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Journal of Plant Nutrition

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Plant tolerance to nickel toxicity: II nickel effects on influx and transport of mineral nutrients in four plant species X. Yangab; V. C. Baligara; D. C. Martensab; R. B. Clarka a U.S. Department of Agriculture, Agricultural Research Service (USDA-ARS), Appalachian Soil & Water Conservation Research Laboratory, Beckley, WV b Department of Crop & Soil Environmental Sciences, Virginia Polytechnic Institute and State University (VPI & SU), Blacksburg, VA, USA

To cite this Article Yang, X. , Baligar, V. C. , Martens, D. C. and Clark, R. B.(1996) 'Plant tolerance to nickel toxicity: II

nickel effects on influx and transport of mineral nutrients in four plant species', Journal of Plant Nutrition, 19: 2, 265 — 279 To link to this Article: DOI: 10.1080/01904169609365121 URL: http://dx.doi.org/10.1080/01904169609365121

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JOURNAL OF PLANT NUTRITION, 19(2), 265-279 (1996)

PLANT TOLERANCE TO NICKEL TOXICITY: II NICKEL EFFECTS ON INFLUX AND TRANSPORT OF MINERAL NUTRIENTS IN FOUR PLANT SPECIES

Downloaded By: [USDA Natl Agricultul Lib] At: 20:17 27 May 2010

X. Yang1, V. C. Baligar2, D. C. Martens1, and R. B. Clark U.S. Department of Agriculture, Agricultural Research Service (USDA-ARS), Appalachian Soil & Water Conservation Research Laboratory, P.O. Box 867, Beckley, WV 25802-0867 ABSTRACT: Nickel (Ni) is an essential micronutrient for higher plants but is toxic to plants at excess levels. Plant species differ extensively for mineral uptake and accumulation, and these differences often help explain plant tolerances to mineral toxicities/deficiencies. Solution culture experiments were conducted under controlled conditions to determine the effects of Ni on influx into roots (IN) and transport from roots to shoots (TR) of zinc (Zn), iron (Fe), copper (Cu), manganese (Mn), calcium (Ca), magnesium (Mg), phosphorus (P), and sulfur (S) in white clover (Trifolium repens L.), cabbage (ßrassica oleracea van capitata L.), ryegrass (Lolium perenne L.), and maize (Zea mays L.). Nickel decreased both IN and TR of Zn, Cu, Ca, and Mg, but only TR of Fe and Mn in white clover. Both IN and TR of Cu, Fe, Mn, Mg, and S were markedly decreased by Ni >30 µM in cabbage, whereas IN and TR of P increased with Ni treatment. For ryegrass, TR of Cu, Fe, Mn, Ca, and Mg was decreased, but IN of these elements except Mg was not affected by Ni. The IN and TR of P and S were increased in ryegrass with increasing external Ni levels. Nickel inhibited IN of Cu, Ca, and Mg, and TR of Zn, Cu, Fe, Mn, Ca, and Mg in maize. Plant species differed in response to Ni relative to IN and TR of mineral nutrients. Plant tolerance to Ni toxicity was

1. Department of Crop & Soil Environmental Sciences, Virginia Polytechnic Institute and State University (VP1 & SU), Blacksburg, VA 24061, USA. 2. Corresponding author.

265 Copyright © 1996 by Marcel Dekker, Inc.

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associated with the influence of Ni on IN and TR of Cu, Fe, and Mn in white clover and cabbage but not in maize and ryegrass. INTRODUCTION Nickel is an essential micronutrient for higher plants (Brown et al., 1987; Eskew et al., 1983,1984). However, Ni at sufficiently high levels may be toxic to plants (Bingham et al, 1986; Farago and Cole, 1986; Foy et al., 1978). Excess Ni can affect physiological/biochemical process like decreasing leaf chlorophyll contents (Pandolfini et al., 1992; Piccini and Malavolta, 1992) and leaf photosynthetic and transpiration activities (Carlson, 1975; Jones and Hutchinson, 1988a; Morgutti et al., 1984; Rauser and Dunbroff, 1981), and impairing membrane permeability associated with enhanced extracellular peroxidase activity (Pandolfini et al., 1992). Typical Ni toxicity symptoms are chlorosis followed by mottling and necrosis on leaves, and distorted and stunted growth of shoots and roots (Hutchinson, 1981; Khalid and Tinsley, 1980; Misha and Kar, 1974; Yang et al., 1996). These symptoms often result from disturbances or imbalances of mineral nutrients. For example, Ni toxicity has often been considered secondary to Cu when plants have been grown in contaminated soils or contain elevated Ni concentrations (Craig, 1978; Dang et al., 1990; Farago and Cole, 1986), and Fe deficiency induced by excess Ni has been regarded as a Ni toxicity symptom (Bingham et al, 1986; Foy et al., 1978). Nickel also competitively inhibited uptake of Ca, Mg, Fe, and Zn in tomato (JLycopersicon esculentum L.) (Chamel and Heuman, 1987), and Cu uptake in rice (Oryza sativa L.) (Tang and Miller, 1991). Excess Ni also reduced shoot concentrations of P, Ca, Mg, and Fe in birch (Betula papyrifera Marsh.) seedlings (Jones and Hutchinson, 1988b). In addition, excess Co, Cu, Fe, and Zn inhibited Ni absorption by soybean [Glycine max (L.) Merr.] roots, but excess Mg and Mn did not (Cataldo et al., 1978). Nickel induced Fe deficiency in plants has often been associated with inhibition of Fe translocation from roots to shoots (Aller et al., 1990; Foy et al., 1978). Nickel effects have also been closely related to Ni/Fe ratios in plant tissue rather than Ni andFe concentrations per se (Khalid and Tinsley, 1980). Nickel was toxic to bean (Phaseolus vulgaris L.) grown with 1 to 2 (Xg Ni/L in nutrient solution, and Ni increased Fe but had no effect on Ca, Mg, Mn, and Zn concentrations (Piccini and Malavolta, 1992). Barley (Hordeum vulgaris L.) also developed Ni toxicity

PLANT TOLERANCE TO NICKEL TOXICITY. II

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from excess Ni, but Ni did not reduce Fe translocation from roots to shoots as noted for Zn, Cu, Mn, and Co (Agarwala et al., 1977). Differences noted in the literature about Ni interactions with mineral nutrient elements may have resulted because of variability among plant species/cultivars used. The effects of Ni on mineral nutrient concentrations in plant tissues may not be evident because of reductions or cessation of plant growth caused by excess Ni. The objectives of this study were to determine effects of Ni on IN and TR of Zn, Cu, Fe, Mn, Ca, Mg, P, and S in four plant species. MATERIALS AND METHODS Four plants species, white clover (Trifolium repens L. cv 'California Ladino1), ryegrass (Lolium perenne L. cv "Linn1), cabbage (Brassica olerácea var. capitataL. cv 'Early Jersey Wakefield'), and maize (Zea mays L. hybrid 'Early Sunglow'), were grown in nutrient solutions in a growth chamber. Chamber conditions were 25/20°C, 60/70% relative humidity, 14/10 h (light/dark) with a photon flux density of 400 |iE/s2/m2 derived from incandescent and fluorescent (Sylvania Cool White VHO 215 W) lamps. Composition of nutrient solutions was: 4.2 NO3-N, 0.4 NH4-N, 2.0 Ca, 1.0 K, 1.0 S, 0.5 Mg, and 0.1 P (in mM), and 20 Fe-EDDHA [ferric N,N'-ethylene bis(2-(2-hydroxy-phenyl) glycine)], 9.4 Cl, 6.6 B, 4.7 Mn, 0.6 Zn, 0.2 Cu, 0.2 Na, and 0.1 Mo (in U.M). To keep nutrient composition similar for the four plant species, Fe-EDDHA was used as the Fe source for all species (Fe-EDDHA for maize caused no Fe deficiency symptoms to appear during growth at Ni levels from 0 to 120 H-M). White clover seeds were scarified with sand paper, sterilized with 0.5% NaOCl (household bleach; 1 NaOCl: 10 water, V:V) for 5 minutes, and thoroughly rinsed with distilled water. Seeds of the other plant species were likewise sterilized. Sterilized seeds were germinated in rolled germination filter papers using aerated 0.1-strength nutrient solution. Once germinated and of sufficient size, seedlings were transferred to containers with full-strength nutrient solutions and grown to obtain additional growth prior to introduction to treatment solutions. Days from germination to the time plants were introduced to Ni treatments were 41 for white clover, 28 for ryegrass, 27 for cabbage, and 18 for maize. The number of plants of each species transferred to each 2-L container with Ni treatment was 20 for white clover, 30 for ryegrass, 15 for cabbage, and 5 for maize. Nickel treatments were 0, 15, 30, 60, 120, 240, and 320 \lM added as Ni(NO3)2. Once plants were intro-


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duced to treatments, pH of nutrient solutions was maintained daily at 5.5. Plants were grown in Ni treatments for 14 days. Treatments were randomized with three replications. Plant samples were harvested at the start and end of Ni treatment periods. At harvest, roots of intact plants were immersed in 20 mM Na2-EDTA (disodium ethylenediaminetetraacetate) for 15 min to remove Ni adhering to root surfaces. Roots and stalk bases were thoroughly rinsed with bi-distilled water, blotted dry, and shoots separated from roots. Shoots were dried at 65°C in a forced-air oven and weighed. Roots were cut into 1-2 cm segments, mixed thoroughly, and ~2 g representative fresh samples collected for root length measurements using a Comair root length scanner (Commonwealth Aircraft Corporation, Melbourne, Australia1). The remainder of roots was dried similar to shoots and weighed. Dried shoot and root samples were ground to pass 0.5-mm stainless steel screen for chemical analysis. Samples (100 mg) were weighed into plastic containers, nitric acid (1.0 mL 15.6M HN03) was added, containers placed in Parr microwave acid digestion bombs (Parr Instrument Co., Moline, IL3), microwaved for 4 minutes at 70% power, cooled, transferred to new containers, diluted to 10.0 mL with bi-distilled water, and filtered. Mineral nutrient and relatively high Ni concentrations were determined by inductively coupled plasma spectroscopy (Applied Research Laboratories, Dearborn, MI1) and Ni at low levels by graphite furnace atomic absorption spectroscopy (Perkin Elmer, Norwalk, CT1). The IN of mineral nutrients into roots and TR of mineral nutrients from roots to shoots were calculated (Baligar et al., 1993): IN = [(PU2 - PUi)/(t2 - ti)] x [(InRL2 - InRLl)/(RL2 - RLi)]

[1]

TR = [(SU2 - SUi)/(t2 - ti)] x [(lnSW2 - InSWi)/(SW2 - SWi)]

[2]

where: PU = Ni concentration in whole plant (mmol Ni/plant); t = time (days) of sampling at the start (subscript 1) and end (subscript 2) of Ni treatment; RL = root length (m/plant); SU = Ni concentration in shoots (mmol/plant); SW = shoot dry weight (g/plant). Values for IN were converted to pmol/cm RL/s and TR to nmol/g SW/s.

3. Mention of particular companies or commercial products does not imply recommendations or endorsement by USDA-ARS or VPI & SU over companies or products not mentioned.

PLANT TOLERANCE TO NICKEL TOXICITY. II

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RESULTS Dry Matter Relative comparisons among plant species for shoot and root dry matter (DM) were made (Fig. 1). Shoot DM decreased to 80% and root DM decreased to 60% of controls for cabbage. Shoot DM increased slightly and root DM decreased to 80% of controls for maize grown with up to 60 \ÏM. Ni. For plants grown with >60 \iM Ni, shoot DM of cabbage and maize decreased to 50% of controls, and root DM of ryegrass and maize decreased to 20% of controls. Root growth of each species decreased more than shoot growth because of added Ni. Influx of Nutrients into Roots The effects of Ni on IN of Zn, Cu, Fe, and Mn differed greatly in the various plant species (Fig- 2). For plants grown with up to 60 |iM Ni, IN of Cu, Fe, and Mn in cabbage was 60, 30, and 80% of controls, respectively. The IN of Zn decreased to 80% and IN of Cu to 60% of controls in white clover grown with up to 60 (iM Ni. However, plants grown with external Ni up to 120 \iM had no decreases in IN of Zn, Fe, and Mn in either ryegrass or maize, nor in IN of Cu in ryegrass. The IN of Mg decreased to ~70% of controls in both cabbage and white clover grown with up to 60 \iM Ni, but was not affected in maize and ryegrass grown with similar external Ni (Fig. 3). The IN of Ca was inhibited in ryegrass grown with 60 \iM Ni.


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Ni concentration (uM) FIGURE 1. Shoot and root dry matter (DM) of four plant species grown with different levels of Ni in nutrient solution. The vertical bars depict LSD (P