Advertisement

Theoretical and Experimental Plant Physiology

, Volume 28, Issue 4, pp 415–423 | Cite as

Accumulation of cadmium by halophytic and non-halophytic Juncus species

  • Tomáš Vaněk
  • Kateřina Moťková
  • Radka PodlipnáEmail author
Article

Abstract

Halophytic plants have developed different strategies to survive and complete their life cycles under high concentrations of salts especially NaCl. Important features of salinity tolerance involve the production of various osmolytes, such as proline, glycine betaine, sugars, and ion compartmentalization. We supposed that these unique features could be also used in response to heavy metal stress. To test this hypothesis, we studied the effects of cadmium (Cd) on two species of a congeneric pair: the halophyte Juncus gerardii and glycophyte (non-halophyte) Juncus inflexus cultivated in vitro and in vivo. Their different salinity tolerance was evidenced by cultivation on media containing 100 and 300 mM NaCl. Only J. gerardii was able to grow well on medium with 300 mM NaCl for 28 days. In addition, both species were cultivated on media supplemented with Cd. The concentrations of Cd and proline in plant roots and leaves were measured after 2, 5, and 7 days in in vitro culture and after 7, 14, and 28 days in hydroponic solution. The accumulation of Cd did not significantly differ between these two species regardless of cultivation conditions (in vitro or hydroponic solution). However, the halophytic plant J. gerardii transported higher amount (128%) of Cd to shoots than J. inflexus and the free proline content significantly increased in response to cadmium exposure. The addition of NaCl (100 mM) decreased by 2.32 fold the accumulation of Cd and by 2.22 folds the proline content in J. gerardii.

Keywords

Halophyte Cadmium accumulation Proline Juncus gerardii Juncus inflexus 

Notes

Acknowledgments

This study was supported by projects MYES of CR n. OC10028 and MIT of CR n. FR-TI3/778.

Supplementary material

40626_2016_78_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 kb)

References

  1. Ali B, Qian P, Jin R, Ali S, Khan M, Aziz R, Tian T, Zhou W (2014) Physiological and ultra-structural changes in Brassica napus seedlings induced by cadmium stress. Biol Plant 58:131–138CrossRefGoogle Scholar
  2. Ashraf M, Foolad MR (2007) Roles of glycinebetaine and proline in improving plant abiotic stress tolerance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  3. Bates LS, Waldren RP, Teari D (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  4. Caçador I, Caetano M, Duarte B, Vale C (2009) Stock and losses of trace metals from salt marsh plants. Mar Environ Res 67(2):75–82CrossRefPubMedGoogle Scholar
  5. Chai MW, Shi FC, Li RL, Liu FC, Qiu GY, Liu LM (2013) Effect of NaCl on growth and Cd accumulation of halophyte Spartina alterniflora under CdCl2 stress. S Afr J Bot 85:63–69CrossRefGoogle Scholar
  6. Chen CT, Chen TH, Loa KF, Chiu CY (2004) Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111CrossRefGoogle Scholar
  7. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dos Reis SP, Lima AM, de Souz CRB (2012) Recent molecular advances on downstream plant responses to abiotic stress. Int J Mol Sci 13:8628–8647CrossRefPubMedPubMedCentralGoogle Scholar
  9. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963CrossRefPubMedGoogle Scholar
  10. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11CrossRefPubMedGoogle Scholar
  11. Hoagland DR (1920) Optimum nutrient solutions for plants. Science 52:562–564CrossRefPubMedGoogle Scholar
  12. Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42CrossRefGoogle Scholar
  13. Jiang YQ, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jones HG, Corlett JE (1992) Current topics in drought physiology. J Agric Sci 119:291–296CrossRefGoogle Scholar
  15. Jordan FL, Robin-Abbott M, Maier RM, Glenn EP (2002) A comparison of chelator-facilitated metal uptake by a halophyte and a glycophyte. Environ Toxicol Chem 21(12):2698–2704CrossRefPubMedGoogle Scholar
  16. Lee JH (2013) An overview of phytoremediation as a potentially promising technology for environmental pollution control. Biotechnol Bioproc E 18:431–439CrossRefGoogle Scholar
  17. Lefèvre I, Marchal G, Meerts P, Corréal E, Lutts S (2009) Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. Environ Exp Bot 65:142–152CrossRefGoogle Scholar
  18. Lutts S, Lefévre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot 115:509–528CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ma LJ, Yu CM, Li XM, Li YY, Wang LL, Ma CY, Tao SY, Bu N (2013) Pretreatment with NaCl induces tolerance of rice seedlings to subsequent Cd or Cd + NaCl stresses. Biol Plant 57:567–570CrossRefGoogle Scholar
  20. Manousaki E, Kalogerakis N (2011) Halophytes-an emerging trend in phytoremediation. Int J Phytoremediat 13(10):959–969CrossRefGoogle Scholar
  21. Monteiro CC, Carvalho RF, Gratao PL, Carvalho G, Tezotto T, Medici LO, Peres LEP, Azevedo RA (2011) Biochemical responses of the ethylene-insensitive Never ripe tomato mutant subjected to cadmium and sodium stresses. Environ Exp Bot 71(2):306–320CrossRefGoogle Scholar
  22. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663CrossRefPubMedGoogle Scholar
  23. Nitsch JP, Nitsch C (1965) Néoformation de fleurs in vitro chez une espèce de jours courts: Plumbago indica L. Ann Physiol Vég 7:251–256Google Scholar
  24. Parraga-Aguado I, González-Alcaraz MN, Álvarez-Rogel J, Conesa HM (2014) Assessment of the employment of halophyte plant species for the phytomanagement of mine tailings in semiarid areas. Ecol Eng 71:598–604CrossRefGoogle Scholar
  25. Podlipná R, Fialová Z, Vaněk T (2010) Degradation of nitroesters by plant tissue cultures. J Hazard Mater 184:591–596CrossRefPubMedGoogle Scholar
  26. Podlipná R, Skálová L, Seidlová H, Szotáková B, Kubíček V, Stuchlíková L, Jirásko R, Vaněk T, Vokřál I (2013) Biotransformation of benzimidazole anthelmintics in reed (Phragmites australis) as a potential tool for their detoxification in environment. Bioresour Technol 144:216–224CrossRefPubMedGoogle Scholar
  27. Qing DJ, Lu HF, Li N, Dong HT, Dong DF, Li YZ (2009) Comparative profiles of gene expression in leaves and roots of maize seedlings under conditions of salt stress and the removal of salt stress. Plant Cell Physiol 50:889–903CrossRefPubMedGoogle Scholar
  28. Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45(4):481–487CrossRefGoogle Scholar
  29. Sangwan RS, Gorenflot R (1975) In vitro culture of Phragmites tissue. Callus formation, organ differentation and cell suspension culture. Z Pflanzenphysiol 75:256–269CrossRefGoogle Scholar
  30. Santos MSS, Pedro CA, Goncalves SC, Ferreira SMF (2015) Phytoremediation of cadmium by the facultative halophyte plant Bolboschoenus maritimus (L.) Palla, at different salinities. Environ Sci Poll Res 22(20):15598–15609CrossRefGoogle Scholar
  31. 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(4):711–726CrossRefPubMedGoogle Scholar
  32. Sharma A, Gontia-Mishra AK, Srivastava I (2011) Toxicity of heavy metals on germination and seedling growth of Salicornia brachiata. J Phytol 3(9):33–36Google Scholar
  33. Soudek P, Petrová Š, Benešová D, Dvořáková M, Vaněk T (2011a) Uranium uptake by hydroponically cultivated crop plants. J Environ Radioact 102(6):598–604CrossRefPubMedGoogle Scholar
  34. Soudek P, Petrova S, Vanek T (2011b) Heavy metal uptake and stress responses of hydroponically cultivated garlic (Allium sativum L.). Environ Exp Bot 74:289–295CrossRefGoogle Scholar
  35. Soudek P, Petrová Š, Vaňková R, Song J, Vaněk T (2014) Accumulation of heavy metals using Sorghum sp. Chemosphere 104:15–24CrossRefPubMedGoogle Scholar
  36. Souza LA, Piotto FA, Nogueirol RC, Azevedo RA (2013) Use of non-hyperaccumulator plant species for the phytoextraction of heavy metals using chelating agents. Sci Agric 70(4):290–295CrossRefGoogle Scholar
  37. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97CrossRefPubMedGoogle Scholar
  38. Theriappan P, Gupta AK, Dhasarathan P (2011) Accumulation of proline under salinity and heavy metal stress in cauliflower seedlings. J Appl Sci Environ Manag 15(2):251–255Google Scholar
  39. Tkalec M, Stefanić PP, Cvjetko P, Sikić S, Pavlica M, Balen B (2014) The effects of cadmium-zinc interactions on biochemical responses in tobacco seedlings and adult plants. PLoS One 9(1):e87582CrossRefPubMedPubMedCentralGoogle Scholar
  40. Touchette BW, Iannacone LR, Turner GE, Frank AR (2007) Drought tolerance versus drought avoidance: a comparison of plant–water relations in herbaceous wetland plants subjected to water withdrawal and repletion. Wetlands 27:656–667CrossRefGoogle Scholar
  41. Touchette BW, Smith GA, Rhodes KL, Poole M (2009) Tolerance and avoidance: two contrasting physiological responses to salt stress in mature marsh halophytes Juncus roemerianus Scheele and Spartina alterniflora Loisel. J Exp Mar Biol Ecol 380:106–112CrossRefGoogle Scholar
  42. Vitoria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57(5):701–710CrossRefPubMedGoogle Scholar
  43. Walia H, Wilson C, Zeng LH, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63:609–623CrossRefPubMedGoogle Scholar
  44. Wang HL, Tian CY, Jiang L, Wang L (2014) Remediation of heavy metals contaminated saline soils: a halophyte choice? Environ Sci Technol 48(1):21–22CrossRefPubMedGoogle Scholar
  45. Watharkar AD, Jadhav JP (2014) Detoxification and decolorization of simulated textile dye mixture by phytoremediation using Petunia grandiflora and Gailardia grandiflora: a plant-plant consortial strategy. Ecotoxicol Environ Saf 103:1–8CrossRefPubMedGoogle Scholar
  46. Xue ZC, Gao HY, Zhang LT (2013) Effects of cadmium on growth, photosynthetic rate, and chlorophyll content in leaves of soybean seedlings. Biol Plant 57:587–590CrossRefGoogle Scholar
  47. Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus Vulgaris L.) seedlings. Acta Biol Crac Ser Bot 47(2):157–164Google Scholar
  48. Zhao F, McGrath SP, Crosland AR (1994) Comparison of three wet digestion methods for the determination of plant sulfur by inductively couple plasma atomic emission spectrometry (ICP-AES). Commun Soil Sci Plant Anal 25:407–418CrossRefGoogle Scholar
  49. Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124(3):941–948CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zlatev ZS (2005) Effects of water stress on leaf water relations of young bean plants. J Cent Eur Agric 6:5–14Google Scholar

Copyright information

© Brazilian Society of Plant Physiology 2016

Authors and Affiliations

  • Tomáš Vaněk
    • 1
  • Kateřina Moťková
    • 1
  • Radka Podlipná
    • 1
    Email author
  1. 1.Laboratory of Plant Biotechnologies, Institute of Experimental BotanyCzech Academy of Sciences v.v.vi.Prague 6Czech Republic

Personalised recommendations