, Volume 73, Issue 4, pp 299–311 | Cite as

Accumulation and tolerance characteristics of lead in Althaea rosea Cav. and Malva crispa L.

  • Yaping Huang
  • Lihong Zu
  • Meili Zhou
  • Cong Shi
  • Guangshuang Shen
  • Fuchen ShiEmail author
Original Article


Two ornamental plants of Althaea rosea Cav. and Malva crispa L. were exposed to various concentrations of lead (Pb) (0, 50, 100, 200 and 500 mg·kg−1) for 70 days to evaluate the accumulating potential and the tolerance characteristics. The results showed that both plant species grown normally under Pb stress, and A. rosea had a higher tolerance than M. crispa, while M. crispa had a higher ability in Pb accumulation than A. rosea. Besides, lower Pb concentration (50 mg·kg−1) stimulated the shoot biomass in both plant species. Pb accumulation in plants was consistent with the increase of Pb levels, and the main accumulation sites were the roots and the older leaves. In addition, the photosynthetic pigments content and chlorophyll fluorescence parameters were influenced by Pb stress. In such case, both of the plants could improve the activities of antioxidant enzymes of superoxide dismutase (SOD), peroxidase (POD), catalase (CAT) and ascorbate peroxidase (APX), and the contents of the total soluble sugar and soluble protein, which reached the highest value at Pb 100 mg·kg−1, as well as the accumulation of the total thiols (T-SH) and non-protein thiols (NP-SH) to adapt to Pb stress. Thus, it provides the theoretical basis and possibility for ornamental plants of A. rosea and M. crispa in phytoremediation of Pb contaminated areas.


Althaea rosea Malva crispa Lead Physiological characteristics Accumulation ability 



This work was financially supported by The 111 Project B08011, The Basic Work of the Ministry of Science and Technology, China (No. 2011FY110300).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. CrossRefPubMedGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. CrossRefPubMedGoogle Scholar
  3. Bai LY, Zeng XB, Su SM, Duan R, Wang YN, Gao X (2015) Heavy metal accumulation and source analysis in greenhouse soils of Wuwei District, Gansu Province, China. Environ Sci Pollut Res 22(7):5359–5369. CrossRefGoogle Scholar
  4. Balakhnina TI, Nadezhkina ES (2017) Effect of selenium on growth and antioxidant capacity of Triticum aestivum L. during development of lead-induced oxidative stress. Russ J Plant Physiol 64(2):215–223. CrossRefGoogle Scholar
  5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. CrossRefPubMedGoogle Scholar
  6. Burges A, Epelde L, Garbisu C (2015) Impact of repeated single-metal and multi-metal pollution events on soil quality. Chemosphere 120:8–15. CrossRefPubMedGoogle Scholar
  7. Cay S, Uyanik A, Engin MS, Kutbay HG (2015) Effect of EDTA and tannic acid on the removal of cd, Ni, Pb and cu from artificially contaminated soil by Althaea rosea Cavan. Int J Phytoremediat 17(6):568–574. CrossRefGoogle Scholar
  8. Cosio C, Vollenweider P, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.): I. Macrolocalization and phytotoxic effects of cadmium. Environ Exp Bot 58(1–3):64–74. CrossRefGoogle Scholar
  9. Davies CS, Nielsen SS, Nielsen NC (1987) Flavor improvement of soybean preparations by genetic removal of lipoxygenase-2. J Am Oil Chem Soc 64(10):1428–1433. CrossRefGoogle Scholar
  10. Devi SR, Prasad MNV (1998) Copper toxicity in Ceratophyllum demersum L.(Coontail), a free floating macrophyte: response of antioxidant enzymes and antioxidants. Plant Sci 138(2):157–165. CrossRefGoogle Scholar
  11. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32(1):93–101. CrossRefGoogle Scholar
  12. Durmus N, Yesilyurt AM, Pehlivan N, Karaoglu SA (2017) Salt stress resilience potential of a fungal inoculant isolated from tea cultivation area in maize. Biologia 72(6):619–627. CrossRefGoogle Scholar
  13. Dzikiewicz M (2000) Activities in nonpoint pollution control in rural areas of Poland. Ecol Eng 14(4):429–434. CrossRefGoogle Scholar
  14. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77. CrossRefPubMedGoogle Scholar
  15. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta-Gen Subj 990(1):87–92. CrossRefGoogle Scholar
  16. Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120. CrossRefPubMedGoogle Scholar
  17. Gupta DK, Nicoloso FT, Schetinger MRC, Rossato LV, Pereira LB, Castro GY, Tripathi RD (2009) Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress. J Hazard Mater 172(1):479–484. CrossRefPubMedGoogle Scholar
  18. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11. CrossRefPubMedGoogle Scholar
  19. He KL, Sun ZH, Hu YN, Zeng XY, Yu ZQ, Cheng HF (2017) Comparison of soil heavy metal pollution caused by e-waste recycling activities and traditional industrial operations. Environ Sci Pollut Res 24(10):9387–9398. CrossRefGoogle Scholar
  20. Jana S, Choudhuri MA (1982) Senescence in submerged aquatic angiosperms: effects of heavy metals. New Phytol 90(3):477–484. CrossRefGoogle Scholar
  21. Kopittke PM, Asher CJ, Kopittke RA, Menzies NW (2007) Toxic effects of Pb2+ on growth of cowpea (Vigna unguiculata). Environ Pollut 150(2):280–287. CrossRefPubMedGoogle Scholar
  22. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592CrossRefGoogle Scholar
  23. Liu JN, Zhou QX, Wang S, Sun T (2009) Cadmium tolerance and accumulation of Althaea rosea Cav. And its potential as a hyperaccumulator under chemical enhancement. Environ Monit Assess 149(1–4):419–427. CrossRefPubMedGoogle Scholar
  24. Liu M, Qi H, Zhang ZP, Song ZW, Kou TJ, Zhang WJ, Yu JL (2012) Response of photosynthesis and chlorophyll fluorescence to drought stress in two maize cultivars. Afr J Agric Res 7(34):4751–4760. CrossRefGoogle Scholar
  25. Malar S, Vikram SS, Favas PJ, Perumal V (2014) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Bot stud 55(1):54.
  26. Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotox Environ Saf 55(1):64–69. CrossRefGoogle Scholar
  27. Maodzeka A, Hussain N, Wei L, Zvobgo G, Mapodzeke JM, Adil MF, Shamsi IH (2017) Elucidating the physiological and biochemical responses of different tobacco (Nicotiana tabacum) genotypes to lead toxicity. Environ Toxicol Chem 36(1):175–181. CrossRefPubMedGoogle Scholar
  28. Maxwell K, Johnson GN (1981) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668. CrossRefGoogle Scholar
  29. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. CrossRefGoogle Scholar
  30. Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt-treated pea (Pisum sativum) cultivars and its putative use as salinity tolerance markers. J Plant Physiol 166(16):1764–1774. CrossRefPubMedGoogle Scholar
  31. Outridge PM, Noller BN (1991) Accumulation of toxic trace elements by freshwater vascular plants. In: Ware GW (ed) Reviews of environmental contamination and toxicology. Springer, New York, pp 1–63.
  32. Piotrowska A, Bajguz A, Godlewska-Żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). Environ Exp Bot 66(3):507–513. CrossRefGoogle Scholar
  33. Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology. Springer, New York, pp 113–136. CrossRefGoogle Scholar
  34. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees-a review. Environ Int 29(4):529–540. CrossRefPubMedGoogle Scholar
  35. Ralph PJ, Burchett MD (1998) Photosynthetic response of Halophila ovalis to heavy metal stress. Environ Pollut 103(1):91–101. CrossRefGoogle Scholar
  36. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? and what makes them so interesting? Plant Sci 180(2):169–181. CrossRefPubMedGoogle Scholar
  37. Rihab BA, Sabrine BO, Lina C, Imed M, Hatem BO, Ali O (2017) Cadmium effect on physiological responses of the tolerant Chlorophyta specie Picocystis sp. isolated from Tunisian wastewaters. Environ Sci Pollut Res 24(2):1803–1810. CrossRefGoogle Scholar
  38. Ruley AT, Sharma NC, Sahi SV (2004) Antioxidant defense in a lead accumulating plant, Sesbania drummondii. Plant Physiol Biochem 42(11):899–906. CrossRefPubMedGoogle Scholar
  39. Santos RW, Schmidt ÉC, Vieira IC, Costa GB, Rover T, Simioni C, Bouzon ZL (2015) The effect of different concentrations of copper and lead on the morphology and physiology of Hypnea musciformis cultivated in vitro: a comparative analysis. Protoplasma 252(5):1203–1215. CrossRefPubMedGoogle Scholar
  40. Sidhu GPS, Singh HP, Batish DR, Kohli RK (2016) Effect of lead on oxidative status, antioxidative response and metal accumulation in Coronopus didymus. Plant Physiol Biochem 105:290–296. CrossRefPubMedGoogle Scholar
  41. Spiro RG (1966) Analysis of sugars found in glycoproteins. Methods Enzymol 8:3–26. CrossRefGoogle Scholar
  42. Stobart AK, Griffiths WT, Ameen-Bukhari I, Sherwood RP (1985) The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol Plant 63(3):293–298. CrossRefGoogle Scholar
  43. Sun YB, Zhou QX, Wang L, Liu WT (2009) Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential cd-hyperaccumulator. J Hazard Mater 161(2–3):808–814. CrossRefPubMedGoogle Scholar
  44. Talbott LD, Zeiger E (1993) Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light. Plant Physiol 102(4):1163–1169. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, Iftikhar U, Abbasi GH (2016) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotox Environ Safe 126:138–146. CrossRefGoogle Scholar
  46. Thomas P, Juedes MJ (1992) Influence of lead on the glutathione status of Atlantic croaker tissues. Aquat Toxicol 23(1):11–29. CrossRefGoogle Scholar
  47. Uhlig C, Salemaa M, Vanha-Majamaa I, Derome J (2001) Element distribution in Empetrum nigrum microsites at heavy metal contaminated sites in Harjavalta, western Finland. Environ Pollut 112(3):435–442. CrossRefPubMedGoogle Scholar
  48. Upadhyaya A, Sankhla D, Davis TD, Sankhla N, Smith BN (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121(5):453–461. CrossRefGoogle Scholar
  49. Wilkins DA (1978) The measurement of tolerance to edaphic factors by means of root growth. New Phytol 80(3):623–633. CrossRefGoogle Scholar
  50. Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76(2):167–179. CrossRefGoogle Scholar
  51. Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14(4):7405–7432. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhou F, Wang J, Yang N (2015) Growth responses, antioxidant enzyme activities and lead accumulation of Sophora japonica and Platycladus orientalis seedlings under Pb and water stress. Plant Growth Regul 75(1):383–389. CrossRefGoogle Scholar
  53. Zhou J, Jiang Z, Ma J, Yang L, Wei Y (2017) The effects of lead stress on photosynthetic function and chloroplast ultrastructure of Robinia pseudoacacia seedlings. Environ Sci Pollut Res 24(11):10718–10726. CrossRefGoogle Scholar

Copyright information

© Plant Science and Biodiversity Centre, Slovak Academy of Sciences 2018

Authors and Affiliations

  • Yaping Huang
    • 1
  • Lihong Zu
    • 1
  • Meili Zhou
    • 1
  • Cong Shi
    • 2
  • Guangshuang Shen
    • 1
  • Fuchen Shi
    • 1
    Email author
  1. 1.Department of Plant Biology & Ecology, College of Life ScienceNankai UniversityTianjinChina
  2. 2.School of Environment and EnergyShenzhen Graduate School of Peking UniversityShenzhenChina

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