Skip to main content
Log in

Manganese tolerance and accumulation in six Mn hyperaccumulators or accumulators

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

This study used hydroponics cultivation to investigate the manganese (Mn) accumulation and tolerance abilities of six species—Phytolacca americana L., Poa annua L., Comnyza canadensis L., Cynodon dactylon L., Polygonum hydropiper L., and Polygonum perfoliatum L. We found that P. perfoliatum, P. hydropiper, and P. americana were Mn-hyperaccumulators and that P. perforliatum have superior Mn accumulation and toleration abilities over the other five species. The Mn concentration within the shoots of P. perfoliatum reached as high as 18,342.3 mg kg−1. The root growth of P. perfoliatum was promoted under low-Mn treatments, but the growths of the five other species were inhibited by the Mn treatments and the damage intensified as Mn concentration increased. The biomass of P. perfoliatum was minimally affected by the Mn treatments. The chlorophyll (CHL), soluble protein (SP), and malondialdehyde (MDA) contents of P. perfoliatum were not adversely affected, but these parameters of the other five species showed significant (P < 0.05) deterioration from the control. By comparison among the six species, the hyperaccumulator P. perfoliatum was the most suitable species for bioremediation of Mn-polluted environments. However, the findings need further study in soil cultivation.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baldisserotto C, Ferroni L, Anfuso E, Pagnoni A, Fasulo MP, Pancaldi S (2007) Responses of Trapa natans L. floating laminae to high concentrations of manganese. Protoplasma 231:65–82. doi:10.1007/s00709-007-0242-2

    Article  CAS  PubMed  Google Scholar 

  • Barančiková G, Madaras M, Rybár Q (2004) Crop contamination by selected trace elements. J Soils Sediments 4:37–42. doi:10.1007/BF02990827

    Article  Google Scholar 

  • Barceló J, Poschenrieder C (2003) Phytoremediation: principles and perspectives. Contrib Sci 2:333–344

    Google Scholar 

  • Bidwell SD, Woodrow IE, Batiano GN, Sommer-Knudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905

    Article  CAS  Google Scholar 

  • Bouwman LA, Bloem J, Römkens PFAM, Japenga J (2005) EDGA amendment of slightly heavy metal loaded soil affects heavy metal solubility, crop growth and microbivorous nematodes but not bacteria and herbivorous nematodes. Soil Biol Biochem 37:71–278

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Büchel C, Barber J, Ananyev G, Eshaghi S, Watt R, Dismukes C (1999) Photoassembly of the manganese cluster and oxygen evolution from monomeric and dimeric CP47-reaction center photosystem II complexes. Proc Natl Acad Sci USA 96:14288–14293

    Article  PubMed  Google Scholar 

  • Cao G, Liang MZ (2004) Manganese-trace element necessary for plants at the balance growth system. Soil Fert 1:23

    Google Scholar 

  • Carranza-Álvarez C, Alonso-Castro AJ, Alfaro-De La Torre MC, Garcίa-De La Cruz RF (2008) Accumulation and distribution of heavy metals in Scirpus americanus and Typha latifolia from an artificial lagoon in San Luis Potosί, México. Water Air Soil Pollut 88:297–309

    Article  Google Scholar 

  • Chaney RL, Li YM, Brown SL, Homer FA, Malik M, Angle JS, Baker AJM, Reeves RD, Chin M (2000) Improving metal hyperaccumulator wild plants to develop commercial phytoextraction systems: approaches and progress. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 129–158

    Google Scholar 

  • Ding JQ, Reardon R, Wu Y, Zheng H, Fu WD (2006) Biological control of invasive plants through collaboration between China and the United States of America: a perspective. Biol Invasions 8:1439–1450. doi:10.1007/s10530-005-5833-2

    Article  Google Scholar 

  • Dučić T, Polle A (2005) Transport and detoxification of manganese and copper in plants. Brazilian J Plant Physiol 17:103–112

    Google Scholar 

  • Erikson KM, Aschner M (2003) Manganese neurotoxicity and glutamate GABA interaction. Neurochem Int 43:475–480. doi:10.1016/S0197-0186(03)00037-8

    Article  CAS  PubMed  Google Scholar 

  • Fan ZL, Mo LY, Chen TB, Zhai LM, Lei M, Huang AQ, Li H (2007) Accumulation of Cu, Mn and Zn in plants grown in areas near three abandoned mines in Guangxi and the discovery of potential Mn-hyperaccumulators. Geograph Res 26:125–131

    Google Scholar 

  • Fellet G, Marchiol L, Perosa D, Zerbi G (2007) The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol Eng 31:207–214. doi:10.1016/j.ecoleng.2007.06.011

    Article  Google Scholar 

  • Fernando DR, Batianoff GN, BakerAJ WIE (2006a) In vivo localization of manganese in the hyperaccumulator Gossia bidwilii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Environ 29:1012–1020

    Article  CAS  PubMed  Google Scholar 

  • Fernando DR, Bakkaus EJ, Perrier N, Baker AJM, Woodrow IE, Batianoff GN, Collins RN (2006b) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytol 171:751–758

    Article  CAS  PubMed  Google Scholar 

  • Fernando DR, Marshall AT, Gouget B, Carrie M, Collins RN, Woodrow IE, Baker AJ (2008a) Novel pattern of foliar metal distribution in a manganese hyperaccumulator. Funct Plant Biol 35:193–200

    Article  CAS  Google Scholar 

  • Fernando DR, Woodrow IE, Jaffr T, Dumontet V, Marshall AT, Baker AJM (2008b) Foliar mangan-ese accumulation by Maytenus founieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185

    CAS  PubMed  Google Scholar 

  • Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236. doi:10.1016/S0960-8524(00)00108-5

    Article  CAS  PubMed  Google Scholar 

  • Guo SL, Huang CB, Bian Y, Lin GP (2002) On absorption and accumulation of six heavy metal elements of weeds in Jinhua suburb-survey on content of six heavy metal elements in weeds and soil. J Shanghai Jiaotong University (Agr Sci) 20:1–8

    Google Scholar 

  • Han YL, Huang SZ, Gu JG, Qiu S, Chen JM (2008) Tolerance and accumulation of lead by species of Iris L. Ecotoxicology 17:853–859. doi:10.1007/s10646-008-0248-3

    Article  CAS  PubMed  Google Scholar 

  • Hegedüs A, Erdei S, Horváth G (2001) Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Sci 106:1085–1093

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1957) California agriculture experiment station. Circular, pp 347

  • Hyatt LA, Araki S (2006) Comparative population dynamics of an invading species in its native and novel ranges. Biol Invasions 8:261–275. doi:10.1007/s10530-004-5572-9

    Article  Google Scholar 

  • Islam E, Liu D, Li TQ, Yang XE, Jin XF, Mahmood Q, Tian SK, Li JY (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazardous Mater 154:914–926. doi:10.1016/j.jhazmat.2007.10.121

    Article  CAS  Google Scholar 

  • Krämer U, Pickering IJ, Prince RC, Raskin I, Salt DE (2002) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1353. doi:10.1104/pp.122.4.1343

    Article  Google Scholar 

  • Lei YB, Chen K, Tian XR, Korpelainen H, Li CY (2007) Effect of Mn toxicity on morphological and physiological changes in two Populus cathayana populations originating from different habitats. Trees 21:569–580

    Article  CAS  Google Scholar 

  • Long XX, Yang X, Ye ZQ, Ni WZ, Shi WY (2002) Differences of uptake and accumulation of Zinc in four species of sedum. Acta Bot Sin 44:152–157

    CAS  Google Scholar 

  • Marchiol L, Sacco P, Assolari S, Zerbi G (2004) Reclamation of Polluted soil: phytoremediation potential of crop related Brassica species. Water Air Soil Pollut 158:345–356. doi:10.1023/B:WATE.0000044862.51031.fb

    Article  CAS  Google Scholar 

  • Mark WP, Alejandro V, Edward FR (2005) Manganese toxicity thresholds for restoration grass species. Environ Pollut 135:313–322. doi:10.1016/j.envpol.2004.08.006

    Article  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 142:77–282. doi:10.1016/S0958-1669(03)00060-0

    Google Scholar 

  • Meerts P, Isacker NV (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231

    Article  Google Scholar 

  • Memon AR, Chino M, Takeoka Y, Hara K, Yatazawa M (1980) Distribution of manganese in leaf tissues of the manganese accumulator: Acanthopanax sciadophylloides as revealed by electronprobe X-ray microanalysis. J Plant Nutr 2:457–476

    Article  CAS  Google Scholar 

  • Memon AR, Aktoprakligil D, Özdemir A, Vertii A (2001) Heavy metal accumulation and detoxification mechanisms in plants. Turk J Bot 25:111–121

    Google Scholar 

  • Panich-Pat T, Pokethitiyook P, Kruareachue M, Upasam ES, Srinives P, Lanza GR (2004) Removal of lead from contaminated soils by Typha agustifolia. Water Air Soil Pollut 155:159–171. doi:10.1023/B:WATE.0000026523.96599.6b

    Article  CAS  Google Scholar 

  • Peng KJ, Li XD, Luo CL, Shen ZG (2006) Vegetation composition and heavy metal uptake by wild plants at three contaminated sites in Xiangxi area. China J Environ Sci Health Part A 41:65–75

    Article  CAS  Google Scholar 

  • Peng KJ, Luo CL, You WX, Lian CL, Li XD, Shen ZG (2008) Manganese uptake and interactions with cadmium in the hyperaccumulator—Phytolacca americana L. J Hazard Mater 154:674–681. doi:10.1016/j.jhazmat.2007.10.080

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742

    Article  CAS  PubMed  Google Scholar 

  • Prasad MNV (2003) Phytoremediation of metal-polluted ecosystems: hype for commercialization. Russ J Plant Physiol 50:686–700. doi:10.1023/A:1025604627496

    Article  CAS  Google Scholar 

  • Proctor J, Phillipps C, Du GK, Heaney A, Robertson FM (1989) Ecological studies on Gunung Silam, a small ultrabasic mountain in Sabah, Malaysia: II Some forest processes. J Ecol 77:317–331

    Article  CAS  Google Scholar 

  • Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65. doi:10.1023/A:1022572517197

    Article  CAS  Google Scholar 

  • Reeves RD, Adigüzel N (2004) Rare plants and nickel accumulators from Turkish serpentine soils, with special reference to Centaurea species. Turkish J Bot 28:147–153

    Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York

    Google Scholar 

  • Ren LM, Liu P (2007) Review of manganese toxicity & the mechanisms of plant tolerance. Acta Ecol Sin 21:356–367

    Google Scholar 

  • Ren LM, Liu P, Cai MZ, Xu GD, Fang XY, Cheng ZX (2007) Physiological response of Polygonum hydropiper, Comnyza canadensis, Polygonum perfoliatum and Phytolacca americana to Manganese toxicity. J Soil Water Conser 21:81–85

    Google Scholar 

  • Ru SH, Wang JQ, Su DC (2004) Characteristics of Cd uptake and accumulation in two Cd accumulator oilseed rape species. J Environ Sci 16:594–598

    CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar PBAN, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnol 13:468–474

    Article  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  CAS  PubMed  Google Scholar 

  • Santandrea G, Pandolfi T, Bennici A (2000) A physiological characterization of Mn-tolerant tobacco plants selected by in vitro culture. Plant Sci 150:163–170

    Article  CAS  Google Scholar 

  • Shen ZG, Liu YL (1998) Progress in the study on that hyperaccumulate heavy metal. Plant Physiol Commun 34:133–139

    Google Scholar 

  • Shen RF, Ma JF, Kyo M, Iwashita T (2002) Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta 215:394–398. doi:10.1007/s00425-002-0763-z

    Article  CAS  PubMed  Google Scholar 

  • Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallic ion decontami-nation from soil. Appl Microbiol Biotechnol 61:405–412

    CAS  PubMed  Google Scholar 

  • 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 161:808–814. doi:10.1016/j.jhazmat.2008.04.030

    Article  CAS  PubMed  Google Scholar 

  • Tie BQ, Yuan M, Tang MZ (2005) Phytolacca americana L.: a new manganese accumulator plant. J Agro-Environ Sci China 24:340–343

    CAS  Google Scholar 

  • Wang ME, Zhou QX (2006) Effects of herbicide chlorimuron-ethyl on physiological mechanisms in wheat (Triticum aestivum). Ecotox Environ Safe 64:190–197. doi:10.1016/j.ecoenv.2005.03.032

    Article  CAS  Google Scholar 

  • Wang QR, Cui YS, Dong YT (2001) Phytoremediation—an effective approach of heavy metal clean up from contaminated soil. Acta Ecol Sin 21:326–331

    Google Scholar 

  • Wang H, Tang SM, Liao XJ, Cao QM, Yang AF, Wang TZ (2007) A new manganese hyperaccumulator: Polygonum hydropiper L. Ecol Environ 16:830–834

    Google Scholar 

  • Wei SH, Zhou QX (2004) Identification of weed species with hyperaccumulative characteristics of heavy metals. Prog Nat Sci 14:1259–1265

    Article  Google Scholar 

  • Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, McIntyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restorat Ecol 12:106–116

    Article  Google Scholar 

  • Wissemeier AH, Horst WJ (1992) Effect of light intensity on manganese toxicity symptoms and callose formation in cowpea (Vigna unguiculata). Plant Soil 143:299–309. doi:10.1007/BF00007886

    Article  CAS  Google Scholar 

  • Wu XY, von Tiedemann A (2002) Impact of fungicides on active oxygen species and antioxidant enzymes in spring barley (Hordeum vulgare L.) exposed to ozone. Environ Pollut 116:37–47. doi:10.1016/S0269-7491(01)00174-9

    Article  CAS  PubMed  Google Scholar 

  • Xu XH, Shi JY, Chen YX, Chen XC, Wan H, Perera A (2006) Distribution and mobility of manganese in the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Plant Soil 285:323–331. doi:10.1007/s11104-006-9018-2

    Article  CAS  Google Scholar 

  • Xu XH, Shi JY, Chen XC, Chen YX, Hu TD (2009) Chemical forms of manganese in the leaves of ma-nganese hyperaccumulator Phytolacca acinosa Roxb (Phytolaccaceae). Plant and Soil 318:197–204. doi:10.1007/s11104-008-9829-4

    Article  CAS  Google Scholar 

  • Xue SG, Chen YX, Lin Q, Xu SY, Wang YP (2003) Phytolacca acinosa Roxb. (Phytolaccaceae): a new manganese hyperaccumulator plant from Southern China. Acta Ecol Sin 23:935–937

    Google Scholar 

  • Yuan M, Tie BQ, Tang MZ, Isao A (2007) Accumulation and uptake of manganese in a hyperaccumulator Phytolacca americana. Miner Eng 20:188–190. doi:10.1016/j.mineng.2006.06.003

    Article  Google Scholar 

  • Zang XP (1999) Manganese toxicity of soil and manganese toxicity of plant. Chin J Soil Sci 30:139–141

    CAS  Google Scholar 

  • Zhou QX, Wei SH, Zhang QR (2004) Ecological remediation. Chinese Environmental Science, Beijing

    Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of People’s Republic of China (No.30540056) and by the Zhejiang Provincial Natural Science Foundation for Young Scientist of People’s Republic of China (No.Y306391). The authors are grateful to professor Jianwei Pan and doctor Wenrong Chen for providing valuable guidance for this experiment and the paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peng Liu.

Additional information

Responsible Editor: Juan Barcelo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, P., Tang, X., Gong, C. et al. Manganese tolerance and accumulation in six Mn hyperaccumulators or accumulators. Plant Soil 335, 385–395 (2010). https://doi.org/10.1007/s11104-010-0427-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-010-0427-x

Keywords

Navigation