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Arsenite Tolerance is Related to Proportional Thiolic Metabolite Synthesis in Rice (Oryza sativa L.)

  • Richa Dave
  • Pradyumna Kumar Singh
  • Preeti Tripathi
  • Manju Shri
  • Garima Dixit
  • Sanjay Dwivedi
  • Debasis Chakrabarty
  • Prabodh Kumar Trivedi
  • Yogesh Kumar Sharma
  • Om Prakash Dhankher
  • Francisco Javier Corpas
  • Juan B. Barroso
  • Rudra Deo TripathiEmail author
Article

Abstract

Thiol metabolism is the primary detoxification strategy by which rice plants tolerate arsenic (As) stress. In light of this, it is important to understand the importance of harmonised thiol metabolism with As accumulation and tolerance in rice plant. For this aim, tolerant (T) and sensitive (S) genotypes were screened from 303 rice (Oryza sativa) genotypes on exposure to 10 and 25 μM arsenite (AsIII) in hydroponic culture. On further As accumulation estimation, contrasting (13-fold difference) T (IC-340072) and S (IC-115730) genotypes were selected. This difference was further evaluated using biochemical and molecular approaches to understand involvement of thiolic metabolism vis-a-vis As accumulation in these two genotypes. Various phytochelatin (PC) species (PC2, PC3 and PC4) were detected in both the genotypes with a dominance of PC3. However, PC concentrations were greater in the S genotype, and it was noticed that the total PC (PC2 + PC+ PC4)–to–AsIII molar ratio (PC-SH:AsIII) was greater in T (2.35 and 1.36 in shoots and roots, respectively) than in the S genotype (0.90 and 0.15 in shoots and roots, respectively). Expression analysis of several metal(loid) stress–related genes showed significant upregulation of glutaredoxin, sulphate transporter, and ascorbate peroxidase in the S genotype. Furthermore, enzyme activity of phytochelatin synthase and cysteine synthase was greater on As accumulation in the S compared with the T genotype. It was concluded that the T genotype synthesizes adequate thiols to detoxify metalloid load, whereas the S genotype synthesizes greater but inadequate levels of thiols to tolerate an exceedingly greater load of metalloids, as evidenced by thiol-to-metalloid molar ratios, and therefore shows a phytotoxicity response.

Keywords

Arsenite Rice Flour Rice Genotype Sulphate Transporter NaAsO2 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors are thankful to the Director of the Council of Scientific and Industrial Research-National Botanical Research Institute (CSIR-NBRI) and Lucknow for use of the facilities as well as financial support from the network projects (CSIR), New Delhi, India. The authors are also thankful for financial support from DST Indo-Spanish Program, New Delhi, India, and ERDF-cofinanced grants from the Ministry of Science and Innovation Project No. ACI2009-0860, Spain.

Supplementary material

244_2012_9818_MOESM1_ESM.doc (510 kb)
Supplementary material 1 (DOC 510 kb)

References

  1. Abedin MJ, Cresser MS, Meharg AA, Feldmann J, Cotter-Howells J (2002) Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ Sci Technol 36:962–968CrossRefGoogle Scholar
  2. Brammer H, Ravenscroft P (2009) Arsenic in groundwater: A threat to sustainable agriculture in South and South-east Asia. Environ Int 35:647–654CrossRefGoogle Scholar
  3. Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D et al (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702CrossRefGoogle Scholar
  4. Dasgupta T, Hossain SA, Meharg AA, Price AH (2004) An arsenate tolerance gene on chromosome 6 of rice. New Phytol 163:45–49CrossRefGoogle Scholar
  5. Dave R, Tripathi RD, Dwivedi S, Tripathi P, Dixit G, Sharma YK et al (2012) Arsenate and arsenite exposure modulate antioxidants and amino acids in contrasting arsenic accumulating rice (Oryza sativa L.) genotypes. J Hazard Mater. doi: 10.1016/j.jhazmat.2012.06.049
  6. Duan GL, Hu Y, Liu WJ, Kneer R, Zhao FJ, Zhu YG (2011) Evidence for a role of phytochelatins in regulating arsenic accumulation in rice grain. Environ Exp Bot 71:416–421Google Scholar
  7. Dwivedi S, Tripathi RD, Srivastava S, Singh R, Kumar A, Tripathi P et al (2010) Arsenic affects mineral nutrients in grains of various Indian rice (Oryza sativa L.) genotypes grown on arsenic-contaminated soils of West Bengal. Protoplasma 245:113–124CrossRefGoogle Scholar
  8. Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104:627Google Scholar
  9. Heikens A (2006) Arsenic contamination of irrigation water, soil and crops in Bangladesh: risk implications for sustainable agriculture and food safety in Asia. FAO, BangkokGoogle Scholar
  10. Heiss S, Schäfer HJ, Kerwer AH, Rausch T (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of a putative low-affinity sulfate transporter and isoforms of ATP sulfurylase and APS reductase. Plant Mol Biol 39:847–857CrossRefGoogle Scholar
  11. Kumar S, Asif MH, Chakrabarty D, Tripathi RD, Trivedi PK (2011) Differential expression and alternative splicing of rice sulphate transporter family members regulate sulphur status during plant growth, development and stress conditions. Funct Integr Genomics 11:259–273CrossRefGoogle Scholar
  12. Liu WJ, Zhu YG, Smith FA, Smith SE (2004) Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture? New Phytol 162:481–488CrossRefGoogle Scholar
  13. Liu WJ, Wood BA, Raab A, McGrath SP, Zhao FJ, Feldmann J (2010) Complexation of arsenite with phytochelatins reduces arsenite efflux and translocation from roots to shoots in Arabidopsis. Plant Physiol 152:2211CrossRefGoogle Scholar
  14. Meharg AA, Hartley-Whitaker J (2002) Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytol 154:29–43CrossRefGoogle Scholar
  15. Meharg A, Jardine L (2003) Arsenite transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44CrossRefGoogle Scholar
  16. Meharg A, Macnair MR (1992) Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524CrossRefGoogle Scholar
  17. Minocha R, Thangavel P, Dhankher OP, Long S (2008) Separation and quantification of monothiols and phytochelatins from a wide variety of cell cultures and tissues of trees and other plants using high performance liquid chromatography. J Chromatogr A 1207:72–83CrossRefGoogle Scholar
  18. Mishra S, Srivastava S, Tripathi RD, Trivedi PK (2008) Thiol metabolism and antioxidant systems complement each other during arsenate detoxification in Ceratophyllum demersum L. Aquat Toxicol 86:205–215CrossRefGoogle Scholar
  19. Norton GJ, Lou-Hing DE, Meharg AA, Price AH (2008) Rice–arsenate interactions in hydroponics: whole genome transcriptional analysis. J Exp Bot 59:2267CrossRefGoogle Scholar
  20. Norton GJ, Duan G, Dasgupta T, Islam MR, Lei M, Zhu Y et al (2009a) Environmental and genetic control of arsenic accumulation and speciation in rice grain: comparing a range of common cultivars grown in contaminated sites across Bangladesh, China, and India. Environ Sci Technol 43:8381–8386CrossRefGoogle Scholar
  21. Norton GJ, Islam MR, Deacon CM, Zhao FJ, Stroud JL, McGrath SP et al (2009b) Identification of low inorganic and total grain arsenic rice cultivars from Bangladesh. Environ Sci Technol 43:6070–6075CrossRefGoogle Scholar
  22. Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic phytochelatin complexes in Holcus lanatus and Pteris cretica. Plant Physiol 134:1113CrossRefGoogle Scholar
  23. Raab A, Schat H, Meharg AA, Feldmann J (2005) Uptake, translocation and transformation of arsenate and arsenite in sunflower (Helianthus annuus): formation of arsenic–phytochelatin complexes during exposure to high arsenic concentrations. New Phytol 168:551–558CrossRefGoogle Scholar
  24. Rai A, Tripathi P, Dwivedi S, Dubey S, Shri M, Kumar S et al (2011) Arsenic tolerances in rice (Oryza sativa) have a predominant role in transcriptional regulation of a set of genes including sulphur assimilation pathway and antioxidant system. Chemosphere 82:986–995CrossRefGoogle Scholar
  25. Schat H, Kalff M (1992) Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed strain? Plant Physiol 99:1475CrossRefGoogle Scholar
  26. Seelig GF, Meister A (1984) γ-Glutamylcysteine synthetase. J Biol Chem 259:3534–3538Google Scholar
  27. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711CrossRefGoogle Scholar
  28. Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P et al (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110CrossRefGoogle Scholar
  29. Sneller FEC, Van Heerwaarden LM, Kraaijeveld-Smit FJL, Ten Bookum WM, Koevoets PLM et al (1999) Toxicity of arsenate in Silene vulgaris, accumulation and degradation of arsenate-induced phytochelatins. New Phytol 144:223–232CrossRefGoogle Scholar
  30. Srivastava S, D’Souza SF (2009) Increasing sulfur supply enhances tolerance to arsenic and its accumulation in Hydrilla verticillata (L. f.) Royle. Environ Sci Technol 43:6308–6313CrossRefGoogle Scholar
  31. Srivastava S, D’Souza SF (2010) Effect of variable sulfur supply on arsenic tolerance and antioxidant responses in Hydrilla verticillata (L.f) Royle. Ecotoxicol Environ Saf 73:1314–1322CrossRefGoogle Scholar
  32. Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (Lf) Royle. Environ Sci Technol 41:2930–2936CrossRefGoogle Scholar
  33. Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283:6095CrossRefGoogle Scholar
  34. Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK et al (2007) Arsenic hazards: Strategies for tolerance and remediation by plants. Trends Biotechnol 25:158–165CrossRefGoogle Scholar
  35. Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP et al (2012) Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicol Environ Saf 79:189–198CrossRefGoogle Scholar
  36. Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Ann Rev Plant Biol 61:535–559CrossRefGoogle Scholar
  37. Zheng MZ, Cai C, Hu Y, Sun GX, Williams PN, Cui HJ et al (2011) Spatial distribution of arsenic and temporal variation of its concentration in rice. New Phytol 189:200–209CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Richa Dave
    • 1
    • 6
  • Pradyumna Kumar Singh
    • 1
  • Preeti Tripathi
    • 1
  • Manju Shri
    • 1
  • Garima Dixit
    • 1
  • Sanjay Dwivedi
    • 1
  • Debasis Chakrabarty
    • 1
  • Prabodh Kumar Trivedi
    • 1
  • Yogesh Kumar Sharma
    • 2
  • Om Prakash Dhankher
    • 3
  • Francisco Javier Corpas
    • 4
  • Juan B. Barroso
    • 5
  • Rudra Deo Tripathi
    • 1
    Email author
  1. 1.Council of Scientific and Industrial Research-National Botanical Research Institute (CSIR-NBRI)LucknowIndia
  2. 2.Department of BotanyUniversity of LucknowLucknowIndia
  3. 3.Department of Plant, Soil and Insect SciencesUniversity of MassachusettsAmherstUSA
  4. 4.Departamento de BioquímicaBiología Celular y Molecular de Plantas, Estación Experimental del Zaidín (EEZ), CSICGranadaSpain
  5. 5.Unidad Asociada al CSIC (EEZ), Área de Bioquímica y Biología MolecularUniversidad de JaénJaénSpain
  6. 6.Amity Institute of Environmental Sciences, Amity UniversityNoidaIndia

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