The Glutathione Peroxidase Homologous Gene from Chlamydomonas Reinhardtii is Transcriptionally Up-regulated by Singlet Oxygen

Overview

Journal Plant Mol Biol

Date 2001 Aug 4

PMID 11485197

Citations 35

Authors

U Leisinger

K Rufenacht

B Fischer

M Pesaro

A Spengler

A J Zehnder

R I Eggen

Affiliations

Soon will be listed here.

Abstract

The glutathione peroxidase homologous gene (Gpxh gene) in Chlamydomonas reinhardtii is up-regulated under oxidative stress conditions. The Gpxh gene showed a remarkably strong and fast induction by the singlet oxygen-generating photosensitizers neutral red, methylene blue and rose Bengal. The Gpxh mRNA levels strongly increased, albeit much more slowly, upon exposure to the organic hydroperoxides tert-butyl hydroperoxide (t-BOOH) and cumene hydroperoxide. In contrast, the Gpxh mRNA levels were only weakly induced by exposure to the superoxide-generating compound paraquat and by hydrogen peroxide. A comparison of the Gpxh mRNA levels with those of the heat shock protein HSP70A and the iron superoxide dismutase gene showed qualitative and quantitative differences for the three genes under oxidative stress conditions tested. The Gpxh gene is specifically induced by singlet-oxygen photosensitizers and the relative induction by other compounds is much weaker for Gpxh than for the other genes investigated. Using Gpxh promoter fusions with the arylsulfatase reporter gene, we have shown that the Gpxh was transcriptionally up-regulated by singlet-oxygen photosensitizers. It is also shown that the Gpxh promoter contains a region between 104 and 179 bp upstream of the transcription start that is responsible for the mRNA up-regulation upon exposure to 1O2 but not t-BOOH. Within this region a regulatory sequence homologous to the mammalian cAMP response element (CRE) and activator protein 1 (AP-1) binding site was identified within a 16 bp palindrome.

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References

Ryter S, Tyrrell R . Singlet molecular oxygen ((1)O2): a possible effector of eukaryotic gene expression. Free Radic Biol Med. 1998; 24(9):1520-34. DOI: 10.1016/s0891-5849(97)00461-9. View

Penson S, Schuurink R, FATH A, Gubler F, Jacobsen J, Jones R . cGMP Is Required for Gibberellic Acid-Induced Gene Expression in Barley Aleurone. Plant Cell. 1996; 8(12):2325-2333. PMC: 161355. DOI: 10.1105/tpc.8.12.2325. View

Briviba K, Klotz L, Sies H . Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol Chem. 1998; 378(11):1259-65. View

Aveline B, Sattler R, Redmond R . Environmental effects on cellular photosensitization: correlation of phototoxicity mechanism with transient absorption spectroscopy measurements. Photochem Photobiol. 1998; 68(1):51-62. View

Kochevar I, Bouvier J, Lynch M, Lin C . Influence of dye and protein location on photosensitization of the plasma membrane. Biochim Biophys Acta. 1994; 1196(2):172-80. DOI: 10.1016/0005-2736(94)00236-3. View

Wang W, Wang W, Boynton J, Gillham N . Genetic control of chlorophyll biosynthesis in Chlamydomonas. Analysis of mutants at two loci mediating the conversion of protoporphyrin-IX to magnesium protoporphyrin. J Cell Biol. 1974; 63(3):806-23. PMC: 2109367. DOI: 10.1083/jcb.63.3.806. View

Jasper F, Quednau B, Kortenjann M, Johanningmeier U . Control of cab gene expression in synchronized Chlamydomonas reinhardtii cells. J Photochem Photobiol B. 1991; 11(2):139-50. DOI: 10.1016/1011-1344(91)80256-h. View

Auchincloss A, Loroch A, Rochaix J . The argininosuccinate lyase gene of Chlamydomonas reinhardtii: cloning of the cDNA and its characterization as a selectable shuttle marker. Mol Gen Genet. 1999; 261(1):21-30. DOI: 10.1007/s004380050937. View

Ehrenberg B, Anderson J, Foote C . Kinetics and yield of singlet oxygen photosensitized by hypericin in organic and biological media. Photochem Photobiol. 1998; 68(2):135-40. View

10.

Telfer A, Bishop S, Phillips D, Barber J . 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; 269(18):13244-53. View

11.

Mayfield S . Over-expression of the oxygen-evolving enhancer 1 protein and its consequences on photosystem II accumulation. Planta. 2013; 185(1):105-10. DOI: 10.1007/BF00194521. View

12.

Sies H, Menck C . Singlet oxygen induced DNA damage. Mutat Res. 1992; 275(3-6):367-75. DOI: 10.1016/0921-8734(92)90039-r. View

13.

Kropat J, von Gromoff E, Muller F, Beck C . Heat shock and light activation of a Chlamydomonas HSP70 gene are mediated by independent regulatory pathways. Mol Gen Genet. 1995; 248(6):727-34. DOI: 10.1007/BF02191713. View

14.

Roudyk S, Moxhet A, Matagne R, Aghion J . Evidence of singlet oxygen evolution by whole living cells of Chlamydomonas reinhardtii. Photosynth Res. 2013; 47(1):99-102. DOI: 10.1007/BF00017757. View

15.

Khan A, KASHA M . Singlet molecular oxygen in the Haber-Weiss reaction. Proc Natl Acad Sci U S A. 1994; 91(26):12365-7. PMC: 45438. DOI: 10.1073/pnas.91.26.12365. View

16.

Ohresser M, Matagne R, Loppes R . Expression of the arylsulphatase reporter gene under the control of the nit1 promoter in Chlamydomonas reinhardtii. Curr Genet. 1997; 31(3):264-71. DOI: 10.1007/s002940050204. View

17.

Bienz M, Pelham H . Heat shock regulatory elements function as an inducible enhancer in the Xenopus hsp70 gene and when linked to a heterologous promoter. Cell. 1986; 45(5):753-60. DOI: 10.1016/0092-8674(86)90789-0. View

18.

Sugimoto M, Furui S, Suzuki Y . Molecular cloning and characterization of a cDNA encoding putative phospholipid hydroperoxide glutathione peroxidase from spinach. Biosci Biotechnol Biochem. 1997; 61(8):1379-81. DOI: 10.1271/bbb.61.1379. View

19.

Goldschmidt-Clermont M, Rahire M . Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. J Mol Biol. 1986; 191(3):421-32. DOI: 10.1016/0022-2836(86)90137-3. View

20.

Lambert C, Kochevar I . Electron transfer quenching of the rose bengal triplet state. Photochem Photobiol. 1997; 66(1):15-25. DOI: 10.1111/j.1751-1097.1997.tb03133.x. View