Environmental Science and Pollution Research

, Volume 22, Issue 10, pp 7600–7611 | Cite as

Palladium uptake by Pisum sativum: partitioning and effects on growth and reproduction

  • Matteo Ronchini
  • Laura Cherchi
  • Simone Cantamessa
  • Marco Lanfranchi
  • Alberto Vianelli
  • Paolo Gerola
  • Graziella Berta
  • Alessandro Fumagalli
Research Article


Environmental palladium levels are increasing because of anthropogenic activities. The considerable mobility of the metal, due to solubilisation phenomena, and its known bioavailability may indicate interactions with higher organisms. The aim of the study was to determine the Pd uptake and distribution in the various organs of the higher plant Pisum sativum and the metal-induced effects on its growth and reproduction. P. sativum was grown in vermiculite with a modified Hoagland’s solution of nutrients in the presence of Pd at concentrations ranging 0.10–25 mg/L. After 8–10 weeks in a controlled environment room, plants were harvested and dissected to isolate the roots, stems, leaves, pods and peas. The samples were analysed for Pd content using AAS and SEM-EDX. P. sativum absorbed Pd, supplied as K2PdCl4, beginning at seed germination and continuing throughout its life. Minimal doses (0.10–1.0 mg Pd/L) severely inhibited pea reproductive processes while showing a peculiar hormetic effect on root development. Pd concentrations ≥1 mg/L induced developmental delay, with late growth resumption, increased leaf biomass (up to 25 %) and a 15–20 % reduction of root mass. Unsuccessful repeated blossoming efforts led to misshapen pods and no seed production. Photosynthesis was also disrupted. The absorbed Pd (ca. 0.5 % of the supplied metal) was primarily fixed in the root, specifically in the cortex, reaching concentrations up to 200 μg/g. The metal moved through the stem (up to 1 μg/g) to the leaves (2 μg/g) and pods (0.3 μg/g). The presence of Pd in the pea fruits, together with established evidence of environmental Pd accumulation and bioavailability, suggests possible contamination of food plants and propagation in the food chain and must be the cause for concern.


Pea Pisum sativum Metal pollution Palladium Metal localisation Toxicity Hormesis AAS SEM-EDX 



The Fondo di Ateneo per la Ricerca (FAR) of the Università degli Studi dell’Insubria funded this study. We are indebted to the following undergraduate students that helped with this research: Carlotta Cattaneo, Simone Pigozzi, Flavia Fineo, Alessio Parise, Chiara Barassi, Massimo Zilio and Rachele Prada. We also thank the technician Giuliano Bonelli for support with the microscopic analyses.


  1. Aidid S, Okamoto H (1993) Responses of elongation growth rate, turgor pressure and cell wall extensibility of stem cells of Impatiens balsamina to lead, cadmium and zinc. Biometals 6:245–249CrossRefGoogle Scholar
  2. Alt F, Weber G, Messerschmidt J, von Bohlen A, Kastenholz B, Guenther K (2002) Bonding states of palladium in phytosystem: first results for endive. Anal Lett 35:1349–1359CrossRefGoogle Scholar
  3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefGoogle Scholar
  4. Aydınalp C, Marinova S (2009) The effect of heavy metals on seed germination and plant growth on alfalfa plant (Medicago sativa). Bulg J Agric Sci 15:348–351Google Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefGoogle Scholar
  6. Battke F, Leopold K, Maier M, Schmidhalter U, Schuster M (2008) Palladium exposure of barley: uptake and effects. Plant Biol 10:272–276CrossRefGoogle Scholar
  7. Brenchley WE (1934) The effect of rubidium sulphate and palladium chloride on the growth of plants. Ann App Biol 21:398–417CrossRefGoogle Scholar
  8. Brown PH, Welch RM, Cary EE (1987a) Nickel: a micronutrient essential for higher plants. Plant Physiol 85:801–803CrossRefGoogle Scholar
  9. Brown PH, Welch RM, Cary EE, Checkai RT (1987b) Beneficial effects of nickel on plant growth. J Plant Nutr 10:2125–2135CrossRefGoogle Scholar
  10. Carlson C, Adriano D, Sajwan K, Abels S, Thoma D, Driver J (1991) Effects of selected trace metals on germinating seeds of six plant species. Water Air Soil Pollut 59:231–240CrossRefGoogle Scholar
  11. Ceruti M, Berta G (1992) Effects of 2-Aza-2,3-dihydrosqualene on fine structure and meristematic activity of root apical cells of Allium porrum L. Life Sci Adv 11:115–123Google Scholar
  12. Chiu D-Y, Liu T (1997) Free radical and oxidative damage in human blood cells. J Biomed Sci 4:256–259CrossRefGoogle Scholar
  13. Cholewa E, Peterson CA (2004) Evidence for Symplastic Involvement in the Radial Movement of Calcium in Onion Roots. Plant Physiol 134:1793–1802CrossRefGoogle Scholar
  14. Clarkson DT (1991) Root structure and sites of ion uptake. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 417–453Google Scholar
  15. de la Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsola kali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere 55:1159–1168CrossRefGoogle Scholar
  16. Ek KH, Morrison GM, Rauch S (2004) Environmental routes for platinum group elements to biological materials—a review. Sci Total Environ 334–335:21–38CrossRefGoogle Scholar
  17. Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer, SunderlandGoogle Scholar
  18. Eskew DL, Welch RM, Cary EE (1983) Nickel: an essential micronutrient for legumes and possibly all higher plants. Science 222:621–623CrossRefGoogle Scholar
  19. Eskew DL, Welch RM, Norvell WA (1984) Nickel in higher plants: further evidence for an essential role. Plant Physiol 76:691–693CrossRefGoogle Scholar
  20. Fumagalli A, Faggion B, Ronchini M, Terzaghi G, Lanfranchi M, Chirico N, Cherchi L (2010) Platinum, palladium, and rhodium deposition to the Prunus laurus cerasus leaf surface as an indicator of the vehicular traffic pollution in the city of Varese area. Environ Sci Pollut Res 17:665–673CrossRefGoogle Scholar
  21. Fusconi A, Repetto O, Bona E, Massa N, Gallo C, Dumas-Gaudot E, Berta G (2006) Effects of cadmium on meristem activity and nucleus ploidy in roots of Pisum sativum L. cv. Frisson seedlings. Environ Exp Bot 58:253–260CrossRefGoogle Scholar
  22. Gagnon ZE, Newkirk C, Hicks S (2006) Impact of platinum group metals on the environment: a toxicological, genotoxic and analytical chemistry study. J Environ Sci Health, Part A 41:397–414CrossRefGoogle Scholar
  23. Gao B, Yu Y, Zhou H, Lu J (2012) Accumulation and distribution characteristics of platinum group elements in roadside dusts in Beijing, China. Environ Toxicol Chem 31:1231–1238CrossRefGoogle Scholar
  24. Gerendás J, Polacco JC, Freyermuth SK, Sattelmacher B (1999) Significance of nickel for plant growth and metabolism. J Plant Nutr Soil Sci 162:241–256CrossRefGoogle Scholar
  25. Grusak MA (1994) Iron Transport to Developing Ovules of Pisum sativum (I. Seed Import Characteristics and Phloem Iron-Loading Capacity of Source Regions). Plant Physiol 104:649–655Google Scholar
  26. Gür N, Topdemir A (2008) Effects of some heavy metals on in vitro pollen germination and tube growth of apricot (Armenica vulgaris Lam.) and cherry (Cerasus avium) L. World Appl Sci J 4:195–198Google Scholar
  27. Halliwell B, Gutteridge JMC (1999) Free Radicals in Biology and Medicine, 3rd edn. Oxford University Press, OxfordGoogle Scholar
  28. Hideg É, Spetea C, Vass I (1994) Singlet oxygen and free radical production during acceptor- and donor-side-induced photoinhibition: studies with spin trapping EPR spectroscopy. Biochim Biophys Acta Bioenerg 1186:143–152CrossRefGoogle Scholar
  29. Hocking P, Pate J (1977) Mobilization of Minerals to Developing Seeds of Legumes. Ann Botany 41:1259–1278Google Scholar
  30. Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187CrossRefGoogle Scholar
  31. Jakob B, Heber U (1996) Photoproduction and Detoxification of Hydroxyl radicals in Chloroplasts and Leaves and Relation to Photoinactivation of Photosystems I and II. Plant Cell Physiol 37:629–635CrossRefGoogle Scholar
  32. Jarvis KE, Parry SJ, Piper JM (2001) Temporal and Spatial Studies of Autocatalyst-Derived Platinum, Rhodium, and Palladium and Selected Vehicle-Derived Trace Elements in the Environment. Environ Sci Technol 35:1031–1036CrossRefGoogle Scholar
  33. Jia L, He X, Chen W, Liu Z, Huang Y, Yu S (2013) Hormesis phenomena under Cd stress in a hyperaccumulator—Lonicera japonica Thunb. Ecotoxicology 22:476–485CrossRefGoogle Scholar
  34. Kopittke PM, Asher CJ, Blamey FPC, Menzies NW (2007) Toxic effects of Pb2+ on the growth and mineral nutrition of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Plant Soil 300:127–136CrossRefGoogle Scholar
  35. Krzesłowska M, Lenartowska M, Mellerowicz EJ, Samardakiewicz S, Woźny A (2009) Pectinous cell wall thickenings formation—A response of moss protonemata cells to lead. Environ Exp Bot 65:119–131CrossRefGoogle Scholar
  36. Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski H, Woźny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable—a remobilization can occur. Environ Pollut 158:325–338CrossRefGoogle Scholar
  37. Leopold K, Maier M, Weber S, Schuster M (2008) Long-term study of palladium in road tunnel dust and sewage sludge ash. Environ Pollut 156:341–347CrossRefGoogle Scholar
  38. Lesniewska BA, Messerschmidt J, Jakubowski N, Hulanicki A (2004) Bioaccumulation of platinum group elements and characterization of their species in Lolium multiflorum by size-exclusion chromatography coupled with ICP-MS. Sci Tot Environ 322:95–108CrossRefGoogle Scholar
  39. Lide DR (1995) CRC Handbook of Chemistry and Physics, 76th edn. CRC PressGoogle Scholar
  40. Liu TZ, Lin TF, Chiu DTY, Tsai K-J, Stern A (1997) Palladium or Platinum Exacerbates Hydroxyl Radical Mediated DNA Damage. Free Radic Bio Med 23:155–161CrossRefGoogle Scholar
  41. Marcheselli M, Sala L, Mauri M (2010) Bioaccumulation of PGEs and other traffic-related metals in populations of the small mammal Apodemus sylvaticus. Chemosphere 80:1247–1254CrossRefGoogle Scholar
  42. Meyers DER, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153:323–332CrossRefGoogle Scholar
  43. Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591CrossRefGoogle Scholar
  44. Møller IM, Jensen PE, Hansson A (2007) Oxidative Modifications to Cellular Components in Plants. Annu Rev Plant Biol 58:459–481CrossRefGoogle Scholar
  45. Nischkauer W, Herincs E, Puschenreiter M, Wenzel W, Limbeck A (2013) Determination of Pt, Pd and Rh in Brassica napus using solid sampling electrothermal vaporization inductively coupled plasma optical emission spectrometry. Spectrochim Acta Part B 89:60–65CrossRefGoogle Scholar
  46. Odjegba VJ, Brown MT, Turner A (2007) Studies on the effects of platinum group elements on Lactuca sativa L. Am J Plant Phys 2:183–194CrossRefGoogle Scholar
  47. Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of Photosynthesis: from molecules to the field. Bios Scientific Publishers, Oxford, pp 1–24Google Scholar
  48. Polacco JC, Mazzafera P, Tezotto T (2013) Opinion—nickel and urease in plants: still many knowledge gaps. Plant Sci 199–200:79–90CrossRefGoogle Scholar
  49. Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta Bioenerg 1787:1151–1160CrossRefGoogle Scholar
  50. Qiu R-L, Zhao X, Tang Y-T, Yu F-M, Hu P-J (2008) Antioxidative response to Cd in a newly discovered cadmium hyperaccumulator, Arabis paniculata F. Chemosphere 74:6–12CrossRefGoogle Scholar
  51. Ravindra K, Bencs L, Van Grieken R (2004) Platinum group elements in the environment and their health risk. Sci Tot Environ 318:1–43CrossRefGoogle Scholar
  52. Ribeiro AP, Figueiredo AMG, Sarkis JES, Hortellani MA, Markert B (2012) First study on anthropogenic Pt, Pd, and Rh levels in soils from major avenues of São Paulo City, Brazil. Environ Monit Assess 184:7373–7382CrossRefGoogle Scholar
  53. Roshchin A, Veselov V, Panova A (1984) Industrial toxicology of metals of the platinum group. J Hyg Epidemiol Microbiol Immunol 28:17Google Scholar
  54. Sabrine H, Afif H, Mohamed B, Hamadi B, Maria H (2010) Effects of cadmium and copper on pollen germination and fruit set in pea (Pisum sativum L.). Sci Hortic 125:551–555CrossRefGoogle Scholar
  55. Schäfer J, Hannker D, Eckhardt JD, Stüben D (1998) Uptake of traffic-related heavy metals and platinum group elements (PGE) by plants. Sci Total Environ 215:59–67CrossRefGoogle Scholar
  56. Searcy KB, Mulcahy DL (1985) Pollen Tube Competition and Selection for Metal Tolerance in Silene dioica (Caryophyllaceae) and Mimulus guttatus (Scrophulariaceae). Am J Bot 72:1695–1699CrossRefGoogle Scholar
  57. Seth CS, Kumar Chaturvedi P, Misra V (2008) The role of phytochelatins and antioxidants in tolerance to Cd accumulation in Brassica juncea L. Ecotoxicol Environ Saf 71:76–85CrossRefGoogle Scholar
  58. Sobrova P, Zehnalek J, Adam V, Beklova M, Kizek R (2012) The effects on soil/water/plant/animal systems by platinum group elements. Cent Eur J Chem 10:1369–1382CrossRefGoogle Scholar
  59. Speranza A, Leopold K, Maier M, Taddei AR, Scoccianti V (2010) Pd-nanoparticles cause increased toxicity to kiwifruit pollen compared to soluble Pd(II). Environ Pollut 158:873–882CrossRefGoogle Scholar
  60. Tang Y-T, Qiu R-L, Zeng X-W, Ying R-R, Yu F-M, Zhou X-Y (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134CrossRefGoogle Scholar
  61. Theron AJ, Ramafi GJ, Feldman C, Grimmer H, Visser SS, Anderson R (2004) Effects of platinum and palladium ions on the production and reactivity of neutrophil-derived reactive oxygen species. Free Radic Bio Med 36:1408–1417CrossRefGoogle Scholar
  62. Vannini C, Domingo G, Marsoni M, Fumagalli A, Terzaghi R, Labra M, De Mattia F, Onelli E, Bracale M (2011) Physiological and molecular effects associated with palladium treatment in Pseudokirchneriella subcapitata. Aquat Toxicol 102:104–113CrossRefGoogle Scholar
  63. Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta Bioenerg 1817:209–217CrossRefGoogle Scholar
  64. Wang Y, Li X (2012) Health Risk of Platinum Group Elements from Automobile Catalysts. Procedia Eng 45:1004–1009CrossRefGoogle Scholar
  65. Weber G, Messerschmidt J, von Bohlen A, Kastenholz B, Günther K (2004) Improved separation of palladium species in biological matrices by using a combination of gel permeation chromatography and isotachophoresis. Electrophoresis 25:1758–1764CrossRefGoogle Scholar
  66. Xiong Z-T, Peng Y-H (2001) Response of Pollen Germination and Tube Growth to Cadmium with Special Reference to Low Concentration Exposure. Ecotoxicol Environ Saf 48:51–55CrossRefGoogle Scholar
  67. Zereini F, Alt F (1999) Antropogenic Platinum-Group Element Emissions. Their impact on Man and Environrnent. Springer, BerlinGoogle Scholar
  68. Zereini F, Wiseman C, Püttmann W (2006) Changes in Palladium, Platinum, and Rhodium Concentrations, and Their Spatial Distribution in Soils Along a Major Highway in Germany from 1994 to 2004. Environ Sci Technol 41:451–456CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Matteo Ronchini
    • 2
  • Laura Cherchi
    • 2
  • Simone Cantamessa
    • 3
  • Marco Lanfranchi
    • 1
  • Alberto Vianelli
    • 2
  • Paolo Gerola
    • 2
  • Graziella Berta
    • 3
  • Alessandro Fumagalli
    • 1
  1. 1.Dipartimento di Scienze Teoriche e Applicate and Centro Grandi Attrezzature per la Ricerca BiomedicaUniversità degli Studi dell’InsubriaVareseItaly
  2. 2.Dipartimento di Scienze Teoriche e ApplicateUniversità degli Studi dell’InsubriaVareseItaly
  3. 3.Dipartimento di Scienze e Innovazione TecnologicaUniversità degli Studi del Piemonte OrientaleAlessandriaItaly

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