Advertisement

Plant and Soil

, Volume 359, Issue 1–2, pp 255–266 | Cite as

Effects of copper on growth, radial oxygen loss and root permeability of seedlings of the mangroves Bruguiera gymnorrhiza and Rhizophora stylosa

  • Hao Cheng
  • Nora Fung-Yee Tam
  • Youshao Wang
  • Shiyu Li
  • Guizhu Chen
  • Zhihong Ye
Regular Article

Abstract

Purpose

Mangrove wetlands have experienced significant contaminant input such as copper (Cu), aggravated by rapid urban development. This study aimed to investigate the possible function of root permeability in metal detoxification.

Methods

Pot trials were conducted to evaluate the responses of root permeability in relation to metal (Cu) exposure in seedlings of two mangroves: Bruguiera gymnorrhiza and Rhizophora stylosa.

Results

Copper inhibited plant growth and root permeability of the two species significantly (due to decreases in root porosity, thickening of exodermis and increases in lignification), leading to a significant reduction in radial oxygen loss (ROL). A negative correlation between soil Cu and ROL from root tip was also observed. The observed metal uptake by excised roots further indicated that increased lignification would directly prevent excessive Cu from further entering into the roots.

Conclusions

In summary, the two mangroves reacted to Cu by producing an impermeable barrier in roots. Such an inducible barrier to ROL is likely to be an adaptive strategy against Cu toxicity. This study reveals new evidence of a structural adaptive strategy for metal tolerance by mangrove plants.

Keywords

Heavy metal Mangrove plant Radial oxygen loss Root anatomy Root porosity 

Notes

Acknowledgments

We sincerely thank Prof. A.J.M. Baker (University of Melbourne, Australia and University of Sheffield, UK) for improving this manuscript and the anonymous reviewers for their helpful suggestions. This work was supported financially by the National 863 projects of China (No. 2007AA091703), National Natural Science Foundation of China (Nos. 30570345, 41106103), Specialized Research Fund for the Doctoral Program of Higher Education of China (20100171110035), China Postdoctoral Science Foundation (20110490934), and the Areas of Excellence established under the RGC of the Hong Kong SAR (Project No. AoE/P-04/04).

Supplementary material

11104_2012_1171_MOESM1_ESM.doc (120 kb)
Fig. S1a,b Anatomical symptoms of the root exodermis in the two mangrove species after 20 days pretreatment of salt (500 mmol L−1 NaCl), 1 cm from root tip. The sections were stained with phloroglucinol and hydrochloric acid to show lignification (red). Similar to Cu, significant increases of lignification were found in salt-pretreated roots. a B. gymnorrhiza, b R. stylosa. Only slight lignification was detected in control roots (data not shown, similar to the control roots shown in Fig. 4). Bar 50 μm (DOC 120 kb)

References

  1. Agoramoorthy G, Chen FA, Hsu MJ (2008) Threat of heavy metal pollution in halophtytic and mangrove plants of Tamil Nadu, India. Environ Pollut 155:320–326PubMedCrossRefGoogle Scholar
  2. Aguilar EA, Turner DW, Gibbs DJ, Armstrong W, Sivasithamparam K (2003) Oxygen distribution and movement, respiration and nutrient loading in banana roots (Musa spp. L.) subjected to aerated and oxygen-depleted environments. Plant Soil 253:91–102CrossRefGoogle Scholar
  3. Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from apex, respiration and waterlogging. Plant Physiol 25:192–197CrossRefGoogle Scholar
  4. Armstrong J, Armstrong W (2001) Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. Am J Bot 88:1359–1370PubMedCrossRefGoogle Scholar
  5. Armstrong J, Armstrong W (2005) Rice: sulfide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638PubMedCrossRefGoogle Scholar
  6. Armstrong W, Beckett PM (1987) Internal aeration and the development of stelar anoxia in submerged. A multishelled mathematical modal combining axial diffusion of oxygen in the cortex with radial losses to the stele, the wall layers and the rhizosphere. New Phytol 105:221–245CrossRefGoogle Scholar
  7. Armstrong W, Wright E (1975) The theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiol Planta 35:21–26CrossRefGoogle Scholar
  8. Armstrong J, Armstrong W, Beckett PM (1992) Phragmites australis: ventuir-and hunmidity-induced pressure flows enhance rhizome aeration and rhizosphere oxidation. New Phytol 120:197–207CrossRefGoogle Scholar
  9. Armstrong J, Keep R, Armstrong W (2009) Effect of oil on internal gas transport, radial oxygen loss, gas films and bud growth in Phragmites australis. Ann Bot 103:333–340PubMedCrossRefGoogle Scholar
  10. Bodegom PMV, Kanter MD, Bakker C, Aerts R (2005) Radial oxygen loss, a plastic property of dune slack plant species. Plant Soil 271:351–364CrossRefGoogle Scholar
  11. Caregnato FF, Koller CE, MacFarlane GR, Moreira JCF (2008) The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 56:1119–1127PubMedCrossRefGoogle Scholar
  12. Cheng H, Liu Y, Tam NFY, Wang X, Li SY, Chen GZ, Ye ZH (2010) The role of radial oxygen loss and root anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut 158:1189–1196PubMedCrossRefGoogle Scholar
  13. Colmer TD (2003a) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309PubMedCrossRefGoogle Scholar
  14. Colmer TD (2003b) Long-distance transport of gases in plants: a perspective on internal aeration and radial loss from roots. Plant Cell Environ 26:17–36CrossRefGoogle Scholar
  15. Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334PubMedCrossRefGoogle Scholar
  16. Degenhardt B, Ginmler H (2000) Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot 51:595–603PubMedCrossRefGoogle Scholar
  17. Deng H, Ye ZH, Wong MH (2009) Lead, zinc and iron (Fe2+) tolerance in wetland plants and relation to root anatomy and spatial pattern of ROL. Environ Exp Bot 65:353–362CrossRefGoogle Scholar
  18. Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49CrossRefGoogle Scholar
  19. Franke R, Schreiber L (2007) Suberin—a biopolyester forming apoplastic plant interfaces. Curr Opin Plant Biol 10:252–259PubMedCrossRefGoogle Scholar
  20. Garthwaite AJ, Armstrong W, Colmer TD (2008) Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum. New Phytol 179:405–416PubMedCrossRefGoogle Scholar
  21. Gibberd MR, Colmer TD, Cocks PS (1999) Root porosity and oxygen movement in waterlogging-tolerant Trifolium tomentosum and –intolerant Trifolium glomeratum. Plant Cell Environ 22:1161–1168CrossRefGoogle Scholar
  22. Insalud N, Bell RW, Colmer TD, Rerkasem B (2006) Morphological and physiological response of rice (Oryza sativa) to limited phosphorus supply in aerated and stagnate solution culture. Ann Bot 98:995–1004PubMedCrossRefGoogle Scholar
  23. Irvine I, Birch GF (1998) Distribution of heavy metals in surficial sediments of Port Jackson, Sydney, New South Wales. Aust J Earth Sci 45:297–304CrossRefGoogle Scholar
  24. Jackson MB, Armstrong W (1999) Formation of aerenchyma and processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287CrossRefGoogle Scholar
  25. Jacob DL, Otte ML (2003) Conflicting process in the wetland plant rhizosphere: metal retention or mobilization? Water Air Soil Pollut 3:91–104Google Scholar
  26. Kludze HK, Delaune RD, Patrick WH (1993) Aerenchyma formation and methane and oxygen exchange in rice. Soil Sci Soc Am J 51:368–391Google Scholar
  27. Krishnan KP, Fernandes SO, Chandan GS, Bharathi PAL (2007) Bacterial contribution to mitigation of iron and manganese in mangrove sediments. Mar Pollut Bull 54:1427–1433PubMedCrossRefGoogle Scholar
  28. Laskov C, Horn O, Hupfer M (2006) Environmental factors regulating the radial oxygen loss from roots of Myriophyllum spicatum and Potamogeton crispus. Aquat Bot 84:333–340CrossRefGoogle Scholar
  29. Leon ML, Warnken J (2008) Copper and sewage inputs from recreational vessels at popular anchor sites in a semi-enclosed Bay (Qld, Australia): estimates of potential annual loads. Mar Pollut Bull 57:838–845PubMedCrossRefGoogle Scholar
  30. Liu Y, Tam NFY, Yang JX, Pi N, Wong MH, Ye ZH (2009) Mixed heavy metals tolerance and radial oxygen loss in mangrove seedlings. Mar Pollut Bull 58:1843–1849PubMedCrossRefGoogle Scholar
  31. MacFarlane GR, Burchett MD (2000) Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquat Bot 68:45–59CrossRefGoogle Scholar
  32. MacFarlane GR, Burchett MD (2001) Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 42:233–241PubMedCrossRefGoogle Scholar
  33. MacFarlane GR, Burchett MD (2002) Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. Mar Environ Res 54:65–84PubMedCrossRefGoogle Scholar
  34. MacFarlane GR, Koller CE, Blomberg SP (2007) Accumulation and partitioning of heavy metals in mangroves: a synthsis of field-based studies. Chemosphere 69:1454–1464PubMedCrossRefGoogle Scholar
  35. Mano Y, Omori F, Takamizo T, Kindiger B, Bird RM, Loaisiga CH (2006) Variation for root aerenchyma formation in flooded and non-flooded maize and teosinte seedlings. Plant Soil 281:269–279CrossRefGoogle Scholar
  36. McDonald MP, Calwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant Cell Environ 24:585–596CrossRefGoogle Scholar
  37. Nishizono H (1987) The role of root cell wall in heavy metal tolerance of Athyriun yokoscense. Plant Soil 101:15–21CrossRefGoogle Scholar
  38. Otte ML, Rozema J, Koster L, Haarsma MS, Broekman RA (1989) Iron plaque on roots of Aster tripoliumL.: interaction with zinc uptake. New Phytol111:309–317CrossRefGoogle Scholar
  39. Pi N, Tam NFY, Wu Y, Wong MH (2009) Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot 90:222–230CrossRefGoogle Scholar
  40. Pi N, Tam NFY, Wong MH (2010) Effects of wastewater discharge on Fe plaque on root surface and radial oxygen loss of mangrove roots. Environ Pollut 158:381–387PubMedCrossRefGoogle Scholar
  41. Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246PubMedCrossRefGoogle Scholar
  42. Ponnamperuma FN (1984) Effect of flooding on soils. In: Kozlowski T (ed) Flooding and plant growth. Academic, New York, pp 9–45Google Scholar
  43. Ranathunge K, Steudle E, Lafitte R (2005) Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. Plant Cell Environ 28:121–133CrossRefGoogle Scholar
  44. Reinhardt DH, Rost TL (1995) Primary and lateral root development of dark and light-grown cotton seedlings under salinity stress. Bot Acta 108:403–465Google Scholar
  45. Santos ES, Knoppers BA, Oliveira EP, Lei T, Santenlli RE (2009) Regional geochemical baseline for sedimentary metals of the tropical São Francisco estuary, NE-Brazil. Mar Pollut Bull 58:601–634CrossRefGoogle Scholar
  46. Setia RC, Bala R (1994) Anatomical changes in root and stem of wheat (Triticum aestivum L.) in response to different heavy metals. Phytomorphology 44:95–104Google Scholar
  47. Shannon MC, Grieve CM, Francois LE (1994) Whole plant response to salinity. In: Wilkinson RE (ed) Plant-environment interactions. Dekker, New York, pp 199–244Google Scholar
  48. Soukup A, Armstrong W, Schreiber L, Franke R, Votrubová O (2007) Apoplastic barriers to radial oxygen loss and solute penetration: a chemical and functional comparison of the exodermis of two wetland species, Phragmites australis and Glyceria maxima. New Phytol 173:264–278PubMedCrossRefGoogle Scholar
  49. Suralta RR, Yamauchi A (2008) Root growth, aerenchyma development, and oxygen transport in rice genotypes subjected to drought and waterlogging. Environ Exp Bot 64:75–82CrossRefGoogle Scholar
  50. Tao S, Chen YJ, Cao XJ, Li BG (2003) Changes of copper speciation in maize rhizosphere soil. Environ Pollut 122:447–454PubMedCrossRefGoogle Scholar
  51. Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant Cell Environ 13:395–403CrossRefGoogle Scholar
  52. Vane CH, Harrison I, Kim AW, Hayes VM, Vickers NP, Hong K (2009) Organic and metal contamination in surface mangrove sediments of South China. Mar Pollut Bull 58:134–144PubMedCrossRefGoogle Scholar
  53. Verkleij JAC, Goldhirsh AG, Antosiewis DM, Schwitzguébel JP, Schrŏder P (2009) Dualities in plant tolerance to pollutants and their uptake and translocation to the upper plants parts. Environ Exp Bot 67:10–22CrossRefGoogle Scholar
  54. Visser ED, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Change in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245CrossRefGoogle Scholar
  55. Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytol 170:213–226PubMedCrossRefGoogle Scholar
  56. Yang JX (2008) Effect of aerenchyma and radial oxygen loss in wetland plants on metal (Pb, Zn) uptake and tolerance. PhD thesis, Sun Yat-sen University, PR ChinaGoogle Scholar
  57. Ye ZH, Baker AJM, Wong MH, Willis AJ (1997) Copper and nickel uptake, accumulation and tolerance in Typha latifolia L. with and without iron plaque on the root surface. New Phytol 136:481–488CrossRefGoogle Scholar
  58. Youssef T, Saenger P (1996) Anatomical adaptive strategies to flooding and rhizosphere oxidation in mangrove seedlings. Aust J Bot 44:297–313CrossRefGoogle Scholar
  59. Zhang CG, Leung KK, Wong YS, Tam NFY (2007a) Germination, growth and physiological responses of mangrove plant (Bruguiera gymnorrhiza) to lubricating oil pollution. Environ Exp Bot 60:127–136CrossRefGoogle Scholar
  60. Zhang FQ, Wang YS, Lou ZP, Dong JD (2007b) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50PubMedCrossRefGoogle Scholar
  61. Zhou F, Guo HC, Hao ZJ (2007) Spatial distribution of heavy metals in Hong Kong’s marine sediments and their human impacts: a GIS-based chemometric approach. Mar Pollut Bull 54:1372–1384PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Hao Cheng
    • 1
    • 2
  • Nora Fung-Yee Tam
    • 3
  • Youshao Wang
    • 2
  • Shiyu Li
    • 4
  • Guizhu Chen
    • 4
  • Zhihong Ye
    • 1
  1. 1.State Key Laboratory for Bio-control and Guangdong Key Laboratory of Plant Resources, School of Life SciencesSun Yat-sen UniversityGuangzhouPeople’s Republic of China
  2. 2.State Key Laboratory of Tropical Oceanography and Daya Bay Marine Biology Research Station, South China Sea Institute of OceanologyChinese Academy of SciencesGuangzhouPeople’s Republic of China
  3. 3.Department of Biology and ChemistryCity University of Hong KongHong KongPeople’s Republic of China
  4. 4.School of Environmental Science and EngineeringSun Yat-sen UniversityGuangzhouPeople’s Republic of China

Personalised recommendations