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Comparative analysis of Cd and Zn impacts on root distribution and morphology of Lolium perenne and Trifolium repens: implications for phytostabilization

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Abstract

Backgrounds and aims

The phytostabilization potential of plants is a direct function of their root systems. An experimental design was developed to investigate the impact of Cd and Zn on the root distribution and morphology of Lolium perenne and Trifolium repens.

Methods

Seedlings were transplanted into columns filled with washed quartz and irrigated daily with Cd- or Zn-containing nutrient solutions during 1 month. Root biomass, root length density (RLD) and diameter were subsequently quantified as a function of depth. Pot experiments were also performed to quantify metal, lignin and structural polysaccharides concentrations as well as cell viability.

Results

Lolium perenne accumulated Cd and Zn in the roots whereas T. repens was unable to restrict heavy metal translocation. Cadmium and Zn reduced rooting depth and RLD but induced thick shoot-borne roots in L. perenne. Cd-induced root swelling was related to lignification occurring in the exodermis and parenchyma of central cylinder. Hemicelluloses and lignin did not play a key role in root metal retention. Cadmium slightly reduced mean root cell viability whereas Zn increased this parameter in comparison to Cd.

Conclusions

Even though plant species like Lolium perenne and Trifolium repens may appear suitable for a phytostabilization scheme based on their shoot metal tolerance, exposure to toxic heavy metals drastically impairs their root distribution. This could jeopardize the setting up of phytostabilization trials. The metal-induced alterations of root system properties are clearly metal- and species-specific. At sites polluted with multiple metals, it is therefore recommended to first test their impact on the root system of multiple plant species so as to select the most appropriate species for each site.

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References

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  • Arganda-Carreras I, Fernandez-Gonzalez R, Munoz-Barrutia A, Ortiz-De-Solorzano C (2010) 3D reconstruction of histological sections : application to mammary gland tissue. Microsc Res Tech 73:1019–1029

    Article  PubMed  Google Scholar 

  • Arienzo M, Adamo P, Cozzolino V (2004) The potential of Lolium perenne for revegetation of contaminated soil from a metallurgical site. Sci Total Environ 319:13–25

    Article  CAS  PubMed  Google Scholar 

  • Bidar G, Garcon G, Pruvot C, Dewaele D, Cazier F, Douay F, Shirali P (2007) Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: plant metal concentration and phytotoxicity. Environ Pollut 147:546–553

    Article  CAS  PubMed  Google Scholar 

  • Bidar G, Verdin A, Garcon G, Pruvot C, Laruelle F, Grandmougin-Ferjani A, Douay F, Shirali P (2008) Changes in fatty acid composition and content of two plants (Lolium perenne and Trifolium repens) grown during 6 and 18 months in a metal (Pb, Cd, Zn) contaminated field. Water Air Soil Pollut 192:281–291

    Article  CAS  Google Scholar 

  • Bidar G, Pruvot C, Garçon G, Verdin A, Shirali P, Douay F (2009) Seasonal and annual variations of metal uptake, bioaccumulation, and toxicity in Trifolium repens and Lolium perenne growing in a heavy metal-contaminated field. Environ Sci Pollut Res 16:42–53

    Article  CAS  Google Scholar 

  • Boisson J, Bouchardon JL, Carrey A, Charissou AM, Colpaert J, Faure O, Guérin V, Joulian C, Pottecher G, Remon E, Vangronsveld J (2009) Evaluation des performances de la phytostabilisation sur un grand site. 2e Rencontres Nationales de la Recherche sur les Sites et Sols Pollués, ADEME, Paris

    Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Broos K, Uyttebroek M, Mertens J, Smolders E (2004) A survey of symbiotic nitrogen fixation by white clover grown on metal contaminated soils. Soil Biol Biochem 36:633–640

    Article  CAS  Google Scholar 

  • Chen G, Liu Y, Wang R, Zhang J, Owens G (2013) Cadmium adsorption by willow root: the role of cell walls and their subfractions. Environ Sci Pollut Res:1–8

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719

    Article  CAS  PubMed  Google Scholar 

  • Dawson LA, Thornton B, Pratt SM, Paterson E (2004) Morphological and topological responses of roots to defoliation and nitrogen supply in Lolium perenne and Festuca ovina. New Phytol 161:811–818

    Article  Google Scholar 

  • Deiana S, Manunza B, Palma A, Premoli A, Gessa C (2001) Interactions and mobilization of metal ions at the root-soil interface. In: Gobran GR, Wenzel WW, Lomobi E (ed) Trace elements in the rhizosphere. Academic Press, pp 127–148

  • Delpérée C, Lutts S (2008) Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations. J Integr Plant Biol 50:300–310

    Article  PubMed  Google Scholar 

  • Dickinson NM, Baker AJ, Doronila A, Laidlaw S, Reeves RD (2009) Phytoremediation of inorganics: realism and synergies. Int J Phytoremediat 11:97–114

    Article  CAS  Google Scholar 

  • Domínguez MT, Maranón T, Murillo JM, Schulin R, Robinson BH (2008) Trace element accumulation in woody plants of the Guadiamar Valley, SW Spain: a large-scale phytomanagement case study. Environ Pollut 152:50–59

    Article  PubMed  Google Scholar 

  • Ďurčeková K, Huttová J, Mistrik I, Ollé M, Tamás L (2007) Cadmium induces premature xylogenesis in barley roots. Plant Soil 290:61–68

    Article  Google Scholar 

  • Ederli L, Reale L, Ferranti F, Pasqualini S (2004) Responses induced by high concentration of cadmium in Phragmites australis roots. Physiol Plant 121:66–74

    Article  CAS  PubMed  Google Scholar 

  • Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–566

    Article  CAS  Google Scholar 

  • Fusconi A, Gallo C, Camusso W (2007) Effects of cadmium on root apical meristems of Pisum sativum L.: cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution. Mutat Res Genet Toxicol Environ 632:9–19

    Article  CAS  Google Scholar 

  • Grant CA, Clarke JM, Duguid S, Chaney RL (2008) Selection and breeding of plant cultivars to minimize cadmium accumulation. Sci Total Environ 390:301–310

    Article  CAS  PubMed  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    Article  CAS  Google Scholar 

  • Houben D, Pircar J, Sonnet P (2012) Heavy metal immobilization by cost-effective amendments in a contaminated soil: effects on metal leaching and phytoavailability. J Geochem Explor 123:87–94

    Article  CAS  Google Scholar 

  • Hu G, Huang S, Chen H, Wang F (2010) Binding of four heavy metals to hemicelluloses from rice bran. Food Res Int 43:203–206

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Kapur JN, Sahoo PK, Wong ACK (1985) A new method for gray-level picture thresholding using the entropy of the histogram. Graph Model 29:273–285

    Google Scholar 

  • Kidd P, Barceló J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S, Clemente R, Monterroso C (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259

    Article  CAS  Google Scholar 

  • Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—a review. Waste Manag 28:215–225

    Article  CAS  PubMed  Google Scholar 

  • Lambrechts T, Gustot Q, Couder E, Houben D, Iserentant A, Lutts S (2011) Comparison of EDTA-enhanced phytoextraction and phytostabilisation strategies with Lolium perenne on a heavy metal contaminated soil. Chemosphere 85:1290–1298

    Article  CAS  PubMed  Google Scholar 

  • Lambrechts T, Lequeue G, Lobet G, Lutts S (2013) Impact of cadmium and zinc on root system of Lolium perenne and Trifolium repens. Commun Agric Appl Biol Sci 78:19–24

    CAS  PubMed  Google Scholar 

  • Larbi A, Morales F, Abadía A, Gogorcena Y, Lucena JJ, Abadía J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–1464

    Article  CAS  Google Scholar 

  • Lobet G, Draye X (2013) Novel scanning procedure enabling the vectorization of entire rhizotron-grown root systems. Plant Methods 9: doi:10.1186/1746-4811-9-1

  • Lopareva-Pohu A, Verdin A, Garçon G, Lounès-Hadj Sahraoui A, Pourrut B, Debiane D, Waterlot C, Laruelle F, Bidar G, Douay F, Shirali P (2011) Influence of fly ash aided phytostabilisation of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environ Pollut 159:1721–1729

    Article  CAS  PubMed  Google Scholar 

  • Lunáčková L, Šottníková A, Masarovičová E, Lux A, Streško V (2003) Comparison of cadmium effect on willow and poplar in response to different cultivation conditions. Biol Plant 47:403–411

    Article  Google Scholar 

  • Lutts S, Almansouri M, Kinet JM (2004) Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus. Plant Sci 167:9–18

    Article  CAS  Google Scholar 

  • Lux A, Martinka M, Vaculík M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37

    Article  CAS  PubMed  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7

    CAS  PubMed Central  PubMed  Google Scholar 

  • Macnicol RD, Beckett PH (1985) Critical tissue concentrations of potentially toxic elements. Plant Soil 85:107–129

    Article  CAS  Google Scholar 

  • Maksimović I, Kastori R, Krstić L, Luković J (2007) Steady presence of cadmium and nickel affects root anatomy, accumulation and distribution of essential ions in maize seedlings. Biol Plant 51:589–592

    Article  Google Scholar 

  • Mattia C, Bischetti GB, Gentile F (2005) Biotechnical characteristics of root systems of typical Mediterranean species. Plant Soil 278:23–32

    Article  CAS  Google Scholar 

  • Mench M, Bussiere S, Boisson J, Castaing E, Vangronsveld J, Ruttens A, De Koe T, Bleeker P, Assunçāo A, Manceau A (2003) Progress in remediation and revegetation of the barren Jales gold mine spoil after in situ treatments. Plant Soil 249:187–202

    Article  CAS  Google Scholar 

  • Mench M, Lepp N, Bert V, Schwitzguébel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070

    Article  CAS  Google Scholar 

  • Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng Geol 60:193–207

    Article  Google Scholar 

  • Nawirska A (2005) Binding of heavy metals to pomace fibers. Food Chem 90:395–400

    Article  CAS  Google Scholar 

  • 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 101:15–20

    Article  CAS  Google Scholar 

  • Passioura JB (2006) Viewpoint: the perils of pot experiments. Funct Plant Biol 33:1075–1079

    Article  Google Scholar 

  • Pejic B, Vukcevic M, Kostic M, Skundric P (2009) Biosorption of heavy metal ions from aqueous solutions by short hemp fibers: effect of chemical composition. J Hazard Mater 164:146–153

    Article  CAS  PubMed  Google Scholar 

  • Pichtel J, Salt CA (1998) Vegetative growth and trace metal accumulation on metalliferous wastes. J Environ Qual 27:618–624

    Article  CAS  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  PubMed  Google Scholar 

  • Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850

    Article  Google Scholar 

  • Poschenrieder CH, Barceló J (2004) Water relations in heavy metal stressed plants. In: Prasad MNV (ed) Heavy metal stress in plants: from molecules to ecosystems, 2nd edn. Springer, Berlin, pp 249–270

    Chapter  Google Scholar 

  • Přibyl P, Cepák V, Zachleder V (2005) Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure: I. The effect of cadmium. Protoplasma 226:231–240

    Article  PubMed  Google Scholar 

  • Reubens B, Poesen J, Danjon F, Geudens G, Muys B (2007) The role of fine and coarse roots in shallow slope stability and soil erosion control with a focus on root system architecture: a review. Trees-Struct Funct 21:385–402

    Article  Google Scholar 

  • Robinson BH, Banuelos G, Conesa HM, Evangelou MW, Schulin R (2009) The phytomanagement of trace elements in soil. Crit Rev Plant Sci 28:240–266

    Article  CAS  Google Scholar 

  • Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126

    CAS  PubMed  Google Scholar 

  • Santibáñez C, Verdugo C, Ginocchio R (2008) Phytostabilization of copper mine tailings with biosolids: implications for metal uptake and productivity of Lolium perenne. Sci Total Environ 395:1–10

    Article  PubMed  Google Scholar 

  • Schützendübel A, Schwanz P, Teichmann T, Gross K, Langenfeld-Heyser R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 127:887–898

    Article  PubMed Central  PubMed  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50

    Article  CAS  PubMed  Google Scholar 

  • Šmilauerová M, Šmilauer P (2002) Morphological responses of plant roots to heterogeneity of soil resources. New Phytol 154:703–715

    Article  Google Scholar 

  • Sresty TVS, Rao MKV (1999) Ultrastructural alterations in response to zinc and nickel stress in the root cells of pigeonpea. Environ Exp Bot 41:3–13

    Article  CAS  Google Scholar 

  • Tack FMG, Singh SP, Verloo MG (1998) Heavy metal concentrations in consecutive saturation extracts of dredged sediment derived surface soils. Environ Pollut 103:109–115

    Article  CAS  Google Scholar 

  • Van Soest PV, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597

    Article  PubMed  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    Article  CAS  PubMed  Google Scholar 

  • Weihermüller L, Siemens J, Deurer M, Knoblauch S, Rupp H, Göttlein A, Pütz T (2007) In situ soil water extraction: a review. J Environ Qual 36:1735–1748

    Article  PubMed  Google Scholar 

  • Yang X, Baligar VC, Martens DC, Clark RB (1995) Influx, transport, and accumulation of cadmium in plant species grown at different Cd2+ activities. J Environ Sci Health B 30:569–583

    Article  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, Manila

    Google Scholar 

  • Zhu J, Ingram PA, Benfey PN, Elich T (2011) From lab to field, new approaches to phenotyping root system architecture. Curr Opin Plant Biol 14:310–317

    Article  PubMed  Google Scholar 

  • Zhu XF, Lei GJ, Jiang T, Liu Y, Li GX, Zheng SJ (2012) Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta:1–9

  • Zobel RW, Kinraide TB, Baligar VC (2007) Fine root diameters can change in response to changes in nutrient concentrations. Plant Soil 297:243–254

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Dr. Xavier Draye for his pertinent suggestions about the experimental design, as well as Thomas Dagbert for his technical assistance concerning the root cross-sections.

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Correspondence to Thomas Lambrechts.

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Responsible Editor: Juan Barcelo.

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Lambrechts, T., Lequeue, G., Lobet, G. et al. Comparative analysis of Cd and Zn impacts on root distribution and morphology of Lolium perenne and Trifolium repens: implications for phytostabilization. Plant Soil 376, 229–244 (2014). https://doi.org/10.1007/s11104-013-1975-7

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