Drought stress induces oxidative stress and the antioxidant defense system in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana

• Autorzy: Niu Y , Wang Y. , Li P. , Zhang F. , Liu H. , Zheng G.
• Języki publikacji: EN

Abstrakty

EN

Drought stress has a negative impact on plant cells and results in the generation of reactive oxygen species (ROS). To increase our understanding of the effects of drought stress on antioxidant processes, we investigated the response of the ascorbate-deficient Arabidopsis thaliana vtc1 mutant to drought stress. After drought stress, vtc1 mutants exhibited increases in several oxidative parameters, including H2O2 content and the production of thiobarbituric acid reactive substances. Decreases in chlorophyll content and chlorophyll fluorescence parameters were also observed. The vtc1 mutants had higher total glutathione than did wild-type (WT) plants after 48 h of drought stress. A reduced ratio of glutathione/total glutathione and an increased ratio of dehydroascorbate/total ascorbate were observed in the vtc1 mutants compared with the WT plants. In addition, the activities of enzymes that are responsible for ROS scavenging, including superoxide dismutase, catalase, and ascorbate peroxidase, were decreased in the vtc1 mutants compared with the WT plants. Similar reductions in activity in the vtc1 mutant were observed for the enzymes that are responsible for the regeneration of ascorbate and glutathione, including monodehydroascorbate reductase, dehydroascorbate reductase, and glutathione reductase. These results suggest that low intrinsic ascorbate and impaired ascorbate–glutathione cycling in the vtc1 mutant induced a decrease in the reduced form of ascorbate, which enhanced sensitivity to drought stress.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2013
• Tom: 35
• Numer: 04
• Opis fizyczny: p.1189-1200,fig.,ref.

Twórcy

autor

Niu Y

• Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China

autor

Wang Y.

• Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Key Laboratory of Crop Improvement and Germplasm Enhancement, College of Agronomy, Gansu Agricultural University, Lanzhou 730070, Gansu, China 123

autor

Li P.

• Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Key Laboratory of Crop Improvement and Germplasm Enhancement, College of Agronomy, Gansu Agricultural University, Lanzhou 730070, Gansu, China 123

autor

Zhang F.

• Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Key Laboratory of Crop Improvement and Germplasm Enhancement, College of Agronomy, Gansu Agricultural University, Lanzhou 730070, Gansu, China 123

autor

Liu H.

• Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China

autor

Zheng G.

• Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China

Bibliografia

• Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
• Alpert P (2006) Constrains of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584
• Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles: evidence for thermal dependence. Plant Physiol 98:501–508
• Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
• Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9
• Asada K (1999) The water–water cycle in chloroplast: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639
• Attolico AD, De Tullio MC (2006) Increased ascorbate content delays flowering in long-day grown Arabidopsis thaliana (L.) Heynh. Plant Physiol Biochem 44:462–466
• Barth C, Moeder W, Klessig DF, Conklin PL (2004) The timing of senescence and response to pathogens is altered in the ascorbatedeficient Arabidopsis mutant vitamin c-1. Plant Physiol 134:1784–1792
• Bilger W, Bjo¨rkman (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in Hedera canariensis. Photosynth Res 25:173–185
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
• Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341
• Brossa R, Lo’pez-Carbonell M, Jubany-Marı0 T, Alegre L (2011) Interplay between abscisic acid and jasmonic acid and its role in water-oxidative stress in wild-type, ABA-deficient, JA-deficient, and ascorbate-deficient Arabidopsis plants. J Plant Growth Regul 30:322–333
• Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384
• Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787
• Chen XY, Li W, Lu QT, Wen XG, Li HW, Kuang TY, Li ZS, Lu CM (2011) The xanthophyll cycle and antioxidative defense system are enhanced in the wheat hybrid subjected to high light stress. J Plant Physiol 167:1828–1836
• Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93:9970–9974
• Conklin PL, Norris SR, Wheeler GL, Williams EH,Smirnoff N, LastRL (1999) Genetic evidence for the role of GDPmannose in plant ascorbic acid (vitamin C) biosynthesis. Proc Natl Acad Sci USA 96:4198–4203
• Conklin PL, Saracco SA, Norris SR, Last RL (2000) Identification of ascorbic acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856
• Demmig-Adams B, Adams WW, Heber U, Neimanis S, Winter K, Kruger A et al (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92:293–301
• Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431
• Foyer CH, Rowell J, Walker D (1983) Measurement of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244
• Gao Q, Zhang LX (2008) Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient vtc1 mutants of Arabidopsis thaliana. J Plant Physiol 165:138–148
• Gechev TS, Breusegem FV, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101
• Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
• Giannopolitis CN, Ries SK (1977) Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318
• Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271
• Hossain MA, Asada K (1984a) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295
• Hossain MA, Asada K (1984b) Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme. Plant Cell Physiol 25:85–92
• Hossain MA, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395
• Huang C, He W, Guo J, Chang X, Su P, Zhang L (2005) Increased sensitivity to salt stress in an ascorbate-deficient Arabidopsis mutant. J Exp Bot 56:3041–3049
• Jakab G, Ton J, Flors V et al (2005) Enhancing arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274
• Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ et al (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5:23–32
• Kitajima M, Butler WL (1975) Excitation spectra for photosystem I and photosystem II in chloroplasts and the spectral characteristics of the distributions of quanta between the two photosystems. Biochim Biophys Acta 408:297–305
• Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM et al (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a humandehydroascorbate reductase gene. J PlantPhysiol 160:347–353
• Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc Natl Acad Sci USA 98:2262–2267
• Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
• Muller-Moule P, Conklin PL, Niyogi KK (2002) Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo. Plant Physiol 128:970–977
• Muller-Moule P, Golan T, Niyogi KK (2004) Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress. Plant Physiol 134:1163–1172
• Noctor G, Veljovic-Jovanovic S, Foyer CH (2000) Peroxide processing in photosynthesis: antioxidant coupling and redox signalling. Philos Trans R Soc Lon B Biol Sci 355:1465–1475
• Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267
• Owens CW, Belcher RV (1965) A colorimetric micro-method for the determination of glutathione. Biochem J 94:705–711
• Pastori GM, Kiddle G, Antoniw J, Bernard S, Veljovic-Jovanovic S, Verrier PJ et al (2003) Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 15:939–951
• Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6:379–389
• Pignocchi C, Kiddle G, Hernandez I, Foster SJ, Asensi A, Taybi T et al (2006) Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiol 141:423–435
• Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012
• Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127:426–435
• Veljovic-Jovanovic S, Noctor G, Foyer CH (2002) Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate. Plant Physiol Biochem 40:501–507
• Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472
• Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, van Montagu M, Inze´ D, van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16:4806–4816
• Yannarelli GG, Noriega GO, Batlle A, Tomaro ML (2006) Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224:1154–1162

Uwagi

rekord w opracowaniu