Plant and Soil

, Volume 336, Issue 1–2, pp 39–48 | Cite as

Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings

Regular Article
First Online:
Received:
Accepted:

Abstract

Ascorbic acid (AsA) is the most abundant antioxidant in plants and plays a role in responding to oxidative stress. It has been shown that AsA plays a role in protecting against abiotic stresses. Rice seedlings stressed with 5 μM CdCl2 showed typical Cd toxicity (chlorosis and increase in malondialdehyde content). Rice seedlings pretreated with heat shock at 45°C (HS) or H2O2 under non-HS conditions resulted in the increase in ascorbic acid (AsA) content and the AsA/dehydroascorbate ratio in rice leaves. Exogenous application of AsA or L-galactonone-1, 4-lactone (GalL), a biosynthetic precursor of AsA, under non-HS conditions, which resulted in an increase in AsA content in leaves, enhanced subsequent Cd tolerance of rice seedlings. Pretreatment with imidazole, an inhibitor of NADPH oxidase, under HS conditions significantly decreased H2O2 and AsA contents in leaves and reduced subsequent Cd tolerance of rice seedlings. We also observed that pretreatment with lycorine, which is known to inhibit the conversion of GalL to AsA, significantly inhibited HS-induced AsA accumulation in leaves and reduced HS-induced protection against subsequent Cd stress of rice stress. It appears that HS- or H2O2-induced protection against subsequent Cd stress of rice seedlings is mediated through AsA. The time-course analyses of HS in rice seedlings demonstrated that the accumulation of H2O2 preceded the increase in AsA. Based on the data obtained in this study, it could be concluded that the early accumulation of H2O2 during HS signals the increase in AsA content, which in turn protects rice seedlings from oxidative damage caused by Cd.

Keywords

Ascorbic acid Cadmium Heat shock Hydrogen peroxide Oryza sativa L. Oxidative stress 

Abbreviations

AsA

Ascorbic acid

APX

Ascorbate peroxidase

DHA

Dehydroascorbate

FW

Initial fresh weight

GalL

L-Galactone-1, 4-lactone

GR

Glutathione reductase

GSH

Reduced glutathione

HS

Heat shcok

IMD

Imidazole

MDA

Malondialdehyde

ROS

Reactive oxygen species

This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This work was supported by the National Science Council of the Republic of China (NSC 97-2313-B002-021).

References

  1. 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 72:248–254CrossRefPubMedGoogle Scholar
  2. Chao Y-Y, Hsu YT, Kao CH (2009) Involvement of glutathione in heat shock- and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings. Plant Soil 318:37–45CrossRefGoogle Scholar
  3. Cho U-H, Seo N-H (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120CrossRefGoogle Scholar
  4. De Gara L, Paciolla C, Tommasi F, Liso R, Arrigoni O (1994) In vivo inhibition of galactono-γ-lactone conversion to ascorbate by lycorine. J Plant Physiol 144:649–653Google Scholar
  5. Eshdat Y, Holland D, Faltin Z, Ben-Hayyim G (1997) Plant glutathione peroxidase. Physiol Plant 100:234–240CrossRefGoogle Scholar
  6. Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 66:482–487CrossRefPubMedGoogle Scholar
  7. Fu J, Zhou Q, Liu J, Liu W, Wang T, Zhang Q, Jiang G (2008) High levels of heavy metals in rice (Oryza sativa L.) from a typical E-waste recycling area in southeast China and its potential risk to human health. Chemosphere 71:1269–1275CrossRefPubMedGoogle Scholar
  8. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101CrossRefPubMedGoogle Scholar
  9. Gratăo PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  10. Greger M, Landberg T (2008) Role of rhizosphere mechanisms in Cd uptake by various wheat cultivars. Plant Soil 312:195–205CrossRefGoogle Scholar
  11. Guo Z, Tan H, Zhu Z, Lu S, Zhou B (2005) Effect of intermediates on ascorbic acid and oxalate biosynthesis of rice and in relation to its stress resistance. Plant Physiol Biochem 43:955–962CrossRefPubMedGoogle Scholar
  12. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefPubMedGoogle Scholar
  13. Halliwell B, Gutteridge MJC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, LondonGoogle Scholar
  14. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  15. Hsu YT, Kao CH (2005) Abscisic acid accumulation and cadmium tolerance in rice seedlings. Physiol Plant 124:71–80CrossRefGoogle Scholar
  16. Hsu YT, Kao CH (2007a) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298:231–241CrossRefGoogle Scholar
  17. Hsu YT, Kao CH (2007b) Heat shock-mediated H2O2 accumulation and protection against Cd toxicity in rice seedlings. Plant Soil 300:137–147CrossRefGoogle Scholar
  18. Jarvis SC, Jones LHP, Hopper MJ (1976) Cadmium uptake from solution by plants and its transport from roots to shoots. Plant Soil 44:179–191CrossRefGoogle Scholar
  19. Kuo MC, Kao CH (2004) Antioxidant enzyme activities are upregulated in response to cadmium in sensitive, but not in tolerant, rice (Oryza sativa L.) seedlings. Bot Bull Acad Sin 45:291–299Google Scholar
  20. Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160:347–353CrossRefPubMedGoogle Scholar
  21. Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and paraquat. Biochem J 210:899–903PubMedGoogle Scholar
  22. Maddison J, Lyons T, Plochl M, Barnes J (2002) Hydroponically cultivated radish fed L-galactono-1, 4-lactone exhibit increased tolerance to ozone. Planta 214:383–391CrossRefPubMedGoogle Scholar
  23. Mahalingam R, Jambunathan N, Gunjan S, Faustin E, Weng H, Ayoubi P (2006) Analysis of oxidative signaling induced by ozone in Arabidopsis thaliana. Plant Cell Environ 29:1357–1371CrossRefPubMedGoogle Scholar
  24. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  25. Neumann D, Lichtenberger O, Günther D, Tschiersch K, Nover L (1994) Heat-shock proteins induce heavy-metal tolerance in higher plants. Planta 194:360–367CrossRefGoogle Scholar
  26. Nieto-Sotolo J, Ho T-HD (1986) Effect of heat shock on the metabolism of glutathione in maize roots. Plant Phjysiol 82:1031–1035CrossRefGoogle Scholar
  27. Noctor G, Foyer CH (1998) Ascorbate and glutathione keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefPubMedGoogle Scholar
  28. Orzech KA, Burke JJ (1988) Heat shock and the protection against metal toxicity in wheat leaves. Plant Cell Environ 11:711–714CrossRefGoogle Scholar
  29. Pál M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246CrossRefGoogle Scholar
  30. Romero-Puertas MC, Corpas FJ, Rodriquez-Serrano M, Gomez M, del Rio LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by cadmium in pea plants. J Plant Physiol 164:1346–1357CrossRefPubMedGoogle Scholar
  31. Sato Y, Murakami T, Funatsuki H, Matsube S, Saruyama H, Tanida M (2001) Heat shock mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52:145–151CrossRefPubMedGoogle Scholar
  32. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365CrossRefPubMedGoogle Scholar
  33. Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211PubMedGoogle Scholar
  34. Smirnoff N, Wheeler GL (2000) Ascorbic acid in plants: biosynthesis and function. Curr Rev Biochem Mol Biol 35:291–314CrossRefGoogle Scholar
  35. Smith K (1985) Stimulation of glutathione synthesis in photorespiring plants by catalase inhibitors. Plant Physiol 79:1044–1047CrossRefPubMedGoogle Scholar
  36. Susuki N, Koizumi N, Sano H (2001) Screening of cadmium responsive genes in Arabidopsis thaliana. Plant Cell Environ 14:1177–1188CrossRefGoogle Scholar
  37. Tsai YC, Hong CY, Liu LF, Kao CH (2004) Relative importance of Na+ and Cl− in NaCl-induced antioxidant systems in roots of rice seedlings. Physiol Plant 122:86–94CrossRefGoogle Scholar
  38. Volkov RA, Panchuk II, Pm M, Schöffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746CrossRefPubMedGoogle Scholar
  39. Wu FB, Chen F, Wei K, Zhang GP (2004) Effect of cadmium on free amino acid, glutathione and ascorbic acid concentrations in two barley genotypes (Hordeum vulgare L.) differing in cadmium tolerance. Chemosphere 57:447–454CrossRefPubMedGoogle Scholar
  40. Yoshida S, Forno DA, Cock JH, Gomez KA (1972) Laboratory manual for physiological studies of rice, 2nd edn. The International Rice Research Institute, Los BañosGoogle Scholar
  41. Zhao ZQ, Cai YL, Zhu YG, Kneer R (2005) Cadmium-induced oxidative stress and protection by L-galactono-1, 4- lactone in winter wheat (Triticum aestivum L.). J Plant Nutr Soil Sci 168:759–763CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of AgronomyNational Taiwan UniversityTaipeiRepublic of China

Personalised recommendations