Abstract
This greenhouse study aimed to examine the contribution of arbuscular mycorrhizal (AM) colonization on the uptake of and tolerance to nickel (Ni) in sunflower (Helianthus annuus L.). We hypothesized that AM colonization increases Ni content and tolerance in sunflower grown under varying soil Ni concentrations. The combined effect of AM colonization and soil Ni input on the assimilation of nitrogen, in particular the activity of glutamine synthetase (GS), in sunflower plants was also investigated. A factorial experimental design was performed with sunflower cv. Lemon Queen, with or without the AM fungus, Glomus intraradices Schenck & Smith, and treated with 0, 100, 200, or 400 mg Ni kg−1 dry soil (DS). The AM colonization significantly enhanced plant growth and Ni content, especially at the lower soil Ni treatments. Furthermore, the AM plants exposed to the highest soil Ni level of 400 mg Ni kg−1 DS had a significantly higher shoot Ni extracted percentage than non-AM plants, suggesting that the AM symbiosis contributed to Ni uptake, then its translocation from roots to shoots. The AM colonization also significantly increased the GS activity in roots, this being likely an indicator of an enhanced Ni tolerance. These findings support the hypothesis that AM symbiosis contributes to an enhanced Ni plant uptake and tolerance and should be considered as part of phytoremediation strategies.
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References
Ahonen-Jonnarth U, Finlay RD (2001) Effects of elevated nickel and cadmium concentrations on growth and nutrient uptake of mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 236:129–138
Audet P, Charest C (2006) Effects of AM colonization on ‘wild tobacco’ plants grown in zinc-contaminated soil. Mycorrhiza 16:277–283
Audet P, Charest C (2007) Heavy metal phytoremediation from a meta-analytical perspective. Environ Pollut 147:231–237
Audet P, Charest C (2008) Allocation plasticity and plant–metal partitioning: metal-analytical perspectives in phytoremediation. Environ Pollut 156:290–296
Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654
Bhatia NP, Walsh KB, Baker AJM (2005) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. J Exper Bot 56:1343–1349
Chen B, Christie P, Li X (2001) A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42:185–192
Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotech 13:393–397
Dalpé Y (1993) Vesicular–arbuscular mycorrhizae. In: Carter MR (ed) Soil sampling and methods of analysis. CRC, Boca Raton, pp 287–301
Davies FT, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407
Gildon A, Tinker PB (1983) Interactions of vesicular–arbuscular mycorrhizal infection and heavy metals in plants: the effects of heavy metals on the development of vesicular–arbuscular mycorrhizae. New Phytol 95:147–161
Hewitt EJ, Smith TA (1975) Plant mineral nutrition. Wiley, New York, pp 32–33
Insightful Corp. (2003) S-Plus 6.2 for Windows. Insightful Corp., Seattle
Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234
Jones MD, Hutchinson TC (1988) Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. Uptake of nickel, calcium, magnesium, phosphorus and iron. New Phytol 108:461–470
Kastori P, Petrovic N, Petrovic M (1996) Effects of lead on water relations, proline concentration and nitrate reductase activity in sunflower plants. Acta Agron Hungar 44:21–28
Killham K, Firestone MK (1983) Vesicular arbuscular mycorrhizal mediation of grass response to acidic and heavy metal depositions. Plant Soil 72:39–48
Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Hálácsy. Plant Physiol 115:1641–1650
Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-hyperaccumulator Thlaspi species. Plant Physiol 122:1343–1353
Leopold I, Günther D, Schmidt J, Neumann D (1999) Phytochelatins and heavy metal tolerance. Phytochemistry 50:1323–1328
Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153
Li YM, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115
Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL (2000) Acquisition of Cu, Zn, Mn and Fe by mycorrhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza 9:331–336
Marschner H (1995) Mineral nutrition in higher plants, 2nd edn. Academic, London
McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207–214
Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229
Reeves RD, Macfarlane RM, Brooks RR (1983) Accumulation of nickel and zinc by western North American genera containing serpentine-tolerant species. Amer J Bot 70:1297–1303
Saber NE, Abdel-Moneim AM, Barakat SY (1999) Role of organic acids in sunflower tolerance to heavy metals. Biol Planta 42:65–73
Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47:339–347
Slivinskaya RB (1991) Nickel effect on sunflower leaf cell membranes. Acta Bot Neerl 40:133–138
Toussaint JP, St-Arnaud M, Charest C (2004) Nitrogen transfer and assimilation between the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith and Ri T-DNA roots of Daucus carota L in an in vitro compartmented system. Can J Microbiol 50:251–260
Turgut C, Pepe MK, Cutright TJ (2004) The effect of EDTA and citric acid on phytoremediation of Cd, Cr, and Ni from soil using Helianthus annuus. Environ Pollut 131:147–154
Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultramafic soils in South Africa. Mycorrhiza 13:185–190
Ximénez-Embún P, Alonso I, Madrid-Albarrán Y, Cámara C (2004) Establishment of selenium uptake and species distribution in lupine, Indian mustard, and sunflower plants. J Agric Food Chem 52:832–838
Yang XH, Brooks RR, Jaffré T, Lee J (1985) Elemental levels and relationships in the Flacourtiaceae of New Caledonia and their significance for the evaluation of the ‘serpentine problem’. Plant Soil 87:281–291
Zornoza P, Robles S, Martin N (1999) Alleviation of nickel toxicity by ammonium supply to sunflower. Plant Soil 208:221–226
Acknowledgment
This work was funded by a grant of the Natural Science and Engineering Research Council of Canada to C. Charest.
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Ker, K., Charest, C. Nickel remediation by AM-colonized sunflower. Mycorrhiza 20, 399–406 (2010). https://doi.org/10.1007/s00572-009-0293-7
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DOI: https://doi.org/10.1007/s00572-009-0293-7