Biol Chem. 1998 Jan 30;273(5):3027-32
PMID: 9446617
-
Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation.
Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1408-12
PMID: 11607279
-
Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis.
Biochemistry. 1995 Jul 25;34(29):9625-31
PMID: 7626631
-
Construction of an Obligate Photoheterotrophic Mutant of the Cyanobacterium Synechocystis 6803 : Inactivation of the psbA Gene Family.
Plant Physiol. 1987 Dec;85(4):1021-5
PMID: 16665796
-
Photochemical activity and components of membrane preparations from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin.
Biochim Biophys Acta. 1974 Aug 23;357(2):231-45
PMID: 4153919
-
Cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts.
EMBO J. 1996 Apr 1;15(7):1687-95
PMID: 8612593
-
A genetically engineered increase in fatty acid unsaturation in Synechococcus sp. PCC 7942 allows exchange of D1 protein forms and sustenance of photosystem II activity at low temperature.
Eur J Biochem. 1998 Feb 1;251(3):641-8
PMID: 9490036
-
Role of free radicals and catalytic metal ions in human disease: an overview.
Methods Enzymol. 1990;186:1-85
PMID: 2172697