Skip to main content
Log in

Antimony tolerance and accumulation in a metallicolous and a non-metallicolous population of Salvia spinosa L.

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Antimony (Sb) is locally found at potentially toxic concentrations in mineralized soils, usually together with arsenic (As). However, local adaptation of plant populations to Sb toxicity has never been shown thus far. Here we compared Sb tolerance and accumulation between a non-metallicolous (NM) population of Salvia spinosa, and a con-specific metallicolous (M) population from a strongly Sb/As-enriched soil in Dashkasan, Iran.

Methods

Plants were exposed in hydroponics to a series of Sb[III] and Sb[V] concentrations. After 3 weeks the dry weights and Sb concentrations of roots and shoots were determined.

Results

Estimated from the effects on shoot dry weight, the M population was more tolerant than the NM one, particularly to Sb[V], but to a lower degree also to Sb[III]. In both populations Sb[III] was taken up and translocated at higher rates than Sb[V]. The Sb concentrations in roots and shoots were slightly, but significantly higher in the M than in the NM population.

Conclusions

Since Sb[V] and As[V] seem to follow very different detoxification pathways, it can be argued that the superior tolerance to Sb[V] in M represents a local adaptation to Sb[V] toxicity itself, rather than being a mere by-product of hypertolerance to its chemical analogue, As[V]. Since Sb[III] and As[III] or As[V] share common detoxification pathways, the apparent Sb[III] hypertolerance in the M population might represent a by-product of As hypertolerance.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anawar HM, Akai J, Mihaljevič M, Sikder AM, Ahmed G, Tareq S, Rahman MM (2011) Arsenic contamination in groundwater of bangladesh: perspectives on geochemical, microbial and anthropogenic. Water 3:1050–1076

    Article  CAS  Google Scholar 

  • Antonovics J, Bradshaw AD, Turner AG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–8

    Article  Google Scholar 

  • Baker AJM, Brooks RR, Pease AJ, Malaisse F (1983) Studies on copper and cobalt tolerancde in 3 closely related taxa within the genus Silene L. (Caryophyllaceae) from Zaire. Plant Soil 73:377–385

    Article  CAS  Google Scholar 

  • Bleeker PM, Hakvoort HWJ, Bliek M, Souer E, Schat H (2006) Enhanced arsenate reduction by a CDC25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J 45:917–929

    Article  CAS  PubMed  Google Scholar 

  • Casado M, Anawar HM, Garcia-Sanchez A, Santa Regina I (2007) Sb and arsenic uptake by plants in an abandoned mining area. Commun Soil Sci Plant Anal 38:1255–1275

    Article  CAS  Google Scholar 

  • Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku J, Zhao FJ, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12:1–17

    Article  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  CAS  PubMed  Google Scholar 

  • Corrales I, Barceló J, Bech J, Poschenrieder C (2014) Antimony accumulation and toxicity mechanisms in Trifolium species. J Geochem Explor 147:167–172

    Article  CAS  Google Scholar 

  • Crommentuijn T, Polder MD, van de Plassche EJ (1997) Maximum permissible concentrations and negligible concentrations of metals, taking background concentrations into account. National Institute of Public Health and the Environment, Bilthoven, the Netherlands. RIVM Report No. 601 501 001

  • Ernst WHO, Verkleij JAC, Schat H (1992) Metal tolerance in plants. Acta Bot Neerl 41:229–248

    Article  CAS  Google Scholar 

  • Filella M, Williams PA, Belzile N (2009) Antimony in the environment: knowns and unknowns. Montserrat Environ Chem 6:95–105

    Article  CAS  Google Scholar 

  • Gregory RPG, Bradshaw AD (1965) Heavy metal tolerance in populations of agrostis tenuis Sibth. and other grasses. New Phytol 64:131–143

    Article  CAS  Google Scholar 

  • Hogan GD, Rauser WE (1979) Tolerance and toxicity of cobalt, copper, nickel and zinc in clones of Agrostis gigantea. New Phytol 83(3):665–670

    Article  CAS  Google Scholar 

  • Jamali Hajiani N, Ghaderian SM, Karimi N, Schat H (2015) A comparative study of Sb accumulation in plants growing in two mining areas in Iran, Moghanlo, and Patyar. Environ Sci Pollut Res 22:16542–16553

    Article  CAS  Google Scholar 

  • Jamali Hajiani N, Ghaderian SM, Karimi N, Schat H (2017) A comparison of antimony accumulation and tolerance among Achillea wilhelmsii, Silene vulgaris and Thlaspi arvense. Plant Soil 412:267–281

    Article  CAS  Google Scholar 

  • Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer–Verlag, Berlin

    Book  Google Scholar 

  • Kabata-Pendias A, Pendias H (2010) Trace elements in soils and plants. CRC Press, Boca Raton

    Book  Google Scholar 

  • Karimi N, Ghaderian SM, Schat H (2013) Arsenic in soil and vegetation of a contaminated area. Int J Environ Sci Technol 10:743–752

    Article  CAS  Google Scholar 

  • Le Faucheur S, Schildknecht F, Behra R, Sigg L (2006) Thiols in Scenedesmus vacuolatus upon exposure to metals and metalloids. Aquat Toxicol 80:355–361

    Article  CAS  PubMed  Google Scholar 

  • Li XD, Thornton I (1993) Arsenic, antimony and bismuth in soil and pasture herbage in some old metalliferous mining areas in England. Environ Geochem Health 15:135–144

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Sperry JS, Shao M (2009) Hydraulic conductance and vulnerability to cavitation in corn (Zea mays L.) hybrids of differing drought resistance environmental and experimental. Environ Exp Bot 66:341–346

    Article  Google Scholar 

  • Macnair MR (1983) The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50:283–293

    Article  CAS  Google Scholar 

  • Macnair MR (1993) The genetics of metal tolerance in vascular plants. New Phytol 124:541–559

    Article  CAS  Google Scholar 

  • Macnair MR, Cumbes QJ, Meharg AA (1992) The genetics of arsenate tolerance in Yorkshire fog, Holcus lanatus L. Heredity 69:325–335

    Article  CAS  Google Scholar 

  • Meharg AA, Jardine L (2003) Arsenic transport into paddy rice (Oryza sativa) roots. New Phytol 157:39–44

    Article  CAS  Google Scholar 

  • Meharg AA, Macnair MR (1992) Suppression of the high-affinity phosphate uptake system – a mechanism of arsenate tolerance in Holcus lanatus L. J Exp Bot 43:519–524

    Article  CAS  Google Scholar 

  • Moritz R, Ghazban F, Singer BS (2006) Eocene gold ore formation at Muteh, Sanandaj-Sirjan extension and exhumation of metamorphic basement rocks within the Zagros orogen. Econ Geol 101:1497–1524

    Article  CAS  Google Scholar 

  • Perez-Sirvent C, Martinez-Sanchez MJ, Martinez-Lopez S, Bech J, Bolan N (2012) Distribution and bioaccumulation of arsenic and antimony in Dittrichia viscosa growing in mining-affected semiarid soils in Southeast Spain. J Geochem Explor 123:128–135

    Article  CAS  Google Scholar 

  • Raab A, Feldmann J, Meharg AA (2004) The nature of arsenic-phytochelatin complexes in Holcus lanatus and Pteris cretica. Am Soc Plant Biol 134:1113–1122

    CAS  Google Scholar 

  • Ren J, Pei-Chen Lin C, Pathak MC, Temple BR, Nile AH, Mousley CJ, Duncan MC, Eckert DM, Leiker TJ, Ivanova PT, Myers DS, Murphy RC, Brown HA, Verdaasdonk J, Bloom KS, Ortlund EA, Neiman AM, Bankaitis VA (2014) A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress-induced membrane biogenesis. Mol Biol Cell 25:712–727

    Article  PubMed  PubMed Central  Google Scholar 

  • Schat H, Ten Bookum WM (1992) Genetic control of copper tolerance in Silene vulgaris. Heredity 68:219–229

    Article  CAS  Google Scholar 

  • Schat H, Vooijs R (1997) Multiple tolerance and co-tolerance to heavy metals in Silene vulgaris: a co-segregation analysis. New Phytol 136(3):489–496

    Article  CAS  Google Scholar 

  • Schat H, Kuiper E, Ten Bookum WM, Vooijs R (1993) General model for the genetic control of copper tolerance in Silene vulgaris: evidence from crosses between plants from different tolerant populations. Heredity 70:142–147

    Article  CAS  Google Scholar 

  • Schat H, Vooijs R, Kuiper E (1996) Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50(5):1888–1895

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman and company, San Francisco

    Google Scholar 

  • Song W-Y, Park J, Mendoza-Cozatl DG, Suter-Grotemeyer M, Shim D, Hortensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroedewr JI, Lee Y, Martinoia E (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Nat Acad Sc USA 107:21187–21192

    Article  Google Scholar 

  • Tilstone G, Macnair MR (1997) Nickel tolerance and copper-nickel co-tolerance in Mimulus guttatus from copper mine and serpentine habitats. Plant Soil 191(2):173–180

    Article  CAS  Google Scholar 

  • Tisarum R, Lessl JT, Dong X, de Oliveira LM, Rathinasabapathi B, Ma LQ (2014) Antimony uptake, efflux and speciation in arsenic hyperaccumulator Pteris vittata. Environ Pollut 186:110–114

    Article  CAS  PubMed  Google Scholar 

  • Tschan M, Robinson BH, Schulin R (2009) Antimony in the soil–plant system – a review. Environ Chem 6:106–115

    Article  CAS  Google Scholar 

  • Van der Ent A, Baker AJM, van Balgooy MMJ, Tjoa A (2013) Ultramafic nickel laterites in Indonesia (Sulawesi, Halmahera): mining, nickel hyperaccumulators and opportunities for phytomining. J Geochem Explor 128:72–79

    Article  CAS  Google Scholar 

  • Vithanage M, Dabrowska BB, Mukherjee AB, Sandhi A, Bhattacharya P (2011) Arsenic uptake by plants and possible phytoremediation applications: a brief overview. Environ Chem Lett 10:217–224

    Article  CAS  Google Scholar 

  • Wysocki R, Clemens S, Augustyniak D, Golik P, Maciaszczyk E, Tamás MJ, Dziadkowiec D (2003) Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p. Biochem Biophys Res Commun 304(2):293–300

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the Graduate School of University of Isfahan for providing research facilities for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seyed Majid Ghaderian.

Additional information

Responsible Editor: Antony Van der Ent.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rajabpoor, S., Ghaderian, S.M. & Schat, H. Antimony tolerance and accumulation in a metallicolous and a non-metallicolous population of Salvia spinosa L.. Plant Soil 437, 11–20 (2019). https://doi.org/10.1007/s11104-019-03961-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-03961-x

Keywords

Navigation