Environmental Science and Pollution Research

, Volume 23, Issue 12, pp 12414–12422 | Cite as

The impact of Ni on the physiology of a Mediterranean Ni-hyperaccumulating plant

  • Enrica Roccotiello
  • Helena Cristina Serrano
  • Mauro Giorgio Mariotti
  • Cristina Branquinho
Research Article

Abstract

High nickel (Ni) levels exert toxic effects on plant growth and plant water content, thus affecting photosynthesis. In a pot experiment, we investigated the effect of the Ni concentration on the physiological characteristics of the Ni hyperaccumulator Alyssoides utriculata when grown on a vermiculite substrate in the presence of different external Ni concentrations (0–500 mg Ni L−1). The results showed that the Ni concentration was higher in leaves than in roots, as evidenced by a translocation factor = 3 and a bioconcentration factor = 10. At the highest concentration tested (500 mg Ni L−1), A. utriculata accumulated 1100 mg Ni per kilogram in its leaves, without an effects on its biomass. Plant water content increased significantly with Ni accumulation. Ni treatment did not, or only slightly, affected chlorophyll fluorescence parameters. The photosynthetic efficiency (FV/FM) of A. utriculata was stable between Ni treatments (always ≥ 0.8) and the photosynthetic performance of the plant under Ni stress remained high (performance index = 1.5). These findings support that A. utriculata has several mechanisms to avoid severe damage to its photosynthetic apparatus, confirming the tolerance of this species to Ni under hyperaccumulation.

Keywords

Bioconcentration factor Biomass Brassicaceae Hyperaccumulation Metal Photosynthesis 

Supplementary material

11356_2016_6461_MOESM1_ESM.doc (100 kb)
ESM 1(DOC 99 kb)

References

  1. Adamidis GC, Aloupi M, Kazakou E, Dimitrakopoulos PG (2014) Intra-specific variation in Ni tolerance, accumulation and translocation patterns in the Ni-hyperaccumulator Alyssum lesbiacum. Chemosphere 95:496–502CrossRefGoogle Scholar
  2. Amari T, Ghnaya T, Debez A, Taamali M, Ben Youssef N, Lucchini G, Sacchi GA, Abdelly C (2014) Comparative Ni tolerance and accumulation potentials between Mesembryanthemum crystallinum (halophyte) and Brassica juncea: metal accumulation, nutrient status and photosynthetic activity. J Plant Physiol 171:1634–1644CrossRefGoogle Scholar
  3. Anjum NA, Singh HP, Khan MIR, Masood A, Per TS, Negi A, Batish DR, Khan NA, Duarte AC, Pereira E, Ahmad I (2015) Too much is bad—an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environ Sci Pollut Res Int 22:3361–3382CrossRefGoogle Scholar
  4. Assunção AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159:351–360CrossRefGoogle Scholar
  5. Barceló J, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37CrossRefGoogle Scholar
  6. Bazzicalupo M, Roccotiello E, De Benedetti L, Bobbio V, Allavena A, Mariotti MG (2014) Analisi AFLP di Alyssoides utriculata (L.) Medik., specie iperaccumulatrice di nichel AFLP. Proceedings of the X Convegno Nazionale Sulla Biodiversità 3–5 settembre 2014 Consiglio Nazionale delle Ricerche, Roma 362–367 Rossi G, Alba E, Benedetti A, Bucci G, Ciaccia C, Pacucci C, Pinzari F, Scarascia Mugnozza G (eds) ISBN 978-88-97081-76-0 (in Italian)Google Scholar
  7. Bert V, Meerts P, Saumitou-Laprade P, Salis P, Gruber W, Verbruggen N (2003) Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249:9–18CrossRefGoogle Scholar
  8. Bhatia NP, Baker AJ, Walsh KB, Midmore DJ (2005) A role for nickel in osmotic adjustment in drought-stressed plants of the nickel hyperaccumulator Stackhousia tryonii Bailey. Planta 223:134–139CrossRefGoogle Scholar
  9. Bjorkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504CrossRefGoogle Scholar
  10. Boisvert S, Joly D, Leclerc S, Govindachary S, Harnois J, Carpentier R (2007) Inhibition of the oxygen-evolving complex of photosystem II and depletion of extrinsic polypeptides by nickel. Biometals 20:879–89CrossRefGoogle Scholar
  11. Bussotti F, Strasser RJ, Schaub M (2007) Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. Environ Pollut 147:430–437CrossRefGoogle Scholar
  12. Centofanti T, Sayers Z, Cabello-Conejo MI, Kidd P, Nishizawa NK, Kakei Y, Davis AP, Sicher RC, Chaney RL (2013) Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373:59–75CrossRefGoogle Scholar
  13. Chaney RL, Chen KY, Li Y-M, Angle JS, Baker AJM (2008) Effects of calcium on nickel tolerance and accumulation in Alyssum species and cabbage grown in nutrient solution. Plant Soil 311:131–140CrossRefGoogle Scholar
  14. Charlot G (1964) Colorimetric determination of elements. Elsevier Scientific Publishing Co, AmsterdamGoogle Scholar
  15. Coman V, Robotin P, Ilea P (2013) Nickel recovery/removal from industrial wastes: a review. Resour Conserv Recycl 73:229–238CrossRefGoogle Scholar
  16. Council Directive 86/278/EEC of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:31986L0278&from=PL. Accessed April 2009
  17. DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132CrossRefGoogle Scholar
  18. Dan TV, KrishnaRaj S, Saxena PK (2000) Metal tolerance of scented geranium (Pelargonium sp. ‘Frensham’): effects of cadmium and nickel on chlorophyll fluorescence kinetics. Int J Phytoremediat 2:91–104CrossRefGoogle Scholar
  19. Decreto Legislativo 3 aprile 2006, n. 152 Norme in materia ambientale pubblicato nella Gazzetta Ufficiale n. 88 del 14 aprile 2006 - suppl. ord. n. 96. http://www.camera.it/parlam/leggi/deleghe/06152dl5.htm (in Italian)
  20. Dixon NE, Gazzola C, Blakeley RL, Zerner B (1975) Jack-Bean Urease (EC 3.5.1.5.3). a metalloenzyme. A simple biological role for nickel. J Am Chem Soc 97:4131–4133CrossRefGoogle Scholar
  21. ENSCONET (2009) ENSCONET Seed Collecting Manual for Wild Species, Edition 1Google Scholar
  22. Gajewska E, SklodowskaM SM, Mazur J (2006) Effect of nickel on antioxidative enzymes activities, proline and chlorophyll contents in wheat shoots. Biol Plant 50:653–659CrossRefGoogle Scholar
  23. Galardi F, Corrales I, Mengoni A, Pucci S, Barletti L, Barzanti R, Arnetoli M, Gabbrielli R, Gonnelli C (2007) Intra-specific differences in nickel tolerance and accumulation in the Ni-hyperaccumulator Alyssum bertolonii. Environ Exp Bot 60:377–384CrossRefGoogle Scholar
  24. GENMEDOC (2005) Un rèseau interrégional de banques de semences de la Mediterranee http://www.genmedoc.org/eng/progetto/raccolta.html. Accessed Jan 2005 (in French)
  25. Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna N (2014) A preliminary study of the role of nickel in enhancing flowering of the nickel hyperaccumulating plant Alyssum inflatum Nyár. (Brassicaceae). S Afr J Bot 92:47–52CrossRefGoogle Scholar
  26. Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna N (2015) Calcium: magnesium ratio affects environmental stress sensitivity in the serpentine-endemic Alyssum inflatum (Brassicaceae). Aust J Bot 63:39–46Google Scholar
  27. Goolsby EW, Mason CM (2015) Toward a more physiologically and evolutionarily relevant definition of metal hyperaccumulation in plants. Front Plant Sci 6:33CrossRefGoogle Scholar
  28. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395CrossRefGoogle Scholar
  29. Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63CrossRefGoogle Scholar
  30. Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer, BerlinCrossRefGoogle Scholar
  31. Katsou E, Malamis S, Haralambous KJ, Loizidou M (2010) Use of ultrafiltration membranes and aluminosilicate minerals for nickel removal from industrial wastewater. J Membr Sci 360:234–249CrossRefGoogle Scholar
  32. Kozlow MV (2005) Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter, natural selection or phenotypic acclimation? Chemosphere 59:189–197CrossRefGoogle Scholar
  33. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefGoogle Scholar
  34. Krämer U, Cotter-Howells JD, Charnock JM, Baker AJM, Smith JAC (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638CrossRefGoogle Scholar
  35. Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353CrossRefGoogle Scholar
  36. Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–3000CrossRefGoogle Scholar
  37. Küpper H, Parameswaran A, Leitenmaier B, Trtílek M, Šetlík I (2007) Cadmium-induced inhibition of photosynthesis and long-term acclimation to cadmium stress in the hyperaccumulator Thlaspi caerulescens. New Phytol 175:655–674CrossRefGoogle Scholar
  38. Lal N (2010) Molecular mechanisms and genetic basis of heavy metal toxicity and tolerance in plants. In: Ashraf M, Ozturk M, Ahmad MSA (eds) Plant adaptation and phytoremediation. Springer, Dordrecht, pp 35–58CrossRefGoogle Scholar
  39. Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883CrossRefGoogle Scholar
  40. Llamas A, Ullrich CI, Sanz A (2008) Ni2+ toxicity in rice: effect on membrane functionality and plant water content. Plant Physiol Biochem 46:905–910CrossRefGoogle Scholar
  41. Lolkema PC, Donker MH, Kanneworff WA (1983) Physiological and biochemical aspects of Cu tolerance in Silene cucubalus. In: Proc Int Conf Heavy metals in the Environment Heidelberg, CEP Consultants, Edinburgh, pp 451–454Google Scholar
  42. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–736CrossRefGoogle Scholar
  43. Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  44. Marsili S (2010) Flora e vegetazione delle ultramafiti italiane: quadro delle conoscenze e studi finalizzati alla conservazione delle specie e degli habitat. PhD Dissertation, University of Genoa (in Italian)Google Scholar
  45. Mehes-Smith M, Nkongolo KK (2015) Physiological and cytological responses of Deschampsia cespitosa and Populus tremuloides to soil metal contamination. Water Air Soil Pollut 226:125CrossRefGoogle Scholar
  46. Molas J (2002) Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni II complexes. Environ Exp Bot 47:115–126CrossRefGoogle Scholar
  47. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216CrossRefGoogle Scholar
  48. Nagy L, Proctor J (1997) Soil Mg and Ni as causal factors of plant occurrence and distribution at the Meikle Kilrannoch ultramafic site in Scotland. New Phytol 135:561–566CrossRefGoogle Scholar
  49. Ouzounidou G, Moustakas M, Symeonidis L, Karataglis S (2006) Response of wheat seedlings to Ni stress: effects of supplemental calcium. Arch Environ Contam Toxicol 50:346–352CrossRefGoogle Scholar
  50. Ozyigit II, Vardar F, Yasar U, Akinci S (2013) Long-term effects of aluminum and cadmium on growth, leaf anatomy, and photosynthetic pigments of cotton. Commun Soil Sci Plant Annal 44:3076–3091CrossRefGoogle Scholar
  51. Pietrini F, Iori V, Cheremisina A, Shevyakova NI, Radyukina N, Kuznetsov VV, Zacchini M (2015) Evaluation of nickel tolerance in Amaranthus paniculatus L. plants by measuring photosynthesis, oxidative status, antioxidative response and metal-binding molecule content. Environ Sci Pollut Res Int 22:482–494CrossRefGoogle Scholar
  52. Pignatti S (1982) Alyssoides. In: Pignatti S (ed) Flora d’Italia, vol 1. Edagricole, Bologna, pp 422–423Google Scholar
  53. Polacco JC, Mazzafera P, Tezotto T (2013) Opinion—nickel and urease in plants: still many knowledge gaps. Plant Sci 199–200:79–90CrossRefGoogle Scholar
  54. Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217–218:8–17CrossRefGoogle Scholar
  55. Riggi A (2014) Tolleranza al nichel in piante e ceppi fungini nativi di suoli metalliferi e non-metalliferi. Dissertation, University of Genoa (in Italian)Google Scholar
  56. Roccotiello E (2011) Caratterizzazione della flora italiana di substrati ultramafici:stato dell’arte e studi finalizzati all’individuazione di nuovi taxa iperaccumulatori. PhD Dissertation, University of Genoa (in Italian)Google Scholar
  57. Roccotiello E, Zotti M, Mesiti S, Marescotti P, Carbone C, Cornara L, Mariotti MG (2010) Biodiversity in metal-polluted soils. Fresenius Environ Bull 19:2420–2425Google Scholar
  58. Roccotiello E, Serrano HC, Mariotti MG, Branquinho C (2015) Nickel phytoremediation potential of the Mediterranean Alyssoides utriculata L. Medik. Chemosphere 119:1372–1378CrossRefGoogle Scholar
  59. Scheckel KG, Chaney RL, Basta NT (2009) Advances in assessing bioavailability of metal(loid)s in contaminated soils. In: Sparks DL (ed) Advances in Agronomy. Elsevier BV, Amsterdam, pp 1–52Google Scholar
  60. Sellami R, Gharbi F, Rejeb S, Rejeb MN, Henchi B, Echevarria G, Morel J (2012) Effects of nickel hyperaccumulation on physiological characteristics of Alyssum murale grown on metal contaminated waste amended soil. Int J Phytoremediat 14:609–620CrossRefGoogle Scholar
  61. Seregin IV, Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russ J Plant Physiol 48:523–544CrossRefGoogle Scholar
  62. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277CrossRefGoogle Scholar
  63. Silva S, Pinto G, Dias MC, Correia C, Moutinho-Pereira J, Pinto-Carnide O, Santos C (2012) Aluminium long-term stress differently affects photosynthesis in rye genotypes. Plant Physiol Biochem 54:105–112CrossRefGoogle Scholar
  64. Singh VP (2005) Metal toxicity in plants systems. In: Metal toxicity and tolerance in plants and animals. Sarup and Sons, New Dheli, pp 152–202Google Scholar
  65. Singh PK, Tewari SK (2003) Cadmium toxicity induced changes in plant water relations and oxidative metabolism of Brassica juncea L. plants. J Environ Biol 24:107–117Google Scholar
  66. Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140CrossRefGoogle Scholar
  67. Strasser RJ, Tsimilli-Michael M (2001) Stress in plants from daily rhythm to global changes, detected and quantified by the JIP test. Chim Nouv 75:3321–3326Google Scholar
  68. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, New York, pp 321–362CrossRefGoogle Scholar
  69. Talke IN, Hanikenne M, Krämer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167CrossRefGoogle Scholar
  70. Van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  71. Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066CrossRefGoogle Scholar
  72. Vithanage M, Rajapaksha AU, Oze C, Rajakaruna N, Dissanayake CB (2014) Metal release from serpentine soils in Sri Lanka. Environ Monit Assess 186:3415–3429CrossRefGoogle Scholar
  73. Weng LP, Wolthoorn A, Lexmond TM, Temminghoff EJM, Van Riemsdijk WH (2004) Understanding the effects of soil characteristics on phytotoxicity and bioavailability of nickel using speciation models. Environ Sci Technol 38:156–162CrossRefGoogle Scholar
  74. WHO (2006) Environmental health criteria 234. Elemental speciation in human health risk assessment. World Health Organization, GenevaGoogle Scholar
  75. Wierzbicka M, Panufnik D (1998) The adaptation of Silene vulgaris to growth on a calamine waste heap (S. Poland). Environ Pollut 101:415–426CrossRefGoogle Scholar
  76. Willems G, Dräger DB, Courbot M, Godé C, Verbruggen N, Saumitou-Laprade P (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri Brassicaceae: an analysis of quantitative trait loci. Genetics 176:659–674CrossRefGoogle Scholar
  77. Witte CP (2011) Urea metabolism in plants. Plant Sci 180:431–438CrossRefGoogle Scholar
  78. Yusuf M, Fariduddin Q, Hayat S, Ahmad A (2011) Nickel: an overview of uptake, essentiality and toxicity in plants. Bull Environ Contam Toxicol 86:1–17CrossRefGoogle Scholar
  79. Zhang Z, Rengel Z, Meney K (2010) Cadmium accumulation and translocation in four emergent wetland species. Water Air Soil Pollut 212:239–249CrossRefGoogle Scholar
  80. Zhang X, Xia H, Li Z, Zhuang P, Gao B (2011) Identification of a new potential Cd-hyperaccumulator Solanum photeinocarpum by soil seed bank-metal concentration gradient method. J Hazard Mater 189:414–419CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Enrica Roccotiello
    • 1
  • Helena Cristina Serrano
    • 2
  • Mauro Giorgio Mariotti
    • 1
  • Cristina Branquinho
    • 2
  1. 1.DISTAV Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Laboratorio di Biologia VegetaleUniversità degli Studi di GenovaGenoaItaly
  2. 2.Centro de Ecologia, Evolução e Alterações Ambientais (cE3c) Faculdade de CiênciasUniversidade de LisboaLisbonPortugal

Personalised recommendations