Environmental Science and Pollution Research

, Volume 26, Issue 1, pp 381–391 | Cite as

Lead uptake by the symbiotic Daucus carota L.–Glomus intraradices system and its effect on the morphology of extra- and intraradical fungal microstructures

  • Carlos Juan Alvarado-López
  • Nabanita Dasgupta-Schubert
  • Jorge Enrique Ambriz
  • Juan Carlos Arteaga-Velazquez
  • Javier A. Villegas
Research Article


This work examines the strategies adopted by an arbuscular mycorrhizal symbiotic system to ameliorate environmental Pb stress by examining the concentrations of P, Fe, and Pb in the fungal microstructures and the host’s root. In vitro cultures of Ri-T DNA-transformed carrot (Daucus carota L.) roots were inoculated with Glomus intraradices and treated with Pb(NO3)2 solution and the extraradical spores and mycelia (S/M) and the root with the vesicles, mycelia, and root cells were subsequently analyzed by polarized energy dispersive x-ray fluorescence (PEDXRF) spectrometry. Upon Pb treatment, within the root, the percentages of mycorrhizal colonization, the vesicles, and mycelia increased as well as the areas of the vesicles and the (extraradical) spores, although the number of spores and arbuscules decreased. The S/M and the mycorrhizal root showed enhanced concentrations of Pb, Fe, and P. These were particularly marked for Fe in the Pb-treated cultures. This indicates a synergistic relationship between the arbuscular mycorrhizal fungus and the host that confers a higher Pb tolerance to the latter by the induction of higher Fe absorption in the host. The intraradical vesicle, mycelia, and arbuscule numbers are interpreted as a “tactic to divert” the intraradical Pb traffic away from the root cells to the higher affinity cell walls of the arbuscular mycorrhizal fungi (AMF) microstructures in the apoplast. The results of this work show that the symbiosis between the AMF G. intraradices and the host plant D. carota distinctly improves the latter’s Pb tolerance, and imply that the appropriate metal tolerant host-AMF combinations could be employed in process designs for the phytoremediation of Pb.


Pb Arbuscular mycorrhizal fungi Phytoremediation Glomus intraradices Daucus carota Symbiosis 



The authors thank Dr. S.E. Borjas of the Laboratorio de Radiación, Instituto de Física y Matemáticas, and Biol. L. Carreto of the Instituto de Investigaciones Químico-Biológicas of the Universidad Michoacana de San Nicolás de Hidalgo, Morelia, México, for technical help. CJAL thanks CONACyT of Mexico for his doctoral fellowship (no. 168355).


  1. Abuhani W, Dasgupta-Schubert N andVillaseñor Cendejas L (2014). Characterizing fundamental parameter-based analysis for soil–ceramic matrices in polarized energy-dispersive X-ray fluorescence (PEDXRF) spectrometry. Powder Diffraction, 29(2): 159-169.Google Scholar
  2. Alvarado CJ, Dasgupta-Schubert N, Ambriz EA, Sanchez-Yañez JM, Villegas HJ (2011) Hongos micrrizicos arbusculares y la fitoremediación del plomo. Rev Int Contam Ambient 27(4):357–364Google Scholar
  3. Alvarado CJ, Abuhani WA, Whelan T, Castillo OS, Villaseñor LM, Borjas SE, Landsberger S, Bribiesca SL, Alexander S, Dasgupta-Schubert N (2013) Comparative analysis of lead and copper in metal-accumulating plants with and without mycorrhizae. Commun Soil Sci Plant Anal 44(22):3293–3309. CrossRefGoogle Scholar
  4. Andrade SAL, Abreu CA, De Abreu MF, Silveira PD (2004) Influence of lead additions on arbuscular mycorrhiza and Rhizobium symbioses under soybean plants. Appl Soil Ecol 26(2):123–131. CrossRefGoogle Scholar
  5. Arriagada CA, Herrera MA, Ocampo JA (2005) Contribution of arbuscular mycorrhizal and saprobe fungi to the tolerance of Eucalyptus globulus to Pb. Water Air Soil Pollut 166(1–4):31–47CrossRefGoogle Scholar
  6. Bécard G, Fortin JA (1988). Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist 108 (2):211-218Google Scholar
  7. Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87(1):63–67CrossRefGoogle Scholar
  8. Briat JF, Lobreaux S (1997) Iron transport and storage in plants. Trends Plant Sci 2(5):187–193CrossRefGoogle Scholar
  9. Castillo OS, Dasgupta-Schubert N, Alvarado CJ, Zaragoza EM, Villegas HJ (2011) The effect of the symbiosis between Tagetes erecta L. (marigold) and Glomus intraradices in the uptake of Copper (II) and its implications for phytoremediation. New Biotechnol 29(1):156–164. CrossRefGoogle Scholar
  10. Dasgupta-Schubert N, Alexander S, Sommer L, Alfaro Cueva Villanueva R, Mendez López ME, Persans MW (2007) The light quanta physiological response of Brassica juncea to Ni(II) stress. Eng Life Sci 7(3):259–267. CrossRefGoogle Scholar
  11. Dasgupta-Schubert N, Barrera MG, Alvarado CJ, Castillo OS, Zaragoza EM, Alexander S, Landsberger S, Robinson S (2011) The uptake of copper by aldama dentata: ecophysiological response, its modeling, and the implication for phytoremediation. Water Air Soil Pollut 220(1–4):37–55. CrossRefGoogle Scholar
  12. Declerck S, Strullu DG, Fortin A (eds) (2005) In vitro culture of mycorrhizas. Springer Verlag, BerlinGoogle Scholar
  13. Dekock PC (1981) Iron nutrition under conditions of stress. J Plant Nutr 3(1–4):513–521CrossRefGoogle Scholar
  14. Del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65(2):718–723Google Scholar
  15. Dong Y, Ma LQ, Rhue RD (1999) Relation of enhanced Pb solubility to Fe partitioning in soils. Environ Pollut 110(3):515–522CrossRefGoogle Scholar
  16. Fahr M, Laplaze L, Bendaou N, Hocher V, El Mzibri M, Bogusz D, Smouni A (2013) Effect of lead on root growth. Front Plant Sci 4:175. CrossRefGoogle Scholar
  17. Galli UH, Schuepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92(2):364–368CrossRefGoogle Scholar
  18. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. Agron Sustain Dev 30(3):581–599. CrossRefGoogle Scholar
  19. Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soil. Curr Sci 86(4):528–534Google Scholar
  20. Giasson P, Jaouich A, Cayer P, Gagné S, Moutoglis P, Massicotte L (2006) Enhanced phytoremediation: a study of micrrhizoremediation of heavy-metal contaminated soil. Remediation 17(1):97–110. CrossRefGoogle Scholar
  21. Ginn BR, Szymanowski JS, Fein JB (2008) Metal and proton binding onto the roots of Fescue rubra. Chem Geol 253(3–4):130–135. CrossRefGoogle Scholar
  22. Gloag D (1981) Sources of Pb pollution. Br Med J 282(1):41–44CrossRefGoogle Scholar
  23. Goehre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223(6):1115–1122. CrossRefGoogle Scholar
  24. González-Guerrero M, Melville LH, Ferrol N, Lott JNA, Azcón-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extra-radical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54(2):103–110. CrossRefGoogle Scholar
  25. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11. CrossRefGoogle Scholar
  26. Hassan G (2005) Contribution of arbuscular mycorrhizal fungus to red kidney and wheat plants tolerance grown in heavy metal-polluted soil. Afr J Biotechnol 4(4):332Google Scholar
  27. Huang JW, Chen J, Berti WR, Cunningham SD (1997) Phytoremediation of Pb contaminated soils: role of synthetic chelates in Pb phytoextraction. Environ Sci Technol 31(3):800–805CrossRefGoogle Scholar
  28. Joner ER, Briones Gallardo R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226(2):227–234. CrossRefGoogle Scholar
  29. Koide RT, Kabir Z (2002) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol 148(3):511–517. CrossRefGoogle Scholar
  30. Koul M, Kapoor R, Luikham N (2001) Influence of lead in soil on mycorrhizal development and plant growth of Cyamopsis tetragonoloba (Linn.) Taub. Indian J Exp Biol 39(1):459–463Google Scholar
  31. Malcová R, Vosátka M, Gryndler M (2003) Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaries L. Appl Soil Ecol 23(1):55–67. CrossRefGoogle Scholar
  32. Mandel J (1984) The mathematical framework of statistics part. II. In: The statistical analysis of experimental data. Dover Publications, New York, pp 410–420Google Scholar
  33. Manecki M, Bogucka A, Bajda T, Borkiewwicz O (2006) Decrease in Pb bioavailability in soils by addition of phosphate ions. Environ Chem Lett 3(4):178–181. CrossRefGoogle Scholar
  34. Meharg AA, Cairney JWG (2000) Co-evolution of mycorrhizal symbionts and their hosts to metal-contaminated environments. Adv Ecol Res 30:69–112. CrossRefGoogle Scholar
  35. Milne GW (ed) (2005) Gardner's commercially important chemicals: synonyms, trade names, and properties. Wiley Interscience, HobokenGoogle Scholar
  36. Nowak J (2007) Effects of cadmium and lead concentrations and arbuscular mycorrhiza on growth, flowering and heavy metal accumulation in scarlet sage (Salvia splendens sello “Torreador”). Acta Agrobot 60(1):79–83CrossRefGoogle Scholar
  37. Nowak B, Schulin R, Robinson B (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40(17):5225–5232. CrossRefGoogle Scholar
  38. Pawlowska TE, Chavat I (2004) Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Appl Environ Microbiol 70(11):6643–6649. CrossRefGoogle Scholar
  39. Peer WA, Baxter IR, Richards EL, Freeman JL, Murphy AS (2005) Phytoremediation and hyperaccumulator plants. In: Tamás MJ, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification. Springer, Berlin, pp 299–340CrossRefGoogle Scholar
  40. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. CrossRefGoogle Scholar
  41. Poschenrieder C, Barceló J (2004) Water relations in heavy metal stressed plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Springer Verlag, Berlin, pp 249–270CrossRefGoogle Scholar
  42. Schramm R, Heckel J (1998) Fast analysis of traces and major elements with ED (P) XRF using polarized X-rays: TURBOQUANT. J Phys IV 8(PR5):Pr5–Pr335. CrossRefGoogle Scholar
  43. Seregin IV, Pekhov VM, Ivanov VB (2002) Plasmolysis as a tool to reveal Lead localization in the apoplast of root cells. Russ J Plant Physiol 49(2):283–285. CrossRefGoogle Scholar
  44. Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17(1):35–52. CrossRefGoogle Scholar
  45. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New YorkGoogle Scholar
  46. Sudová R, Pavlíková D, Macek T, Vosátka M (2007) The effect of EDDS chelate and inoculation with the arbuscular mycorrhizal fungus Glomus intraradices on the efficacy of lead phytoextraction by two tobacco clones. Appl Soil Ecol 35(1):163–173. CrossRefGoogle Scholar
  47. Turnau K, Kottke I, Oberwinkler F (1993) Element localization in mycorrhizal roots of Pteridium aquilinum (L.) Kuhn collected from experimental plots treated with cadmium dust. New Phytol 123(2):313–324CrossRefGoogle Scholar
  48. Vierheilig H, Coughlan AP, Wyss URS, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64(12):5004–5007Google Scholar
  49. Vogel-Mikuš K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133(2):233–242. CrossRefGoogle Scholar
  50. Vogel-Mikuš K, Pongrac P, Kump P, Nečemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139(2):362–371. CrossRefGoogle Scholar
  51. Wong CC, Wu SC, Kuek C, Khan AG, Wong MH (2007) The role of mycorrhizae associated with vetiver grown in Pb-/Zn-contaminated soils: greenhouse study. Restor Ecol 15(1):60–67. CrossRefGoogle Scholar
  52. Zhang HH, Tang M, Chen H, Zheng CI, Niu ZC (2010) Effect of inoculation with AM fungi on lead uptake, translocation and stress alleviation of Zea mays L. seedlings planting in soil with increasing lead concentrations. Eur J Soil Biol 46(5):306–311. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Catedratico CONACYT, División de Estudios de Posgrado e InvestigaciónInstituto Tecnológico de ConkalConkalMexico
  2. 2.Facultad de Ciencias Físico MatemáticasUniversidad Michoacana de San Nicolás de Hidalgo, Cd. UniversitariaMoreliaMexico
  3. 3.Ingeniería en la Tecnología de la MaderaUniversidad Michoacana de San Nicolás de Hidalgo, Cd. UniversitariaMoreliaMexico
  4. 4.Instituto de Física y MatemáticasUniversidad Michoacana de San Nicolás de Hidalgo, Cd. UniversitariaMoreliaMexico
  5. 5.Instituto de Investigaciones Químico BiológicasUniversidad Michoacana de San Nicolás de Hidalgo, Cd. UniversitariaMoreliaMexico

Personalised recommendations