Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel.
The nickel (Ni) hyperaccumulator Alyssum murale has been developed as a commercial crop for phytoremediation/phytomining Ni from metal-enriched soils. Here, metal co-tolerance, accumulation and localization were investigated for A. murale exposed to metal co-contaminants. A. murale was irrigated with Ni-enriched nutrient solutions containing basal or elevated concentrations of cobalt (Co) or zinc (Zn). Metal localization and elemental associations were investigated in situ with synchrotron X-ray microfluorescence (SXRF) and computed-microtomography (CMT). A. murale hyperaccumulated Ni and Co (> 1000 microg g(-1) dry weight) from mixed-metal systems. Zinc was not hyperaccumulated. Elevated Co or Zn concentrations did not alter Ni accumulation or localization. SXRF images showed uniform Ni distribution in leaves and preferential localization of Co near leaf tips/margins. CMT images revealed that leaf epidermal tissue was enriched with Ni but devoid of Co, that Co was localized in the apoplasm of leaf ground tissue and that Co was sequestered on leaf surfaces near the tips/margins. Cobalt-rich mineral precipitate(s) form on leaves of Co-treated A. murale. Specialized biochemical processes linked with Ni (hyper)tolerance in A. murale do not confer (hyper)tolerance to Co. A. murale relies on a different metal storage mechanism for Co (exocellular sequestration) than for Ni (vacuolar sequestration).
Tappero
R
R
Plant and Soil Sciences, University of Delaware, Newark, DE 19716, USA.
Peltier
E
E
Plant and Soil Sciences, University of Delaware, Newark, DE 19716, USA.
Gräfe
M
M
Plant and Soil Sciences, University of Delaware, Newark, DE 19716, USA.
Heidel
K
K
Plant and Soil Sciences, University of Delaware, Newark, DE 19716, USA.
Ginder-Vogel
M
M
Geological and Environmental Sciences, Stanford University, Stanford, CA 94305, USA.
Livi
K J T
KJT
Earth and Planetary Sciences, John Hopkins University, Baltimore, MD 21218, USA.
Rivers
M L
ML
Geophysical Sciences and Center for Advanced Radiation Sources, University of Chicago, Chicago, IL 60637, USA.
Marcus
M A
MA
Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Chaney
R L
RL
USDA-ARS, Environmental Management and By-products Utilization, Beltsville, MD 20705, USA.
Sparks
D L
DL
Plant and Soil Sciences, University of Delaware, Newark, DE 19716, USA.
D001673:Biodegradation, Environmental; D019607:Brassicaceae / Q000378:metabolism*; D002118:Calcium / Q000737:chemistry / Q000378:metabolism; D003035:Cobalt / Q000737:chemistry / Q000378:metabolism*; D008345:Manganese / Q000737:chemistry / Q000378:metabolism; D008670:Metals / Q000737:chemistry / Q000378:metabolism*; D009532:Nickel / Q000737:chemistry / Q000378:metabolism*; D018515:Plant Leaves / Q000378:metabolism; D012987:Soil / Q000032:analysis; D015032:Zinc / Q000737:chemistry / Q000378:metabolism
D008670:Metals; D012987:Soil; D003035:Cobalt; D008345:Manganese; D009532:Nickel; D015032:Zinc; D002118:Calcium
Adriano DC. 1986. Trace elements in the terrestrial environment. New York, NY, USA: Springer-Verlag, Inc., 1-18.
Arru L, Rognoni S, Baroncini M, Bonatti PM, Perata P. 2004. Copper localization in Cannabis sativa L. grown in a copper-rich solution. Euphytica 140: 33-38.
Baker AJM. 1981. Accumulators and excluders - strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3: 643-654.
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: 9-18.
Bidwell SD, Crawford SA, Woodrow IE, Sommer-Knudsen J, Marshall AT. 2004. Sub-cellular localization of Ni in the hyperaccumulator Hybanthus floribundus (Lindley) F. Muell. Plant, Cell & Environment 27: 705-716.
Broadhurst CL, Chaney RL, Angle JA, Erbe EF, Maugel TK. 2004a. Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265: 225-242.
Broadhurst CL, Chaney RL, Angle JS, Maugel TK, Erbe EF, Murphy CA. 2004b. Simultaneous hyperaccumulation of nickel, manganese, and calcium in Alyssum leaf trichomes. Environmental Science & Technology 38: 5797-5802.
Brooks RR, Lee J, Reeves RD, Jaffre T. 1977. Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. Journal of Geochemistry and Exploration 7: 49-57.
Chaney RL. 1983. Plant uptake of inorganic waste constituents. In: Parr JF, Marsh PB, Kla JM, eds. Land treatment of hazardous wastes. Park Ridge, NJ, USA: Noyes Data Corp., 50-76.
Chaney RL. 1988. Plants can utilize iron from Fe-N,N′-di-(2-hydroxy-benzoyl)-ethylenediamine-N,N′-diacetic acid, a ferric chelate with 106 greater formation constant than Fe-EDDHA. Journal of Plant Nutrition 11: 1033-1050.
Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM. 1997. Phytoremediation of soil metals. Current Opinions in Biotechnology 8: 279-284.
Chaney RL, Angle JS, Baker AJM, Li YM. 2004. Method for phytomining of nickel, cobalt, and other metals from soil. US patent 5,944,872.
Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H. 2001. Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213: 45-50.
Dixon NE, Gazola C, Blakeley RL, Zerner B. 1975. Jack bean urease (EC 3.5.1.5), a metalloenzyme. A simple biological role for nickel? Journal of the American Chemistry Society 97: 4131-4133.
Dowd BA, Campbell GH, Marr RB, Nagarkar VV, Tipnis SV, Axe L, Siddons DP. 1999. Developments in synchrotron X-ray computed microtomography at the National Synchrotron Light Source. Proceedings of SPIE, Developments in X-Ray Tomography II 3772: 224-236.
Fellows RJ, Wang Z, Ainsworth CC. 2003. Europium uptake and partitioning in Oat (Avena sativa) roots as studied by laser-induced fluorescence spectroscopy and confocal microscopy profiling technique. Environmental Science & Technology 37: 5247-5253.
Frérot H, Lefèbvre C, Petit C, Collin C, Dos Santos A, Escarré J. 2005. Zinc tolerance and hyperaccumulation in F1 and F2 offspring from intra and interecotype crosses of Thlaspi caerulescens. New Phytologist 165: 111-119.
Frey B, Keller C, Zierold K, Schulin R. 2000. Distribution of Zn in functionally different leaf epidermal cells of the hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 23: 675-687.
Gabbrielli R, Mattioni C, Vergnano O. 1991. Accumulation mechanisms and heavy metal tolerance of a nickel hyperaccumulator. Journal of Plant Nutrition 14: 1067-1080.
Gustafson FG. 1956. Absorption of 60Co by leaves of young plants and its translocation through the plant. American Journal of Botany 43: 157-160.
Hamilton EI. 1994. The geobiochemistry of cobalt. Science of the Total Environment 150: 7-39.
Handreck KA, Riceman DS. 1969. Cobalt distribution in several plant species grown in culture solutions. Australian Journal of Agricultural Research 20: 213-226.
Heath SM, Southworth D, Allura JAD. 1997. Localization of nickel in epidermal subsidiary cells of leaves of Thlaspi montanum var. siskiyouense (Brassicaceae) using energy-dispersive X-ray microanalysis. International Journal of Plant Science 158: 184-188.
Homer FA, Morrison RS, Brooks RR, Clemens J, Reeves RD. 1991. Comparative studies of nickel, cobalt, and copper uptake by some nickel hyperaccumulators of the genus Alyssum. Plant Soil 138: 195-205.
Ingrouille MJ, Smirnoff N. 1986. Thlaspi caerulescens J. & C. Presl. (T. alpestre L.) in Britain. New Phytologist 102: 219-233.
Irving H, Williams RJP. 1948. Order of stability of metal complexes. Nature 6: 746-747.
Kabata-Pendias A, Kabata H. 1984. Elements of Group VIII. In: Trace elements in soils and plants. Boca Raton, FL, USA: CRC Press Inc., 238-246.
Kerkeb L, Krämer U. 2003. The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiology 131: 716-724.
Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML. 2006. Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314: 1295-1298.
Krämer U, Cotterhowells JD, Charnock JM, Baker AJM, Smith JC. 1996. Free histidine as a metal chelator in plants that accumulate nickel. Nature 379: 635-638.
Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE. 1997a. The role of metal transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiology 115: 1641-1650.
Krämer U, Grime GW, Smith JAC, Hawes CR, Baker AJM. 1997b. Micro-PIXE as a technique to study nickel localization in leaves of the hyperaccumulator plant Alyssum lesbiacum. Nuclear Instruments and Methods in Physics Research B 130: 346-350.
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 Physiology 122: 1343-1354.
Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ. 2004. The effect of pH on metal accumulation in two Alyssum species. Journal of Environmental Quality 33: 2090-2102.
Küpper H, Zhao FJ, McGrath SP. 1999. Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiology 119: 305-311.
Küpper H, Lombi E, Zhao FJ, McGrath SP. 2000. Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212: 75-84.
Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP. 2001. Cellular compartmentation of nickel in the hyperaccumulator Alyssum lesbiacum, Alyssum bertolonii, and Thlaspi goesingense. Journal of Experimental Botany 52: 2291-2300.
Küpper H, Kroneck PMH. 2005. Heavy metal uptake by plants and cyanobacteria. In: Sigel A, Sigel H, Sigel Royal, eds. Metal ions in biological systems, Vol. 44. New York, NY, USA: Marcel Dekker, 97-142.
Langston R. 1956. Distribution patterns of radioisotopes in plants. Proceedings of the American Society of Horticultural Science 68: 370-376.
Li YM, Chaney RL, Brewer E, Roseberg R, Angle JS, Baker AJM, Reeves R, Nelkin J. 2003a. Development of a technology for commercial phytoextraction of nickel: economic and technological considerations. Plant Soil 249: 107-115.
Li YM, Chaney RL, Brewer EP, Angle JS, Nelkin J. 2003b. Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environmental Science & Technology 37: 1463-1468.
Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D. 1999. Zinc tolerance and hyperaccumulation are genetically independent characters. Proceedings of the Royal Society of London B 266: 2175-2179.
Macnair MR, Tilstone GH, Smith SE. 2000. The genetics of metal tolerance and accumulation in higher plants. In: Terry N, Bañuelos G, eds. Phytoremediation of contaminated soil and water. Boca Raton, FL, USA: Lewis Publishers, 235-250.
Malik M, Chaney RL, Brewer EP, Li Y, Angle JS. 2000. Phytoextraction of soil cobalt using hyperaccumulator plants. International Journal of Phytoremediation 2: 319-329.
Marcus MA, MacDowell AA, Celestre R, Manceau A, Miller T, Padmore HA, Sublett RE. 2004. Beamline 10.3.2 at ALS: a hard X-ray microprobe for environmental and materials sciences. Journal of Synchrotron Radiation 11: 239-247.
Marschner H. 1995. Mineral nutrition of higher plants, 2nd edn. New York, NY, USA: Academic Press.
McNear DH Jr, Peltier E, Everhart J, Chaney RL, Newville M, Rivers M, Sutton S, Sparks DL. 2005. Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environmental Science and Technology 39: 2210-2218.
Mesjasz-Przybylowicz J, Przybylowicz WJ, Prozesky VW, Pineda CA. 1997. Quantitative micro-PIXE comparison of elemental distribution in Ni-hyperaccumulating and non-accumulating genotypes of Senecio coronatus. Nuclear Instruments and Methods in Physics Research B 130: 368-373.
Mizuno N, Takahashi A, Wagatsuma T, Mizuno T, Obata H. 2002. Chemical composition of guttation fluid and leaves of Petasites japonicus var. giganteus and Polygonum cuspidatum growing on ultramafic soil. Soil Science Plant Nutrition 48: 451-453.
Morrison Richard S. 1980. Aspects of the accumulation of cobalt, copper, and nickel by plants. PhD Thesis, Massey University, Palmerton North, New Zealand.
Neumann D, Zur Nieden U. 2001. Silicon and heavy metal tolerance of higher plants. Phytochemistry 56: 685-692.
Neumann D, Zur Nieden U, Schwieger W, Leopold I, Lichtenberger O. 1997. Heavy metal tolerance of Minuartia verna. Journal of Plant Physiology 151: 101-108.
Norkus E, Vaskelis A, Griguceviciene A, Rozovskis G, Reklaitis J, Norkus P. 2001. Oxidation of cobalt (II) with air oxygen in aqueous ethylenediamine solutions. Transition Metal Chemistry 26: 465-472.
Palit S, Sharma A, Talukder G. 1994. Effects of cobalt on plants. Botany Reviews 60: 149-181.
Pollard AJ, Powell KD, Harper FA, Smith JAC. 2002. The genetic basis of metal hyperaccumulation in plants. Critical Reviews in Plant Science 21: 539-566.
Psaras GK, Constantinidis T, Cotsopoulos B, Manetas Y. 2000. Relative abundance of nickel in the leaf epidermis of eight hyperaccumulators: evidence that the metal is excluded from both guard cells and trichomes. Annals of Botany 86: 73-78.
Rivers M, Wang Y. 2006. Recent developments in microtomography at GeoSoil-EnviroCARS. Proceedings of SPIE, Developments in X-ray tomography. V. 631(0J-): 1-15.
Salt DE, Krämer U. 2000. Mechanism of metal hyperaccumulation in plants. In: Raskin L, Ensley BD, eds. Phytoremediation of toxic metals. New York, NY, USA: John Wiley, 231-236.
Sarret G, Harada E, Choi YE, Isaure MP, Geoffroy N, Birschwilks M, Clemens S, Fakra S, Marcus MA, Manceau A. 2006. Trichomes of tobacco excrete zinc as Zn-substituted calcium carbonate and other Zn-containing compounds. Plant Physiology 141: 1021-1034.
Schat H, Llugany M, Bernhard R. 2000. Metal-specific patterns of tolerance, uptake, and transport of heavy metals in hyperaccumulating and nonhyperaccumulating metallophytes. In: Terry N, Bañuelos G, eds. Phytoremediation of contaminated soil and water. Boca Raton, FL, USA: Lewis Publishers, 171-188.
Scheckel KG, Lombi E, Rock SA, McLaughlin MJ. 2004. In vivo synchrotron study of Thallium speciation and compartmentalization in Iberris intermedia. Environmental Science Technology 38: 5095-5100.
Sparks DL. 2003. Environmental Soil Chemistry, 2nd edn. New York, NY, USA: Academic Press, 133-186.
Still ER, Williams RJP. 1980. Potential methods for selective accumulation of Nickel (II) ions by plants. Journal of Inorganic Biochemistry 13: 35-40.
Sutton S, Bertsch PM, Newville M, Rivers M, Lanzirotti A, Eng P. 2002. Microfluorescence and microtomography analyses of heterogeneous earth and environmental materials. In: Fenter PM, Rivers M, Sturchio N, Sutton S, eds. Applications of synchrotron radiation in low-temperature geochemistry and environmental science, Vol. 49. Washington DC, USA: Mineralogical Society of America, 429-483.
Vergnano O, Hunter JG. 1952. Nickel and cobalt toxicities in Oat plants. Annals of Botany 17: 317-329.
Walker DJ, Bernal MP. 2004. The effects of copper and lead on growth and zinc accumulation of Thlaspi caerulescens J. & C. Presl: implications for phytoremediation of contaminated soils. Water Air Soil Pollution 151: 361-372.
Welch RM. 1995. Micronutrient nutrition of plants. Critical Reviews in Plant Science 14: 49-82.