Plant and Soil

, Volume 428, Issue 1–2, pp 213–222 | Cite as

Differential interactive effects of the Ca/Mg quotient and PEG-simulated drought in Alyssum inflatum and Fortuynia garcinii

  • Behrooz Salehi-Eskandari
  • Seyed Majid Ghaderian
  • Henk Schat
Regular Article


Background and aims

Serpentine soils typically have low Ca/Mg quotients, low water-holding capacities, and are rich in Ni and Cr, but poor in N and P. To better understand the role of drought and low Ca/Mg quotients in plant adaptation to serpentine soil, we compared the effects of different Ca/Mg quotients (0.18, 2 and 4) and polyethyleneglycol (PEG)–imposed osmotic stress on growth and Ca and Mg uptake and translocation between two Iranian serpentine endemic plant species, the Ni-hyperaccumulator Alyssum inflatum, and the non-accumulator Fortuynia garcinii.


Seedlings were grown in modified Hoagland’s solution with varying Ca/Mg molar quotients (0.18, 2 and 4) and then exposed to PEG (209.7 g L−1) for 8 days.


In both species, shoot dry weight was highest at the highest Ca/Mg quotient (4). However, at this Ca/Mg quotient A. inflatum suffered much more from PEG-induced drought (84% mortality and severe growth inhibition in the survivors), compared with the lower Ca/Mg quotients (<20% mortality and no significant growth inhibition). In F. garcinii, the PEG*Ca/Mg interaction was not significant. Shoot Ca concentrations and translocation factors in A. inflatum were higher than in F. garcinii in all the treatments. In both species the Mg translocation factor was highest at the highest Ca/Mg quotient (4) in the PEG treatment.


We conclude that a high Ca/Mg quotient stimulated growth in the absence of PEG in both species, but strongly decreased survival and growth in combination with PEG in A. inflatum. In F. garcinii root dry weight and the root to shoot dry weight ratio were significantly decreased at the highest Ca/Mg quotient (4), particularly after PEG treatment, suggesting that F. garcinii also may require a moderate or low Ca/Mg quotient to cope with natural drought.


Serpentine soil Ca/Mg quotients Osmotic stress Uptake Translocation 



We would like to thank the Graduate School of University of Isfahan for providing research facilities. We also thank Plant Antioxidants Center of Excellence (PACE) University of Isfahan for its support of this study.


  1. Anacker BL (2014) The nature of serpentine endemism. Am J Bot 101:219–224CrossRefPubMedGoogle Scholar
  2. Asemaneh T, Ghaderian SM, Baker AJM (2007) Responses to Mg/Ca balance in an Iranian serpentine endemic plant, Cleome heratensis (Capparaceae) and a related non-serpentine species, C. foliolosa. Plant Soil 293:49–59CrossRefGoogle Scholar
  3. Bhatia NP, Baker AJM, Walsh KB, Midmore DJ (2005) A role for nickelin osmotic adjustment in drought-stressed plants of the nickel hyperaccumulator Stackhousia tryonii bailey. Planta 223:134–139CrossRefPubMedGoogle Scholar
  4. Boldaji SH, Khavari-Nejad R, Sajedi RH, Fahimi H, Saadatmand S (2012) Water availability effects on antioxidant enzyme activities, lipid peroxidation, and reducing sugar contents of alfalfa (Medicago sativa L.). Acta Physiol Plant 34:1177–1186CrossRefGoogle Scholar
  5. Boyd RS, Martens SN (1992) The raison d’être for metal hyperaccumulation by plants. In: AJM B, Proctor J, Reeves RD (eds) The ecology of ultramaffic (serpentine) soils. Intercept, Andover, pp 279–289Google Scholar
  6. Bradshaw HD (2005) Mutations in CAX1 produce phenotypes characteristic of plants tolerant to serpentine soils. New Phytol 167:81–88CrossRefPubMedGoogle Scholar
  7. Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  8. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland, OregonGoogle Scholar
  9. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Biol 46:95–122CrossRefGoogle Scholar
  10. Cheng NH, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364CrossRefPubMedPubMedCentralGoogle Scholar
  11. Comino E, Whiting SN, Neumann PM, Baker AJM (2005) Salt (NaCl) tolerance in the Ni hyperaccumulator Alyssum murale and the Zn hyperaccumulator Thlaspi caerulescens. Plant Soil 270:91–99CrossRefGoogle Scholar
  12. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212CrossRefGoogle Scholar
  13. Ghaderian SM, Baker AJM (2007) Geobotanical and biogeochemical reconnaissance of the ultramafics of Central Iran. J Geochem Explor 92:34–42CrossRefGoogle Scholar
  14. Ghaderian SM, Mohtadi A, Rahiminejad MR, Baker AJM (2007a) Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from ultramafics of Iran. Environ Pollut 145:293–298CrossRefPubMedGoogle Scholar
  15. Ghaderian SM, Mohtadi A, Rahiminejad MR, Reeves RD, Baker AJM (2007b) Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant Soil 293:91–97CrossRefGoogle Scholar
  16. Ghasemi R, Chavoshi ZZ, Ghaderian SM (2015a) Stenocalcic properties in the serpentine-endemic plant Alyssum inflatum Nyárády. Aust JBot 63:31–38Google Scholar
  17. Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna N (2015b) Calcium: magnesium ratio affects environmental stress sensitivity in the serpentine-endemic Alyssum inflatum (Brassicaceae). Aust J Bot 63:39–46Google Scholar
  18. Ghasemi R, Share H, Sharifi R, Boyd RS, Rajakaruna N (2018) Inducing Ni sensitivity in the Ni hyperaccumulator plant Alyssum inflatum Nyárády (Brassicaceae) by transforming with CAX1, a vacuolar membrane calcium transporter. Ecol Res (in press)Google Scholar
  19. Goodwin-Bailey C, Woodell S, Loughman B (1992) The response of serpentine, mine spoil and saltmarsh races of Armeria maritima (mill.) Willd. To each others’ soils, the vegetation of ultramafic (serpentine) soils. Proceedings of the First International Conference on Serpentine Ecology, Hampshire, Intercept Ltd, p 390Google Scholar
  20. Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K (2015) Magnesium stress signaling in plant: just a beginning. Plant Signal Behav 10:e992287CrossRefPubMedPubMedCentralGoogle Scholar
  21. Harrison S, Rajakaruna N (2011) Serpentine: the evolution and ecology of a model system. Univ. of California Press, BerkeleyGoogle Scholar
  22. Hohl M, Peter S (1991) Water relationsof growing maize coleoptiles. Comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressure. Plant Physiol 95:716–722CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kachenko AG (2008) A role for nickel in drought resistance in water-stressed Hybanthus floribundus subsp. floribundus. PhD thesis, Univ. of Sydney, pp. 1–20Google Scholar
  24. Kazakou E, Dimitrakopoulos P, Baker AJM, Reeves RD, Troumbis A (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508PubMedGoogle Scholar
  25. Kazakou E, Adamidis G, Baker AJM, Reeves RD, Godino M, Dimitrakopoulos P (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332:369–385CrossRefGoogle Scholar
  26. Kolář F, Dortová M, Lepš J, Pouzar M, Krejčová A, Štech M (2014) Serpentine ecotypic differentiation in a polyploid plant complex: shared tolerance to Mg and Ni stress among di-and tetraploid serpentine populations of Knautia arvensis (Dipsacaceae). Plant Soil 374:435–447CrossRefGoogle Scholar
  27. Lawlor D (1970) Absorption of polyethylene glycols by plants and their effects on plant growth. New Phytol 69:501–513CrossRefGoogle Scholar
  28. Miller SP, Cumming JR (2000) Effects of serpentine soil factors on Virginia pine (Pinus virginiana) seedlings. Tree Physiol 20:1129–1135CrossRefPubMedGoogle Scholar
  29. Money NP (1989) Osmotic pressure of aqueous polyethylene glycols relationship between molecular weight and vapor pressure deficit. Plant Physiol 91:766–769CrossRefPubMedPubMedCentralGoogle Scholar
  30. Murren CJ, Douglass L, Gibson A, Dudash MR (2006) Individual and combined effects of Ca/Mg ratio and water on trait expression in Mimulus guttatus. Ecology 87:2591–2601CrossRefPubMedGoogle Scholar
  31. O’Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf ca: mg than in tolerance of low N, low P, or heavy metals. Plant Soil 280:49–64CrossRefGoogle Scholar
  32. Pakdaman N, Ghaderian SM, Ghasemi R, Asemaneh T (2013) Effects of calcium/magnesium quotients and nickel in the growth medium on growth and nickel accumulation in Pistacia atlantica. J Plant Nutr 36:1708–1718CrossRefGoogle Scholar
  33. Palm E, Brady K, Van Volkenburgh E (2012) Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Funct Plant Biol 39:679–688CrossRefGoogle Scholar
  34. Pandey R, Agarwal RM (1998) Water stress-induced changes in proline contents and nitrate reductase activity in rice under light and dark conditions. Physiol Mol Biol Plants 4:53–57Google Scholar
  35. Proctor J, Woodell SRJ (1975) The ecology of serpentine soils. Adv Ecol Res 9:255–366CrossRefGoogle Scholar
  36. Rajakaruna N, Boyd R (2008) The edaphic factor. In ‘Encyclopedia of ecology. Vol. 2’.(eds Jorgensen SE, Fath B) Elsevier, Oxford, pp 1201–1207Google Scholar
  37. Rajakaruna N, Siddiqi MY, Whitton J, Bohm BA, Glass AD (2003) Differential responses to Na+/K+ and Ca2+/Mg2+ in two edaphic races of the Lasthenia californica (Asteraceae) complex: a case for parallel evolution of physiological traits. New Phytol 157:93–103CrossRefGoogle Scholar
  38. Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59:435–444CrossRefPubMedGoogle Scholar
  39. Reeves RD, Baker A, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38CrossRefGoogle Scholar
  40. Roccotiello E, Serrano HC, Mariotti MG, Branquinho C (2015) Nickel phytoremediation potential of the Mediterranean Alyssoides utriculata (L.) Medik. Chemosphere 119:1372–1378CrossRefPubMedGoogle Scholar
  41. Salehi Eskandari B, Ghaderian SM, Ghasemi R, Schat H (2017a) Optimization of seed germination in an Iranian serpentine endemic, Fortuynia garcinii. Flora 231:38–42CrossRefGoogle Scholar
  42. Salehi Eskandari B, Ghaderian SM, Schat H (2017b) The role of nickel (Ni) and drought in serpentine adaptation: contrasting effects of Ni on osmoprotectants and oxidative stress markers in the serpentine endemic, Cleome heratensis, and the related non-serpentinophyte, Cleome foliolosa. Plant Soil 147:183–195CrossRefGoogle Scholar
  43. Schat H (1984) A comparative ecophysiological study on the effects of waterlogging and submergence on dune slack plants: growth, survival and mineral nutrition in sand culture experiments. Oecologia 62:279–286CrossRefPubMedGoogle Scholar
  44. Shi G, Xia S, Ye J, Huang Y, Liu C, Zhang Z (2015) PEG-simulated drought stress decreases cadmium accumulation in castor bean by altering root morphology. Environ Exp Bot 111:127–134CrossRefGoogle Scholar
  45. Statwick JM, Williams AK, Sher A (2017) Lack of evidence for the drought tolerance hypothesis of hyperaccumulation in Astragalus species. Int J Plant Sci 178:478–484CrossRefGoogle Scholar
  46. Verslues PE, Ober ES, Sharp RE (1998) Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiol 116:1403–1412CrossRefPubMedPubMedCentralGoogle Scholar
  47. Whiting SN, Neumann PM, Baker AJM (2003) Nickel and zinc hyperaccumulation by Alyssum murale and Thlaspi caerulescens (Brassicaceae) do not enhance survival and whole-plant growth under drought stress. Plant Cell Environ 26:351–360CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Behrooz Salehi-Eskandari
    • 1
    • 2
  • Seyed Majid Ghaderian
    • 1
  • Henk Schat
    • 3
  1. 1.Department of Biology, Faculty of SciencesUniversity of IsfahanIsfahanIran
  2. 2.Department of BiologyPayame Noor UniversityTehranIran
  3. 3.Department of Ecological Science, Faculty of Earth and Life SciencesVrije UniversiteitAmsterdamThe Netherlands

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