Sugar-induced tolerance to the herbicide atrazine in Arabidopsis seedlings involves activation of oxidative and xenobiotic stress responses

Plant Cell Reports

Volumn 25, Issue 5, 2006, Pages 489-498

  Sulmon, Cécile ^a   Gouesbet, Gwenola ^a   El Amrani, Abdelhak ^a   Couée, Ivan ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Atrazine; Oxidative stress; Photosynthesis; Singlet oxygen; Sucrose

Indexed keywords

PHOTOSYNTHESIS; SUGAR (SUCROSE);

ACTIVATION; ARABIDOPSIS SEEDLINGS; ATRAZINE; CHLOROPLAST BIOGENESIS; CYTOSOLIC GLUTATHIONE-S-TRANSFERASE; GENE EXPRESSION; OXIDATIVE STRESS; SINGLET OXYGEN; WHOLE-CELL GLUCOSE-6-PHOSPHATE DEHYDROGENASE ACTIVITY; XENOBIOTIC STRESS RESPONSES;

HERBICIDES;

ARABIDOPSIS PROTEIN; ATRAZINE; GLUCOSE; GLUTATHIONE TRANSFERASE; GSTF8 PROTEIN, ARABIDOPSIS; HERBICIDE; SUCROSE; SUPEROXIDE DISMUTASE; XENOBIOTIC AGENT;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; DRUG EFFECT; ENZYME ACTIVATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SEEDLING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATRAZINE; CHLOROPLASTS; ENZYME ACTIVATION; GLUCOSE; GLUTATHIONE TRANSFERASE; HERBICIDES; OXIDATIVE STRESS; SEEDLING; SUCROSE; SUPEROXIDE DISMUTASE; XENOBIOTICS;

HERBICIDES; PHOTOSYNTHESIS; SUCROSE;

ARABIDOPSIS;

EID: 33646013917     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-005-0062-9     Document Type: Article

References (55)

1. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53:1331-1341
2. Ashton AR, Ziegler P (1987) Lack of effect of the photosystem II-based herbicides diuron and atrazine on growth of photoheterotrophic Chenopodium rubrum cells at concentrations inhibiting photoautotrophic growth of these cells. Plant Science 51:269-275
3. Barra L, Pica N, Gouffi K, Walker GC, Blanco C, Trautwetter A (2003) Glucose-6-phosphate dehydrogenase is required for sucrose and trehalose to be efficient osmoprotectants in Sinorhizobium meliloti. FEMS Microbiology Letters 229:183-188
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254
5. Brouquisse R, James E, Raymond P, Pradet A (1991) Study of glucose starvation in excised maize root tips. Plant Physiology 96:619-626
6. 2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant Journal 10:955-966
7. Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant Journal 19:667-677
8. Cohen G, Hochstein P (1963) Glutathione peroxidase: the primary agent for the elimination of hydrogen peroxide in erythrocytes. Biochemistry 2:1420-1428
9. Coleman JOD, Frova C, Schroeder P, Tissut M (2001) Exploiting plant metabolism for the phytoremediation of persistent herbicides. Environmental Science and Pollution Research 9:18-28
10. Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701-703
11. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen network of Arabidopsis. The Plant Cell 17:268-281
12. De Prado R, Lopez-Martinez N, Gonzalez-Gutierrez J (2000) Identification of two mechanisms of atrazine resistance in Setaria faberi and Setaria viridis biotypes. Pesticide Biochemistry and Physiology 67:114-124
13. Debnam PM, Fernie AR, Laisse A, Golding A, Bowsher CG, Grimshaw C, Knight JS, Emes MJ (2004) Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. Plant Journal 38:49-59
14. DeRidder BP, Dixon DP, Beussman DJ, Edwards R, Goldsbrough PB (2002) Induction of Glutathione S-Transferases in Arabidopsis by Herbicide Safeners. Plant Physiology 130:1497-1505
15. Desikan R, A.-H.-Mackerness S, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis Transcriptome by Oxidative Stress. Plant Physiology 127:159-172
16. Didierjean L, Gondet L, Perkins R, Lau SMC, Schaller H, O'Keefe DP, Werck-Reichhart D (2002) Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiology 130:1-11
17. Fracheboud Y, Haldimann P, Leipner J, Stamp P (1999) Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany 50:1533-1540
18. Frear DS, Swanson HR (1970) The biosynthesis of S-(4-ethylamino-6-isopropylamino-2-s-triazino)glutathione: partial purification and properties of a glutathione-S-transferase from corn. Phytochemistry 9:2123-2132
19. Freire MA, Tourneur C, Granier F, Camonis J, El Amrani A, Browning KS, Robaglia C (2000) Plant lipoxygenase 2 is a translation initiation factor-4E-binding protein. Plant Molecular Biology 44:129-140
20. Gaetani GF, Galiano S, Canepa L, Ferraris AM, Kirkman HN (1989) Catalase and glutathione peroxidase are equally active in detoxification of hydrogen peroxide in human erythrocytes. Blood 73:334-339
21. Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiology 103:1067-1073
22. Hauschild R, von Schaewen A (2003) Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. Plant Physiology 133:47-62
23. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annual Reviews of Plant Physiology and Molecular Biology 47:509-540
24. Kovtun Y, Daie J (1995) End-product control of carbon metabolism in culture-grown sugar beet plants. Plant Physiology 108:1647-1656
25. Li H, Sherman LA (2000) A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology 182:4268-4277
26. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11:591-592
27. Lopez-Martinez N, Marshall G, De Prado R (1997) Resistance of barnyardgrass (Echinochloa crus-galli) to atrazine and quinchlorac. Pesticide Science 51:171-175
28. Lupinkova L, Komenda J (2004) Oxidative modifications of the Photosystem II D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochemistry and Photobiology 79:152-162
29. Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilisation and photosynthetic gene expression are regulated by carbon: nitrogen availability. Plant Physiology 128:472-481
30. May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. Journal of Experimental Botany 49:649-667
31. Mould R, Robinson C (1991) A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. Journal of Biological Chemistry 266:12189-12193
32. Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321-11330
33. Nogushi T (2002) Dual role of triplet localization on the accessory chlorophyll in the photosystem II reaction center: photoprotection and photodamage of the D1 protein. Plant Cell Physiology 43:1112-1116
34. op den Camp RGL, Przybila D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320-2332
35. Pego JV, Kortstee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. Journal of Experimental Botany 51:407-416
36. Price J, Laxmi A, Martin SKS, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128-2150
37. Rinalducci S, Pedersen JZ, Zolla L (2004) Formation of radicals from singlet oxygen produced during photoinhibition of isolated light-harvesting proteins of photosystem II. Biochimica and Biophysica Acta 1608:63-73
38. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell supplement 2002:S185-S205
39. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiology 130:1109-1120
40. Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends in Biochemical Science 26:648-653
41. Ryter SW, Tyrrell RM (1998) Singlet molecular oxygen: a possible effector of eukaryotic gene expression. Free Radical Biology and Medecine 24:1520-1534
42. Ryu JY, Song JY, Lee JM, Jeong SW, Chow WS, Choi SB, Pogson BJ, Park YI (2004) Glucose-induced expression of carotenoid biosynthesis genes in the dark is mediated by cytosolic pH in the cyanobacterium Synechocystis sp. PCC 6803. Journal of Biological Chemistry 279:25320-25325
43. Salerno GL, Curatti L (2003) Origin of sucrose metabolism in higher plants: when, how and why? Trends in Plant Science 8:63-69
44. Salvemini F, Franzé A, Iervolino A, Filosa S, Salzano S, Ursini MV (1999) Enhanced glutathione levels and oxidoresistance mediated by increased glucose-6-phosphate dehydrogenase expression. Journal of Biological Chemistry 274:2750-2757
45. Sulmon C, Gouesbet G, Couée I, El Amrani A (2004) Sugar-induced tolerance to atrazine in Arabidopsis seedlings: interacting effects of atrazine and soluble sugars on psbA mRNA and D1 protein levels. Plant Science 167:913-923
46. Tasli S (1995) Devenir de l'atrazine en culture de maïs. PhD thesis, Université Joseph Fourier, Grenoble, France
47. Taylor M, Feyereisen R (1996) Molecular biology and evolution of resistance of toxicants. Molecular Biology and Evolution 13:719-734
48. Thibaud MC, Gineste S, Nussaume L, Robaglia C (2004) Sucrose increases pathogenesis-related PR-2 expression in Arabidopsis thaliana through an SA-dependent but NPR1-independent signaling pathway. Plant Physiology and Biochemistry 42:81-88
49. Van Camp W, Capiau K, Van Montagu M, Inzé D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiology 112:1703-1714
50. Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione-S-transferase gene family. Plant Molecular Biology 49:515-532
51. Wagner D, Przybyla D, Op den Camp R, Kim C, Langraf F, Lee KP, Wursch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183-1185
52. Wakao S, Benning C (2004) Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis. The Plant Journal 41:243-256
53. Xu J, Maki D, Stapleton SR (2003) Mediation of cadmium-induced oxidative damage and glucose-6-phosphate dehydrogenase expression through glutathione depletion. Journal of Biochemical and Molecular Toxicology 17:67-75
54. Zheleva D, Tsonev T, Sergiev I, Karanov E (1994) Protective effect of exogenous polyamines against atrazine in pea plants. Journal of Plant Growth Regulation 13:203-211
55. Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proceedings of National Academy of Science USA 95:10294-10299