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Strategies of adaptation to heavy metal pollution in Deschampsia caespitosa and Lychnis flos-cuculi: Analysis based on dose-response relationship

Abstract

The response to copper pollution was studied in the vegetative progeny of tufted hair grass (Deschampsia caespitosa (L.) Beauv.) and ragged robin (Lychnis flos-cuculi L.) plants growing together in chronically polluted areas around the Middle Ural Copper Smelter or in background areas. The root elongation test was used, with copper sulfate (0.006–0.51 mg Cu/L) being added directly to the nutrient medium. Using multimodel inference, dose-response curves were plotted for each of 85 maternal plants, and their parameters (effective Cu concentrations and curve slope in the linear segment) were evaluated. The pattern of transformation in dose dependence of root increment upon transition from background to impact populations proved to be basically different in the two species. The curves for L. flos-cuculi showed a parallel shift, with their shape remaining generally unchanged. In D. caespitosa, this transition was accompanied by a decrease in sensitivity to Cu, but tolerance to this metal was found to increase only at the highest concentration range. These results provide evidence for different strategies of adaptation to heavy metal pollution, which are discussed by comparing the physiological and ecological properties of the two species.

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References

  1. Biere, A., Genotypic and plastic variation in plant size: Effects on fecundity and allocation patterns in Lychnis floscuculi along a gradient of natural soil fertility, J. Ecol., 1995, vol. 83, no. 4, pp. 629–642.

    Article  Google Scholar 

  2. Bradshaw, A.D., Evolutionary significance of phenotypic plasticity in plants, Adv. Genet., 1965, vol. 13, pp. 115–155.

    Article  Google Scholar 

  3. Buckland, S.T., Burnham, K.P., and Augustin, N.H., Model selection: An integral part of inference, Biometrics, 1997, vol. 53, no. 2, pp. 603–618.

    Article  Google Scholar 

  4. Burnham, K.P. and Anderson, D.R., Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, New York: Springer, 2002.

    Google Scholar 

  5. Canty, A. and Ripley, B., boot: Bootstrap R (S-Plus) functions. R package version 1.3–4. 2012. http://cran.r-project.org/web/packages/boot/index.html

    Google Scholar 

  6. Chaloupecká E. and Lepš, J. Equivalence of competitor effects and tradeoff between vegetative multiplication and generative reproduction: Case study with Lychnis floscuculi and Myosotis nemorosa, Flora, 2004, vol. 199, no. 2, pp. 157–167.

    Article  Google Scholar 

  7. Cox, R.M. and Hutchinson, T.C., Multiple metal tolerances in the grass Deschampsia caespitosa (L.) Beauv. from the Sudbury smelting area, New Phytol., 1980, vol. 84, no. 4, pp. 631–647.

    Article  CAS  Google Scholar 

  8. Davy, A.J., Biological flora of the British Isles: Deschampsia caespitosa (L.) Beauv., J. Ecol., 1980, vol. 62, no. 149, pp. 367–378.

    Google Scholar 

  9. De Vos, C.H.R., Schat, H., De Waal, M.A.M., Vooijs, R., and Ernst, W.H.O., Increased resistance to copper-induced damage of the root cell plasmalemma in copper-tolerant Silene cucubalus, Physiol. Plant., 1991, vol. 82, no. 4, pp. 523–528.

    Article  Google Scholar 

  10. Ducousso, A., Petit, D., Valero, M., and Vernet, P., Genetic variation between and within populations of a perennial grass, Arrhenatherum elatius, Heredity, 1990, vol. 65, pp. 179–188.

    Article  Google Scholar 

  11. Dulya, O.V. and Mikryukov, V.S., Effect of methodological factors on the results of ecological experiments: Meta-analysis, in Ekologiya: Skvoz’ vremya i rasstoyanie (Ecology: Through Time and Distance), Yekaterinburg, 2011, pp. 60–68.

    Google Scholar 

  12. Ernst, W.H.O., Evolution of metal tolerance in higher plants, For. Snow Landsc. Res., 2006, vol. 80, no. 3, pp. 251–274.

    Google Scholar 

  13. Hall, J.L., Cellular mechanisms for heavy metal detoxification and tolerance, J. Exp. Bot., 2002, vol. 53, no. 366, pp. 1–11.

    PubMed  Article  CAS  Google Scholar 

  14. Kopittke, P.M., Blamey, F.P., Asher, C.J., and Menzies, N.W., Trace metal phytotoxicity in solution culture: A review, J. Exp. Bot., 2010, vol. 61, no. 4, pp. 945–954.

    PubMed  Article  CAS  Google Scholar 

  15. Macnair, M.R., Smith, S.E., and Cumbes, Q.J., Heritability and distribution of variation in degree of copper tolerance in Mimulus guttatus at Copperopolis, California, Heredity, 1993, vol. 71, no. 5, pp. 445–455.

    Article  CAS  Google Scholar 

  16. Meerts, P. and Van Isacker, N., Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe, Plant Ecol., 1997, vol. 133, no. 1, pp. 221–231.

    Article  Google Scholar 

  17. Mengoni, A., Barabesi, C., Gonnelli, C., et al., Genetic diversity of heavy metal-tolerant populations in Silene paradoxa L. (Caryophyllaceae): A chloroplast microsatellite analysis, Mol. Ecol., 2001, vol. 10, no. 8, pp. 1909–1916.

    PubMed  Article  CAS  Google Scholar 

  18. Mengoni, A., Gonnelli, C., Hakvoort, H.W.J., et al., Evolution of copper tolerance and increased expression of a 2btype metallothionein gene in Silene paradoxa L. populations, Plant Soil, 2003, vol. 257, no. 2, pp. 451–457.

    Article  CAS  Google Scholar 

  19. Nesterkov, A.V. and Vorobeichik, E.L., Changes in the structure of chortobiont invertebrate community exposed to emissions from a copper smelter, Russ. J. Ecol., 2009, vol. 40, no. 4, pp. 286–296.

    Article  CAS  Google Scholar 

  20. Paschke, M.W. and Redente, E.F., Copper toxicity thresholds for important restoration grass species of the western United States, Env. Toxicol. Chem., 2002, vol. 21, no. 12, pp. 2692–2697.

    Article  CAS  Google Scholar 

  21. Ritz, C., Toward a unified approach to dose-response modeling in ecotoxicology, Env. Toxicol. Chem., 2010, vol. 29, no. 1, pp. 220–229.

    Article  CAS  Google Scholar 

  22. Ritz, C. and Streibig, J.C., Bioassay analysis using R, J. Stat. Softw., 2005, vol. 12, no. 5, pp. 1–22.

    Google Scholar 

  23. Rousseeuw, P.J. and Croux, C., Alternatives to the median absolute deviation, J. Am. Stat. Assoc., 1993, vol. 88, no. 424, pp. 1273–1283.

    Article  Google Scholar 

  24. Seliskar, D.M., Effect of reciprocal transplanting between extremes of plant zones on morphometric plasticity of five plant species in an Oregon salt marsh, Can. J. Bot., 1985, vol. 63, no. 12, pp. 2254–2262.

    Article  Google Scholar 

  25. Slikker, W., Jr., Andersen, M.E., Bogdanffy, M.S., et al., Dose-dependent transitions in mechanisms of toxicity, Toxicol. Appl. Pharmacol., 2004, vol. 201, no. 3, pp. 203–225.

    PubMed  Article  CAS  Google Scholar 

  26. The Angiosperm Phylogeny Group, An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III, Bot. J. Linn. Soc., 2009, vol. 161, no. 2, pp. 105–121.

    Google Scholar 

  27. The R Development Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, 2012. http://www.R-project.org/

    Google Scholar 

  28. Tieszen, L.L. and Helgager, J.A., Genetic and physiological adaptation in the Hill reaction of Deschampsia caespitosa, Nature, 1968, vol. 219, pp. 1066–1967.

    PubMed  Article  CAS  Google Scholar 

  29. Trubina, M.R. and Dulya, O.V., Specific features of changes in the abundance of local populations and the distribution pattern of individual plants in meadow species growing in the vicinity of a copper smelter, in Biologicheskaya rekul’tivatsiya i monitoring narushennykh zemel’ (Biological Remediation of Disturbed Lands), Yekaterinburg, 2007, pp. 639–649.

    Google Scholar 

  30. Trubina, M.R. and Vorobeichik, E.L., Severe industrial pollution increases the β-diversity of plant communities, Doklady Biol. Sci., 2012, vol. 442, pp. 17–19.

    Article  CAS  Google Scholar 

  31. Verkleij, J.A., Van Hoof, N., Chardonnens, A.N., et al., Mechanisms of heavy metal resistance in Silene vulgaris, in Plant Nutrition: Food Security and Sustainability of Agro-Ecosystems, Horst, W.J., Schenk, M.K., et al., Eds., Amsterdam: Kluwer, 2001, pp. 446–447.

    Google Scholar 

  32. Vorobeichik, E.L. and Pozolotina, V.N., Microscale spatial variation in forest litter phytotoxicity, Russ. J. Ecol., 2003, vol. 34, no. 6, pp. 381–388.

    Article  CAS  Google Scholar 

  33. Vorobeichik, E.L., Sadykov, O.F., and Farafontov, M.G., Ekologicheskoe normirovanie tekhnogennykh zagryaznenii nazemnykh ekosistem (Ecological Rating of Technogenic Pollution in Terrestrial Ecosystems), Yekaterinburg: Nauka, 1994.

    Google Scholar 

  34. Weltje, L., Integrating evolutionary genetics and ecotoxicology: On the correspondence between reaction norms and concentration-response curves, Ecotoxicology, 2003, vol. 12, no. 6, pp. 523–528.

    PubMed  Article  CAS  Google Scholar 

  35. Wilkins, D.A., A technique for the measurement of lead tolerance in plants, Nature, 1957, vol. 180, no. 4575, pp. 37–38.

    Article  CAS  Google Scholar 

  36. Wilkins, D.A., The measurement of tolerance to edaphic factors by means of root growth, New Phytol, 1978, vol. 80, no. 3, pp. 623–633.

    Article  CAS  Google Scholar 

  37. Zhukova, L.A., Tufted hair grass, in Biologicheskaya flora Moskovskoi oblasti (Biological Flora of the Moscow Region), Moscow, 1976, vol. 3, pp. 62–75.

    Google Scholar 

  38. Zhuravskaya, A.N., Pozolotina, V.N., and Kershengol’ts, B.M., The radiosensitivity of the seeds of the plants of Central Yakutia, Russ. J. Ecol., 1997, vol. 28, no. 1, pp. 15–19.

    Google Scholar 

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Correspondence to O. V. Dulya.

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Original Russian Text © O.V. Dulya, V.S. Mikryukov, E.L. Vorobeichik, 2013, published in Ekologiya, 2013, No. 4, pp. 243–253.

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Dulya, O.V., Mikryukov, V.S. & Vorobeichik, E.L. Strategies of adaptation to heavy metal pollution in Deschampsia caespitosa and Lychnis flos-cuculi: Analysis based on dose-response relationship. Russ J Ecol 44, 271–281 (2013). https://doi.org/10.1134/S1067413613040036

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Keywords

  • Lychnis
  • Deschampsia
  • Silene
  • root elongation test
  • population
  • adaptation
  • tolerance
  • sensitivity
  • dose-response relationship
  • effective concentrations
  • industrial pollution
  • heavy metals
  • copper
  • Middle Ural Copper Smelter