Skip to main content
Log in

Evidence of vacuolar compartmentalization of arsenic in the hyperaccumulator Pteris vittata

  • Articles / Plant Physiology
  • Published:
Chinese Science Bulletin

Abstract

Pteris vittata can hyperaccumulate arsenic (As) to >1% of its dry weight without showing any signs of toxicity, indicating the existence of effective plant-internal detoxification mechanisms. Although vacuolar compartmentalization is known to play an important role in heavy metal detoxification and tolerance, direct evidence of arsenic compartmentalization in this hyperaccumulator was lacking. Here we report the subcellular localization of As in the callus of P. vittata. The callus induced from gametophytes of P. vittata exposed to 0.2 mmol/L arsenate for 20 days were examined by directly isolating cell walls, protoplasts and vacuoles, and determining arsenic concentrations. Of the total As in the callus, about 94% was in the protoplast, and of that, 91% was present in the vacuoles, indicating that vacuoles are a major storage site for As in P. vittata. In addition, the changes in the chemical components of vacuoles were analyzed by Fourier transform infrared spectroscopy (FTIR).

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Meharg A A, Macnair M R. The mechanisms of arsenate tolerance in Deschampsia cespitosa (L.) Beauv and Agrostis capillaris L. New Phytol, 1991, 119: 291–297

    Article  Google Scholar 

  2. Meharg A A, Macnair M R. Suppression of the high-affinity phosphate uptake system: A mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot, 1992, 43: 519–524

    Article  Google Scholar 

  3. Bleeker P M, Schat H, Vooijs R, et al. Mechanisms of arsenate tolerance in Cytisus striatus. New Phytol, 2003, 157: 33–38

    Article  Google Scholar 

  4. Ma L Q, Komar K M, Tu C, et al. A fern that hyperaccumulates arsenic. Nature, 2001, 409: 579

    Article  Google Scholar 

  5. Francesconi K, Visoottiviseth P, Sridokchan W, et al. Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci Total Environ, 2002, 284: 27–35

    Article  Google Scholar 

  6. Visoottiviseth P, Francesconi K, Sridokchan W. The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut, 2002, 118: 453–461

    Article  Google Scholar 

  7. Zhao F J, Dunham S J, McGrath S P. Arsenic hyperaccumulation by different fern species. New Phytol, 2002, 156: 27–31

    Article  Google Scholar 

  8. Zhao F J, Ma J F, Meharg A A, et al. Arsenic uptake and metabolism in plants. New Phytol, 2009, 181: 777–794

    Article  Google Scholar 

  9. Wang J, Zhao F J, Meharg A A, et al. Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol, 2002, 130:1552–1561

    Article  Google Scholar 

  10. Tu S, Ma L Q. Comparison of arsenic and phosphate uptake and distribution in arsenic hyperaccumulating and nonhyperaccumulating fern. J Plant Nutr, 2004, 27: 1227–1242

    Article  Google Scholar 

  11. Lombi E, Zhao F J, Fuhrman M, et al. Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol, 2002, 156: 195–203

    Article  Google Scholar 

  12. Zhang W H, Cai Y, Tu C, et al. Arsenic speciation and distribution in an arsenic hyperaccumulating plant. Sci Tot Environ, 2002, 300: 167–177

    Article  Google Scholar 

  13. Shoji R, Yajima R, Yano Y. Arsenic speciation for the phytoremediation by the Chinese brake fern, Pteris vittata. J Environ Sci (in Chinese), 2008, 20: 1463–1468

    Article  Google Scholar 

  14. Ellis D R, Gumaelius L, Indriolo E, et al. A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol, 2006, 141: 1544–1554

    Article  Google Scholar 

  15. Pickering I J, Gumaelius L, Harris H H, et al. Localizing the biochemical transformations of arsenate in a hyperaccumulating fern. Environ Sci Technol, 2006, 40: 5010–5014

    Article  Google Scholar 

  16. Zhao F J, Wang J R, Barker J H A, et al. The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol, 2003, 159: 403–410

    Article  Google Scholar 

  17. Zhang W H, Cai Y, Downum K R, et al. Arsenic complexes in the arsenic hyperaccumulator Pteris vittata (Chinese brake fern). J Chromatogr A, 2004, 1043: 249–254

    Article  Google Scholar 

  18. Bluemlein K, Raab A, Meharg A A, et al. Can we trust mass spectrometry for determination of arsenic peptides in plants: comparison of LC-ICP-MS and LC-ES-MS/ICP-MS with XANES/EXAFS in analysis of Thunbergia alata. Anal Bioanal Chem, 2008, 390: 1739–1751

    Article  Google Scholar 

  19. Meharg A A, Hartley-Whitaker J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol, 2002, 154: 29–43

    Article  Google Scholar 

  20. Bleeker P M, Hakvoort H W, Bliek M, et al. Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J, 2006 45: 917–929

    Article  Google Scholar 

  21. Yang X, Chen H, Xu W, et al. Hyperaccumulation of arsenic by callus, sporophytes and gametophytes of Pteris vittata cultured in vitro. Plant Cell Rep, 2007, 26: 1889–1897

    Article  Google Scholar 

  22. DiTomaso J M, Hart J J, Kochian L V. Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol, 1992, 98: 611–620

    Article  Google Scholar 

  23. Shen R F, Ma J F, Kyo M, et al. Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta, 2002, 215: 394–398

    Article  Google Scholar 

  24. Ma J F, Ueno D, Zhao F J, et al. Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta, 2005, 220: 731–736

    Article  Google Scholar 

  25. Storrie B, Madden E A. Isolation of subcellular organelles. Method Enzymol, 1990, 182: 203–225

    Article  Google Scholar 

  26. Leigh R A, Walker R R. ATPase and acid phosphatase activities associated with vacuoles isolated from storage roots of red beet (Beta vulgaris L.). Planta, 1980, 150: 222–229

    Article  Google Scholar 

  27. Jones J J, Case V V. Sampling, Handling, and Analyzing Plant Tissue Samples. In: Westerman R L, eds. Soil Testing and Plant Analysis. Second Ed. Soil Science Society of America, Madison WI, 1990. 389–427

    Google Scholar 

  28. Wang Q, Kong L, Hao H, et al. Effects of brefeldin A on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion. Plant Physiol, 2005, 139: 1692–1703

    Article  Google Scholar 

  29. Tu C, Ma L Q. Effects of arsenic concentrations and forms on arsenic uptake by the hyperaccumulator ladder brake. J Environ Qual, 2002, 31: 641–647

    Article  Google Scholar 

  30. Cosgrove D J. Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol, 1997, 13: 171–201

    Article  Google Scholar 

  31. Buchanan B B, Gruissem W, Jones R L. Biochemistry and Molecular Biology of Plants. Am Soc Plant Physiol, Rockville MD, 2000

  32. Bringezu K, Lichtenberger O, Leopold I, et al. Heavy metal tolerance of Silene vulgaris. J Plant Physiol, 1999, 154: 536–546

    Google Scholar 

  33. Boominathan R, Doran P M. Organic acid complexation, heavy metal distribution and the effect of ATPase inhibition in hairy roots of hyperaccumulator plant species. J Biotechno1, 2003, 101: 131–146

    Article  Google Scholar 

  34. Vogeli-Lange R, Wagner G J. Subcellular localization of cadmium and cadmium binding peptides in tobacco leaves. Plant Physiol, 1990, 92: 1086–1093

    Article  Google Scholar 

  35. Chen T B, Yan X L, Liao X Y, et al. Subcellular and compartmentalization of arsenic in Pteris vittata L. China. Chinese Sci Bull, 2005, 50: 2843–2849

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mi Ma.

Additional information

Supported by the National High Technology Research and Development Program of China (Grant No. 2007AA021404) and National Natural Science Foundation of China (Grant No. 30670171)

About this article

Cite this article

Yang, X., Chen, H., Dai, X. et al. Evidence of vacuolar compartmentalization of arsenic in the hyperaccumulator Pteris vittata . Chin. Sci. Bull. 54, 4229–4233 (2009). https://doi.org/10.1007/s11434-009-0675-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-009-0675-4

Keywords

Navigation