Journal of Plant Research

, Volume 129, Issue 2, pp 251–262 | Cite as

Lead tolerance mechanism in Conyza canadensis: subcellular distribution, ultrastructure, antioxidative defense system, and phytochelatins

  • Ying Li
  • Chuifan Zhou
  • Meiying Huang
  • Jiewen Luo
  • Xiaolong Hou
  • Pengfei Wu
  • Xiangqing MaEmail author
Regular Paper


We used hydroponic experiments to examine the effects of different concentrations of lead (Pb) on the performance of the Pb-tolerable plant Conyza canadensis. In these experiments, most of the Pb was accumulated in the roots; there was very little Pb accumulated in stems and leaves. C. canadensis is able to take up significant amounts of Pb whilst greatly restricting its transportation to specific parts of the aboveground biomass. High Pb concentrations inhibited plant growth, increased membrane permeability, elevated antioxidant enzyme activity in roots, and caused a significant increase in root H2O2 and malondialdehyde content. Analysis of Pb content at the subcellular level showed that most Pb was associated with the cell wall fraction, followed by the nucleus-rich fraction, and with a minority present in the mitochondrial and soluble fractions. Furthermore, transmission electron microscopy and energy dispersive X-ray analysis of root cells revealed that the cell wall and intercellular space in C. canadensis roots are the main locations of Pb accumulation. Additionally, high Pb concentrations adversely affected the cellular structure of C. canadensis roots. The increased enzyme activity suggests that the antioxidant system may play an important role in eliminating or alleviating Pb toxicity in C. canadensis roots. However, the levels of non-protein sulfhydryl compounds, glutathione, and phytochelatin did not significantly change in either the roots or leaves under Pb-contaminated treatments. Our results provide strong evidence that cell walls restrict Pb uptake into the root and act as an important barrier protecting root cells, while demonstrating that antioxidant enzyme levels are correlated with Pb exposure. These findings demonstrate the roles played by these detoxification mechanisms in supporting Pb tolerance in C. canadensis.


Lead Conyza canadensis Subcellular distribution Ultrastructure Antioxidative defense system Phytochelatins 



This work was supported by Research project of forestry public welfare industry of the State Forestry Bureau of China (201304303), Foundation for Cultivation plan of Distinguished Young Scholars of Fujian Province, National Natural Science Foundation of China (31400465, 41401364), and Major projects of agricultural science and technology cooperation in Agricultural University (2013N5002).


  1. Aebi H (1984) Methods in enzymology. Elsevier, London, pp 121–126Google Scholar
  2. Andersen HR, Nielsen JB, Nielsen F, Grandjean P (1997) Antioxidative enzyme activities in human erythrocytes. Clin Chem 43:562–568PubMedGoogle Scholar
  3. Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradère P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71:2187–2192CrossRefPubMedGoogle Scholar
  4. Basile A, Giordano S, Cafiero G, Spagnuolo V, Castaldo-Cobianchi R (1994) Tissue and cell localization of experimentally-supplied lead in Funaria hygrometrica Hedw. using X-ray SEM and TEM microanalysis. J Bryol 18:69–81CrossRefGoogle Scholar
  5. Bibi M, Hussain M (2005) Effect of copper and lead on photosynthesis and plant pigments in black gram [Vigna mungo (L.) Hepper]. B Environ Contam Tox 74:1126–1133CrossRefGoogle Scholar
  6. Cheng H, Hu Y (2010) Lead (Pb) isotopic fingerprinting and its applications in lead pollution studies in China: a review. Environ Pollut 158:1134–1146CrossRefPubMedGoogle Scholar
  7. De Vos CR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98:853–858PubMedCentralCrossRefPubMedGoogle Scholar
  8. Ebbs S, Lau I, Ahner B, Kochian L (2002) Phytochelatin synthesis is not responsible for Cd tolerance in the Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214:635–640CrossRefPubMedGoogle Scholar
  9. Fu X, Dou C, Chen Y, Chen X, Shi J, Yu M, Xu J (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J Hazard Mater 186:103–107CrossRefPubMedGoogle Scholar
  10. Ghaedi M, Ahmadi F, Shokrollahi A (2007) Simultaneous preconcentration and determination of copper, nickel, cobalt and lead ions content by flame atomic absorption spectrometry. J Hazard Mater 142:272–278CrossRefPubMedGoogle Scholar
  11. Gupta DK, Nicoloso FT, Schetinger M, Rossato LV, Pereira LB, Castro GY, Srivastava S, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172:479–484CrossRefPubMedGoogle Scholar
  12. Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444CrossRefPubMedGoogle Scholar
  13. Huang JW, Chen J, Berti WR, Cunningham SD (1997) Phytoremediation of lead-contaminated soils: role of synthetic chelates in lead phytoextraction. Environ Sci Technol 31:800–805CrossRefGoogle Scholar
  14. Huang H, Gupta DK, Tian S, Yang X, Li T (2012) Lead tolerance and physiological adaptation mechanism in roots of accumulating and non-accumulating ecotypes of Sedum alfredii. Environ Sci Pollut R 19:1640–1651CrossRefGoogle Scholar
  15. Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926CrossRefPubMedGoogle Scholar
  16. Kastori R, Plesničar M, Sakač Z, Panković D, Arsenijević Maksimović I (1998) Effect of excess lead on sunflower growth and photosynthesis. J Plant Nutr 21:75–85CrossRefGoogle Scholar
  17. Kopittke PM, Asher CJ, Blamey FPC, Auchterlonie GJ, Guo YN, Menzies NW (2008) Localization and chemical speciation of Pb in roots of signal grass (Brachiaria decumbens) and Rhodes grass (Chloris gayana). Environ Sci Technol 42:4595–4599CrossRefPubMedGoogle Scholar
  18. Kosobrukhov A, Knyazeva I, Mudrik V (2004) Plantago major plants responses to increase content of lead in soil: growth and photosynthesis. Plant Growth Regul 42:145–151CrossRefGoogle Scholar
  19. Kumar A, Prasad M, Sytar O (2012) Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere 89:1056–1065CrossRefPubMedGoogle Scholar
  20. Li X, Zhang L, Li Y, Ma L, Bu N, Ma C (2012) Changes in photosynthesis, antioxidant enzymes and lipid peroxidation in soybean seedlings exposed to UV-B radiation and/or Cd. Plant Soil 352:377–387CrossRefGoogle Scholar
  21. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–VIS spectroscopy. Current protocols in food analytical chemistry. Rev Environ Contam T 26:11–17Google Scholar
  22. Liu J, Mei C, Cai H, Wang M (2015) Relationships between subcellular distribution and translocation and grain accumulation of Pb in different rice cultivars. Water Air Soil Poll 226:1–9Google Scholar
  23. Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398CrossRefGoogle Scholar
  24. Małecka A, Piechalak A, Morkunas I, Tomaszewska B (2008) Accumulation of lead in root cells of Pisum sativum. Acta Physiol Plant 30:629–637CrossRefGoogle Scholar
  25. Meyers DE, Auchterlonie GJ, Webb RI, Wood B (2008) Uptake and localisation of lead in the root system of Brassica juncea. Environ Pollut 153:323–332CrossRefPubMedGoogle Scholar
  26. Mingorance MD, Leidi EO, Valdés B, Oliva SR (2012) Evaluation of lead toxicity in Erica andevalensis as an alternative species for revegetation of contaminated soils. Int J Phytoremediat 14:174–185CrossRefGoogle Scholar
  27. Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039CrossRefPubMedGoogle Scholar
  28. Nishizono H, Ichikawa H, Suziki S, Ishii F (1987) The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant Soil 101:15–20CrossRefGoogle Scholar
  29. Patra J, Lenka M, Panda BB (1994) Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc. New Phytol 128:165–171CrossRefGoogle Scholar
  30. Pawlik-Skowrońska B (2002) Correlations between toxic Pb effects and production of Pb-induced thiol peptides in the microalga Stichococcus bacillaris. Environ Pollut 119:119–127CrossRefPubMedGoogle Scholar
  31. Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam 213:113–136 (Springer) Google Scholar
  32. Qiao X, Zheng Z, Zhang L, Wang J, Shi G, Xu X (2015) Lead tolerance mechanism in sterilized seedlings of Potamogeton crispus L.: subcellular distribution, polyamines and proline. Chemosphere 120:179–187CrossRefPubMedGoogle Scholar
  33. Salazar MJ, Pignata ML (2014) Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation. J Geochem Explor 137:29–36CrossRefGoogle Scholar
  34. Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Safe 74:78–84CrossRefGoogle Scholar
  35. Sharma P, Dubey RS (2005) Lead toxicity in plants. B J Plant Physiol 17:35–52CrossRefGoogle Scholar
  36. Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad M (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999CrossRefGoogle Scholar
  37. Tamura H, Honda M, Sato T, Kamachi H (2005) Pb hyperaccumulation and tolerance in common buckwheat (Fagopyrum esculentum Moench). J Plant Res 118:355–359CrossRefPubMedGoogle Scholar
  38. Tian S, Lu L, Yang X, Webb SM, Du Y, Brown PH (2010) Spatial imaging and speciation of lead in the accumulator plant Sedum alfredii by microscopically focused synchrotron X-ray investigation. Environ Sci Technol 44:5920–5926CrossRefPubMedGoogle Scholar
  39. Tian S, Lu L, Yang X, Huang H, Brown P, Labavitch J, He Z (2011) The impact of EDTA on lead distribution and speciation in the accumulator Sedum alfredii by synchrotron X-ray investigation. Environ Pollut. 159:782–788CrossRefPubMedGoogle Scholar
  40. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  41. Wang S, Zhang J (2006) Blood lead levels in children, China. Environ Res 101:412–418CrossRefPubMedGoogle Scholar
  42. Wang X, Liu Y, Zeng G, Chai L, Song X, Min Z, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Gaud. Environ Exp Bot 62:389–395CrossRefGoogle Scholar
  43. Wu Z, McGrouther K, Chen D, Wu W, Wang H (2013) Subcellular distribution of metals within Brassica chinensis L. in response to elevated lead and chromium stress. J Agr Food Chem 61:4715–4722CrossRefGoogle Scholar
  44. Zhou XY, Qiu RL, Li QF, Shi N, Zhang T, Hu PJ, Ying RR (2008) Effects of zinc on distribution and chemical form of lead in Potentilla griffithii var. velutina. Acta Sci Circumstantiae 28:2064–2071Google Scholar
  45. Zhou CF, Wang YJ, Sun RJ, Liu C, Fan GP, Qin WX, Li CC, Zhou DM (2014) Inhibition effect of glyphosate on the acute and subacute toxicity of cadmium to earthworm Eisenia fetida. Environ Toxicol Chem 33:2351–2357CrossRefPubMedGoogle Scholar
  46. Zhou CF, Zhang K, Lin JW, Li Y, Chen NL, Zou XH, Hou XL, Ma XQ (2015) Physiological responses and tolerance mechanisms to cadmium in Conyza canadensis. Int J Phytoremediation 17:280–289CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2015

Authors and Affiliations

  • Ying Li
    • 1
  • Chuifan Zhou
    • 1
  • Meiying Huang
    • 1
  • Jiewen Luo
    • 1
  • Xiaolong Hou
    • 1
  • Pengfei Wu
    • 1
  • Xiangqing Ma
    • 1
    Email author
  1. 1.College of ForestryFujian Agriculture and Forestry UniversityFuzhouChina

Personalised recommendations