Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Changes in physicochemical characteristics of a serpentine soil and in root architecture of a hyperaccumulating plant cropped with a legume

  • 315 Accesses

  • 4 Citations



Agromining is a new technology that establishes agricultural systems on ultramafic soils in order to produce valuable metal compounds such as nickel (Ni), with the final aim of restoring a soil’s agricultural functions. But ultramafic soils are characterized by low fertility levels, and this can limit yields of hyperaccumulators and metal phytoextraction. The objectives of the present work were to test if the association of a hyperaccumulating plant (Alyssum murale) and a Fabaceae (Vicia sativa var. Prontivesa) could induce changes in physicochemical characteristics of a serpentine soil and in root architecture of a hyperaccumulating plant then lead to efficient agromining practices through soil quality improvement.

Materials and methods

Based on standard agricultural systems, consisting in the association of legumes and another crop such as wheat or rape, a 3-month rhizobox experiment was carried out to study the effect of the co-cropping (Co) or rotation (Ro) of a hyperaccumulating plant (A. murale) with a legume (Vicia sativa) and incorporating legume biomass to soil, in comparison with mineral fertilization (FMo), on the structure and physicochemical properties of an ultramafic soil and on root architecture.

Results and discussion

All parameters measured (biomass, C and N contents, and Ni taken up) on A. murale conducted in Co showed the highest values followed by FMo and Ro (Co > FMo > Ro), except for root Ni yield for which Ro was better than FMo. The rhizosphere soil of A. murale in co-cropping had larger soil particles size and better aggregate stability than other treatments. Using geostatistics, co-cropped Alyssum showed a greater root surface area spatial distribution. Moreover, co-cropping and rotation induced lower soil diethylene triamine pentaacetic acid-extractable Ni concentrations than other treatments, but higher pH values. A. murale co-cropped with a legume showed a higher biomass production, improved soil physical characteristics, and enhanced Ni phytoextraction.


Consequently, legume introduction in Ni-agromining systems could be an innovative strategy to reduce chemical inputs and to improve soil functions.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7


  1. Abou Shanab RI, Delorme TA, Angle JS, Chaney RL, Ghane K, Moawad H, Ghozlan HA (2003) Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int J Phytoremediat 5(4):367–379.

  2. Akhtar M, Yaqub M, Iqbal Z, Ashraf MY, Akhter J, Hussain F (2010) Improvement in yield and nutrient uptake by co-cropping of wheat and chickpea. Pakistan J Bot 42:4043–4049

  3. Alamgir M, McNeill A, Tang C, Marschner P (2012) Changes in soil P pools during legume residue decomposition. Soil Biol Biochem 49:70–77.

  4. Álvarez-López V, Prieto-Fernández Á, Cabello-Conejo MI, Kidd P (2016) Organic amendments for improving biomass production and metal yield of Ni-hyperaccumulating plants. Sci Total Environ 548-549:370–379.

  5. Amezketa E (1999) Soil aggregate stability: a review. J Sustain Agric 14(2-3):83–151.

  6. Bani A, Echevarria G, Sulçe S, Morel JL, Mullai A (2007) In-situ phytoextraction of Ni by a native population of Alyssum murale on an ultramafic site (Albania). Plant Soil 293(1-2):79–89.

  7. Bani A, Echevarria G, Sulçe S, Morel JL (2015a) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediat 17(2):117–127.

  8. Bani A, Echevarria G, Zhang X, Benizri E, Laubie B, Morel JL, Simonnot M-O (2015b) The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77

  9. Bani A, Imeri A, Echevarria G, Pavlova D, Reeves RD, Morel JL, Sulçe S (2013) Nickel hyperaccumulation in the serpentine flora of Albania. Fresenius Environ Bull 22:1792–1801

  10. Barbaroux R, Mercier G, Blais JF, Morel JL, Simonnot MO (2011) A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum murale. Sep Purif Technol 83:57–65.

  11. Béchet B, Carré F, Florentin L, Leyval C, Montanarella L, Morel JL, Raimbault G, Rodriguez F, Rossignol JP, Schwartz C (2009) Caractéristiques et fonctionnement des sols urbains. In: “Sous les pavés, la terre. Connaître et gérer les sols urbains”. Cheverry C, Gascuel CM (eds),  Omniscience, Montreuil, pp 45–77

  12. Bédoussac L, Justes E (2010) Dynamic analysis of competition and complementarity for light and N use to understand the yield and the protein content of a durum wheat-winter pea intercrop. Plant Soil 330(1-2):37–54.

  13. Bohren CF, Huffman DR (2008) Absorption and scattering of light by small particles. John Wiley & Sons, New York 544 pp

  14. Bot A, Benites J (2005) The importance of soil organic matter key to drought-resistant soil and sustained crop production. FAO Soils Bulletin, Rome 80 pp

  15. Breitenbeck GA, Hutchinson RL, Boquet DJ (1994) Nitrogen status of cotton following winter cover crops. In: Proceedings—Beltwide Cotton Conferences, San Diego, CA, USA. National Cotton Council, Memphis, pp 1505–1507

  16. Broadhurst CL, Chaney R (2016) Growth and metal accumulation of an Alyssum murale nickel hyperaccumulator ecotype co-cropped with Alyssum montanum and perennial ryegrass in serpentine soil. Front Plant Sci 7:451

  17. Brown SL, Chaney RL, Angle JS, Baker AJM (1994) Phytoremediation potential of Thlaspi caerulescens and bladder campion for zinc- and cadmium-contaminated soil. J Environ Qual 23(6):1151–1157.

  18. Brown RB (1998) Soil texture, soil and water science. Fact Sheet SL-29, Department, Institute of Food and Agricultural Science, University of Florida

  19. Chaney RL, Chen KY, Li YM, 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(1-2):131–140.

  20. Chu J, Zhang T, Chang W, Zhang D, Zulfiqar S, Fu A, Hao Y (2016) Impacts of cropping systems on aggregates associated organic carbon and nitrogen in a semiarid highland agroecosystem. PLoS One 11(10):e0165018.

  21. Coleman DC, Crossley DA, Hendrix PF (2004) Fundamentals of soil ecology, 2nd edn. Elsevier Academic Press, Amsterdam–Boston 386 pp

  22. Constantin J, Beaudoin N, Launay M, Duval J, Mary B (2012) Long-term nitrogen dynamics in various catch crop scenarios: test and simulations with STICS model in a temperate climate. Agric Ecosyst Environ 147:36–46.

  23. Coppens F, Garnier P, Findeling A, Merckx R, Recous S (2007) Decomposition of mulched versus incorporated crop residues: modelling with PASTIS clarifies interactions between residue quality and location. Soil Biol Biochem 39(9):2339–2350.

  24. Corre-Hellou G, Brisson N, Launay M, Fustec J, Crozat Y (2007) Effect of root depth penetration on soil nitrogen competitive interactions and dry matter production in pea–barley intercrops given different soil nitrogen supplies. Field Crops Res 103(1):76–85.

  25. Corre-Hellou G, Fustec J, Crozat Y (2006) Interspecific competition for soil N and its interaction with N2 fixation, leaf expansion and crop growth in pea-barley intercrops. Plant Soil 282(1-2):195–208.

  26. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

  27. Echevarria G, Morel JL, Fardeau JC, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. J Environ Qual 27(5):1064–1070.

  28. Fornara DA, Tilman D (2008) Plant functional composition influences rates of soil carbon and nitrogen accumulation. J Ecol 96(2):314–322.

  29. Fujita K, Ofosu-Budu KG, Ogata S (1992) Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant Soil 141(1-2):155–175.

  30. Gonzalez-Prieto SJ, Carballas M, Carballas T (1991) Mineralization of a nitrogen-bearing organic sustrate model 14C, 15N-glycine in two acid soils. Soil Biol Biochem 23(1):53–63.

  31. Görres JH, Dichiaro MJ, Lyons JB, Amador JA (1998) Spatial and temporal patterns of soil biological activity in a forest and an old field. Soil Biol Biochem 30(2):219–230.

  32. Gregorich EG, Drury CF, Baldock JA (2001) Changes in soil carbon under long-term maize in monoculture and legume-based rotation. Can J Soil Sci 81(1):21–31.

  33. Harker KN, O'Donovan JT, Turkington TK, Blackshaw RE, Lupwayi NZ, Smith EG, Klein-Gebbinck H, Dosdall LM, Hall LM, Willenborg CJ, Kutcher HR, Malhi SS, Vera CL, Gan Y, Lafond GP, May WE, Grant CA, McLaren DL (2012) High-yield no-till canola production on the Canadian prairies. Can J Plant Sci 92(2):221–233.

  34. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156(3):1078–1086.

  35. Jamont M, Piva G, Fustec J (2013) Sharing N resources in the early growth of rapeseed intercropped with faba bean: does N transfer matter? Plant Soil 371(1-2):641–653.

  36. Jiang CA, QT W, Goudon R, Echevarria G, Morel JL (2015) Biomass and metal yield of co-cropped Alyssum murale and Lupinus albus. Aust J Bot 63:159–166

  37. Justes E, Bedoussac L, Corre-Hellou G, Fustec J, Hinsinger P, Journet E-P, Louarn G, Naudin C, Pelzer E (2014) La complémentarité pour l’acquisition des ressources abiotiques dans les associations végétales : quels processus déterminent leur fonctionnement ? Innovations Agronomiques 40:1–24

  38. Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33(6):2090–2102.

  39. Kuo S, Sainju UM, Jellum EJ (1997) Winter cover crop effects on soil organic carbon and carbohydrate in soil. Soil Sci Soc Am J 61(1):145–152.

  40. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42(9):1363–1371.

  41. Li L, Li SM, Sun JH, Zhou LL, Bao XG (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci U S A 104(27):11192–11196.

  42. Li L, Sun J, Zhang F, Guo T, Bao X, Smith FA, Smith SE (2006) Root distribution and interactions between intercropped species. Oecologia 147(2):280–290.

  43. Li L, Sun J, Zhang F, Li X, Rengel Z, Yang S (2001) Wheat/maize or wheat/soybean strip intercropping: II. Recovery or compensation of maize and soybean after wheat harvesting. Field Crops Res 71(3):173–181.

  44. Li NY, Li ZA, Zhuang P, Zhou B, McBride M (2009) Cadmium uptake from soil by maize with intercrops. Water Air Soil Pollut 199(1-4):45–56.

  45. Li YM, Chaney RL, Brewer EP, Angle JS, Nelkin J (2003) Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel contaminated soils. Environ Sci Technol 37(7):1463–1468.

  46. Liu L, Hu LL, Tang JJ, Li YF, Zhang Q, Chen X (2012a) Food safety assessment of planting patterns of four vegetable-type crops grown in soil contaminated by electronic waste activities. J Environ Manag 93(1):22–30.

  47. Lindsay WL, Norvell WA (1978) Development of DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42(3):421–428.

  48. Liu L, Zhang Q, Hu L, Tang J, Xu L, Yang X, Yong JWH, Chen X (2012b) Legumes can increase cadmium contamination in neighboring crops. PLoS One 7(8):e42944.

  49. Lizarazo CI, Yli-Halla M, Stoddard FL (2015) Pre-crop effects on the nutrient composition and utilization efficiency of faba bean (Vicia faba L.) and narrow-leafed lupin (Lupinus angustifolius L.) Nutr Cycl Agroecosys 103(3):311–327.

  50. Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75(6):719–725.

  51. McVay KA, Radcliffe DE, Hargrove WL (1989) Winter legume effects on soil properties and nitrogen fertiliser requirement. Soil Sci Soc Am J 53(6):1856–1862.

  52. Michael G, Schumacher H, Marschner H (1965) Aufnahme von Ammonium- und Nitratstickstoff aus markiertem ammoniumnitrat und deren verteilung in der pflanze. J Plant Nutr Soil Sc 110:225–238

  53. Mie G (1908) Contributions to the optics of turbid media, particularly of colloidal metal solutions. Annals of Physics, Leipzig 25:377–445

  54. Minasny B, McBratney AB (2001) The Australian soil texture boomerang: a comparison of the Australian and USDA/FAO soil particlesize classification systems. Aust J Soil Res 39(6):1443–1451.

  55. Morel JL (2013) Using plants to “micro-mine” metals. In:

  56. Ofosu-Budu KG, Noumura K, Fujita K (1995) Nitrogen fixation, N transfer and biomass production of soybean cv. bragg or its super-nodulating NTS-1007 and sorghum mixing-cropping at two rates of N fertilizer. Soil Biol Biochem 27(3):311–317.

  57. Paulo J, Ribeiro JR, Diggle PJ (2016) geoR: analysis of geostatistical data. R package version 1.7–5.2.

  58. Pelzer E, Bazot M, Makowski D, Corre-Hellou G, Naudin C, Al Rifaï M, Baranger E, Bedoussac L, Biarnès V, Boucheny P, Carrouée B, Dorvillez D, Foissy D, Gaillard B, Guichard L, Mansard M-C, Omon B, Prieur L, Yvergniaux M, Justes E, Jeuffroy MH (2012) Pea–wheat intercrops in low-input conditions combine high economic performances and low environmental impacts. Eur J Agron 40:39–53.

  59. Peters CA, Chaney RL, Angle JS, Roseberg RJ (2000) Effect of the pH of pH-buffered nutrient solutions on Ni accumulation by hyperaccumulator species p. 50. In 2000 Agronomy abstracts. ASA, Madison, WI

  60. Redin M, Recous S, Aita C, Dietrich G, Skolaude AC, Ludke WH, Schmatz R, Giacomini SJ (2014) How the chemical composition and heterogeneity of crop residue mixtures decomposing at the soil surface affects C and N mineralization. Soil Biol Biochem 78:65–75.

  61. Rengel Z, Damon PM (2008) Crops and genotypes differ in efficiency of potassium uptake and use. Physiol Plant 133(4):624–636.

  62. Rochester I, Peoples M (2005) Growing vetches (Vicia villosa Roth) in irrigated cotton systems: inputs of fixed N, N fertiliser savings and cotton productivity. Plant Soil 271(1-2):251–264.

  63. Rochester IJ, Peoples MB, Hulugalle NR, Gault RR, Constable GA (2001) Using legumes to enhance nitrogen fertility and improve soil condition in cotton cropping systems. Field Crops Res 70(1):27–41.

  64. Saad R, Kobaissi A, Robin C, Echevarria G, Benizri E (2016) Nitrogen fixation and growth of Lens culinaris as affected by nickel availability: a pre-requisite for optimization of agromining. Environ Exp Bot 131:1–9.

  65. Schröder D, Köpke U (2012) Faba bean (Vicia faba L.) intercropped with oil crops—a strategy to enhance rooting density and to optimize nitrogen use and grain production? Field Crops Res 135:74–81.

  66. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60(100):182–194.

  67. Shallari S, Schwartz C, Hasko A, Morel JL (1998) Heavy metals in soils and plants of serpentine and industrial sites of Albania. Sci Total Environ 209(2-3):133–142.

  68. Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale (Waldst. & Kit.) S Afr J Sci 97:568–570

  69. Sheoran V, Sheoran AS, Poonia P (2016) Factors affecting phytoextraction: a review. Pedosphere 26(2):148–166.

  70. Sutton MA, Oenema O, Erisman JW, Leip A, van Grinsven H, Winiwarter W (2011) Too much of a good thing. Nature 472(7342):159–162.

  71. Stevenson FC, van Kessel C (1996) The nitrogen and non-nitrogen rotation benefits of pea to succeeding crops. Can J Plant Sci 76(4):735–745.

  72. van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot MO, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol 49(8):4773–4780.

  73. Wang K, Huang H, Zhu Z, Li T, He Z, Yang X, Alva A (2013) Phytoextraction of metals and rhizoremediation of PAHs in co-contaminated soil by co-planting of Sedum alfredii with ryegrass (Lolium perenne) or castor (Ricinus communis). Int J Phytoremed 15(3):283–298.

  74. Wei SH, Zhou QX (2004) Identification of weed species with hyperaccumulative characteristics of heavy metals. Prog Nat Sci 14(6):495–503.

  75. Yan E, Schubert S, Mengel K (1996) Soil pH increase due to biological decarboxylation of organic anions. Soil Biol Biochem 28(4-5):617–624.

  76. Zhang CC, Postma JA, York LM, Lynch JP (2014a) Root foraging elicits niche complementarity-dependent yield advantage in the ancient ‘three sisters’ (maize/bean/squash) polyculture. Ann Bot-London 114(8):1719–1733.

  77. Zhang X, Houzelot V, Bani A, Morel JL, Echevarria G, Simonnot MO (2014b) Selection and combustion of Ni-hyperaccumulators for the phytomining process. Int J Phytoremediat 16(10):1058–1072.

  78. Zhao J, Zeng Z, He X, Chen H, Wang K (2015) Effects of monoculture and mixed culture of grass and legume forage species on soil microbial community structure under different levels of nitrogen fertilization. Eur J Soil Biol 68:61–68.

  79. Zou XL (2015) Phytoextraction of heavy metals from contaminated soil by co-cropping Solanum nigrum L. with ryegrass associated with endophytic bacterium. Sep Sci Technol 50(12):1806–1813.

Download references


We would like to acknowledge the technical team of “Laboratoire Sols et Environnement” especially Mr. Lucas Charrois, Mr. Romain Goudon, Mr. Stéphane Colin, and Mr. Alain Rakoto for their help and support. We are thankful for the technical assistance of the joint research unit INRA of Champenoux, UMR 1092 AgroParisTech INRA Laboratoire d’Etude des ressources FOrêt Bois “LERFoB” Plate-forme Technique Xylosciences especially Mrs. Charline Freyburger for the X-ray analysis. We are thankful for the technical assistance of the joint research unit Consejo Superior de Investigaciones Científicas (CSIC, Santiago de Compostella, Spain) especially the “Soil Microbiology Group” represented by Dr. Petra Kidd. We would like to thank also Dr. Ali Kanso for his support in the laser diffraction granulometry analyses. Finally, we are thankful to the Association of Specialization and Scientific Guidance (ASSG, Lebanon) for funding the PhD scholarship of Ramez Saad.


This work was supported by the French National Research Agency through the national “Investissements d’avenir” program, reference ANR-10-LABX-21-LABEX RESSOURCES21 and through the ANR-14-CE04-0005 project “Agromine”.

Author information

Correspondence to Emile Benizri.

Additional information

Responsible editor: Dong-Mei Zhou

Electronic supplementary material


(DOCX 17 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Saad, R.F., Kobaissi, A., Amiaud, B. et al. Changes in physicochemical characteristics of a serpentine soil and in root architecture of a hyperaccumulating plant cropped with a legume. J Soils Sediments 18, 1994–2007 (2018).

Download citation


  • Alyssum murale
  • Plant association
  • Co-cropping
  • Hyperaccumulating plant
  • Legume
  • Rotation
  • Serpentine soil
  • Soil physicochemical properties