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SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii.

ABSTRACT: Acclimation of Chlamydomonas reinhardtii cells to low levels of singlet oxygen, produced either by photoreactive chemicals or high light treatment, induces a specific genetic response that strongly increases the tolerance of the algae to subsequent exposure to normally lethal singlet oxygen-producing conditions. The genetic response includes the increased expression of various oxidative stress response and detoxification genes, like the glutathione peroxidase homologous gene GPXH/GPX5 and the ?-class glutathione-S-transferase gene GSTS1. To identify components involved in the signal transduction and activation of the singlet oxygen-mediated response, a mutant selection was performed. This selection led to the isolation of the singlet oxygen resistant 1 (sor1) mutant, which is more tolerant to singlet oxygen-producing chemicals and shows a constitutively higher expression of GPXH and GSTS1. Map-based cloning revealed that the SOR1 gene encodes a basic leucine zipper transcription factor, which controls its own expression and the expression of a large number of oxidative stress response and detoxification genes. In the promoter region of many of these genes, a highly conserved 8-bp palindromic sequence element was found to be enriched. This element was essential for GSTS1 induction by increased levels of lipophilic reactive electrophile species (RES), suggesting that it functions as an electrophile response element (ERE). Furthermore, GSTS1 overexpression in sor1 requires the ERE, although it is unknown whether it occurs through direct binding of SOR1 to the ERE. RES can be formed after singlet oxygen-induced lipid peroxidation, indicating that RES-stimulated and SOR1-mediated responses of detoxification genes are part of the singlet oxygen-induced acclimation process in C. reinhardtii.

SUBMITTER: Fischer BB

PROVIDER: S-EPMC3356615 | biostudies-literature | 2012 May

REPOSITORIES: biostudies-literature

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SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii.

Fischer Beat B BB Ledford Heidi K HK Wakao Setsuko S Huang ShihYau Grace SG Casero David D Pellegrini Matteo M Merchant Sabeeha S SS Koller Andreas A Eggen Rik I L RI Niyogi Krishna K KK

Proceedings of the National Academy of Sciences of the United States of America 20120423 20

Acclimation of Chlamydomonas reinhardtii cells to low levels of singlet oxygen, produced either by photoreactive chemicals or high light treatment, induces a specific genetic response that strongly increases the tolerance of the algae to subsequent exposure to normally lethal singlet oxygen-producing conditions. The genetic response includes the increased expression of various oxidative stress response and detoxification genes, like the glutathione peroxidase homologous gene GPXH/GPX5 and the σ- ...[more]

PMID: 22529359

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Project description:The protein superfamily of short-chain dehydrogenases/reductases (SDR), including members of the atypical type (aSDR), covers a huge range of catalyzed reactions and in vivo substrates. This superfamily also comprises isoflavone reductase-like (IRL) proteins, which are aSDRs highly homologous to isoflavone reductases from leguminous plants. The molecular function of IRLs in non-leguminous plants and green microalgae has not been identified as yet, but several lines of evidence point at their implication in reactive oxygen species homeostasis. The Chlamydomonas reinhardtii IRL protein IFR1 was identified in a previous study, analyzing the transcriptomic changes occurring during the acclimation to sulfur deprivation and anaerobiosis, a condition that triggers photobiological hydrogen production in this microalgae. Accumulation of the cytosolic IFR1 protein is induced by sulfur limitation as well as by the exposure of C. reinhardtii cells to reactive electrophile species (RES) such as reactive carbonyls. The latter has not been described for IRL proteins before. Over-accumulation of IFR1 in the singlet oxygen response 1 (sor1) mutant together with the presence of an electrophile response element, known to be required for SOR1-dependent gene activation as a response to RES, in the promoter of IFR1, indicate that IFR1 expression is controlled by the SOR1-dependent pathway. An implication of IFR1 into RES homeostasis, is further implied by a knock-down of IFR1, which results in a diminished tolerance toward RES. Intriguingly, IFR1 knock-down has a positive effect on photosystem II (PSII) stability under sulfur-deprived conditions used to trigger photobiological hydrogen production, by reducing PSII-dependent oxygen evolution, in C. reinhardtii. Reduced PSII photoinhibition in IFR1 knock-down strains prolongs the hydrogen production phase resulting in an almost doubled final hydrogen yield compared to the parental strain. Finally, IFR1 knock-down could be successfully used to further increase hydrogen yields of the high hydrogen-producing mutant stm6, demonstrating that IFR1 is a promising target for genetic engineering approaches aiming at an increased hydrogen production capacity of C. reinhardtii cells.

Project description:When photosynthetic organisms are exposed to harsh environmental conditions such as high light intensities or cold stress, the production of reactive oxygen species like singlet oxygen is stimulated in the chloroplast. In Chlamydomonas reinhardtii singlet oxygen was shown to act as a specific signal inducing the expression of the nuclear glutathione peroxidase gene GPXH/GPX5 during high light stress, but little is known about the cellular mechanisms involved in this response. To investigate components affecting singlet oxygen signaling in C. reinhardtii, a mutant screen was performed.Mutants with altered GPXH response were isolated from UV-mutagenized cells containing a GPXH-arylsulfatase reporter gene construct. Out of 5500 clones tested, no mutant deficient in GPXH induction was isolated, whereas several clones showed constitutive high GPXH expression under normal light conditions. Many of these GPXH overexpressor (gox) mutants exhibited higher resistance to oxidative stress conditions whereas others were sensitive to high light intensities. Interestingly, most gox mutants produced increased singlet oxygen levels correlating with high GPXH expression. Furthermore, different patterns of altered photoprotective parameters like non-photochemical quenching, carotenoid contents and ?-tocopherol levels were detected in the various gox mutants.Screening for mutants with altered GPXH expression resulted in the isolation of many gox mutants with increased singlet oxygen production, showing the relevance of controlling the production of this ROS in photosynthetic organisms. Phenotypic characterization of these gox mutants indicated that the mutations might lead to either stimulated triplet chlorophyll and singlet oxygen formation or reduced detoxification of singlet oxygen in the chloroplast. Furthermore, changes in multiple protection mechanisms might be responsible for high singlet oxygen formation and GPXH expression, which could either result from mutations in multiple loci or in a single gene encoding for a global regulator of cellular photoprotection mechanisms.

Dataset Information

SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii.

Publications

SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii.

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