Skip to main content
Log in

Linking root traits to copper exclusion mechanisms in Silene paradoxa L. (Caryophyllaceae)

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

Abstract

Background and aims

Copper is one of the most important pollutants in mine-contaminated soils. This study tests the response in a sensitive population vs a tolerant one of the model species Silene paradoxa in order to understand the general mechanisms of tolerance at the micromorphological and ultrastructural level.

Methods

Two populations of Silene paradoxa were grown in hydroponics and exposed to different CuSO4 treatments. The roots were investigated with light, fluorescence and transmission electron microscope. Callose and lignin were spectrophotometrically determined.

Results

The tolerant population constitutively possessed a higher amount of mucilage and was able to reduce the length of the zone between the apex and the first lignified tracheids. Callose production decreased. It did not show remarkable copper-induced ultrastructural modifications, apart from the presence of precipitates in the tangential walls. The sensitive population showed huge nucleoli with a spongy periphery in the central cylinder together with the presence of electrondense granules in the mitochondria. Plastids were rarely observed and generally very electrondense and elongated.

Conclusions

n the copper tolerant population of S. paradoxa some of the root traits concurring to generate metal-excluding roots were suggested to be mucilage and lignin production and the reduction of the subapical root zone.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Archambault DJ, Zhang GC, Taylor GJ (1996) Accumulation of Al in root mucilage of an Al-resistant and an Al-sensitive cultivar of wheat. Plant Physiol 112:1471–1478

    PubMed Central  CAS  PubMed  Google Scholar 

  • Arnetoli M (2004) Tossicità e tolleranza all’arsenico in due popolazioni di Silene paradoxa L. Bachelor Thesis. Università di Firenze, Italy

  • Arnetoli M, Vooijs R, Gonnelli C, Gabbrielli R, Verkleij JAC, Schat H (2008) High-level Zn and Cd tolerance in Silene paradoxa L. from a moderately Cd- and Zn-contaminated copper mine tailing. Environ Pollut 156:380–386

    Article  CAS  PubMed  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Baker AJM (1987) Metal tolerance. New Phytol 106:93–111

    Article  CAS  Google Scholar 

  • Balsberg Påhlsson AM (1989) Toxicity of heavy metals (Zn, Cu, Cd, Pb) to vascular plants. Water Air Soil Pollut 47:287–319

    Article  Google Scholar 

  • Bouazizi H, Jouili H, Geitmann A, El Ferjani E (2010) Structural changes of cell wall and lignifying enzymes modulations in bean roots in response to copper stress. Biol Trace Elem Res 136:232–240

    Article  CAS  PubMed  Google Scholar 

  • Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI (2010) The nucleolus under stress. Mol Cell 40:216–227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brinkmann K, Blaschke L, Polle A (2002) Comparison of different methods for lignin determination as a basis for calibration of near infra-red reflectance spectroscopy and implication of lignoproteins. J Chem Ecol 28:2483–2501

    Article  CAS  PubMed  Google Scholar 

  • Brooks RR, Lee J, Reeves RD, Jaffré T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57

    Article  CAS  Google Scholar 

  • Bruni A, Vannini GL (1973) Possibilità d’impiego dell’arancio di Acridina e dell’acriflavina nella ricerca istochimica dei polisaccaridi insolubili della cellula vegetale. G Bot Ital 107:201–206

    Article  CAS  Google Scholar 

  • Cai MZ, Wang FM, Li RF, Zhang SN, Wang N, Xu GD (2011) Response and tolerance of root border cells to aluminum toxicity in soybean seedlings. J Inorg Biochem 105:966–971

    Article  CAS  PubMed  Google Scholar 

  • Cai M, Wang N, Xing C, Wang F, Wu K, Du X (2013) Immobilization of aluminum with mucilage secreted by root cap and root border cells is related to aluminum resistance in Glycine max L. Environ Sci Pollut Res 20:8924–8933

    Article  CAS  Google Scholar 

  • Chen E-L, Chen Y-A, Chen L-M, Liu Z-H (2002) Effect of copper on peroxidase activity and lignin content in Raphanus sativus. Plant Physiol Biochem 40:439–444

    Article  CAS  Google Scholar 

  • Colzi I, Doumett S, Del Bubba M, Fornaini J, Arnetoli M, Gabbrielli R, Gonnelli C (2011) On the role of the cell wall in the phenomenon of copper tolerance in Silene paradoxa L. Environ Exp Bot 72:77–83

    Article  CAS  Google Scholar 

  • Colzi I, Arnetoli M, Gallo A, Doumett S, Del Bubba M, Pignattelli S, Gabbrielli R, Gonnelli C (2012) Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L. Environ Exp Bot 78:91–98

    Article  CAS  Google Scholar 

  • Dronnet VM, Renard CMGC, Axelos MAV, Thibault JF (1996) Characterisation and selectivity of divalent metal ions binding by citrus and sugar-beet pectins. Carbohyd Polym 30:253–263

    Article  CAS  Google Scholar 

  • Ernst WHO (2006) Evolution of metal tolerance in higher plants. Forest Snow Land Res 80:251–274

    Google Scholar 

  • Feigl G, Kumar D, Lehotai N, Tugyi N, Molnár A, Ordog A, Szepesi A, Gemes K, Laskay G, Erdei L, Kolbert Z (2013) Physiological and morphological responses of the root system of Indian mustard (Brassica juncea (L.) Czern.) and rapeseed (Brassica napus L.) to copper stress. Ecotox Environ Safe 94:179–189

    Article  CAS  Google Scholar 

  • Geng MJ, Xu MM, Xiao HD, Wang HZ, He LL, Zhao ZQ, Yu M (2012) Protective role of mucilage against Al toxicity to root apex of pea (Pisum sativum). Acta Physiol Plant 34:1261–1266

    Article  CAS  Google Scholar 

  • Ghanem ME, Han RM, Classen B, Quetin-Leclerq J, Mahy G, Ruan CJ, Pérez-Alfocea F, Lutts S (2010) Mucilage and polysaccharides in the halophyte plant species Kosteletzkya virginica: localization and composition in relation to salt stress. J Plant Physiol 167:382–392

    Article  CAS  Google Scholar 

  • Gidley MJ, Nishinari K (2009) Physico-chemistry of (1,3)-beta glucans. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry and biology of (1,3)-beta glucans and related polysaccharides. Academic, Burlington, pp 47–118

    Chapter  Google Scholar 

  • Hall LJ (2002) Cellular mechanism for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hawes MC, Brigham LA, Wen FS, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Ann Rev Phytopathol 36:311–327

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Californian Agric Experiment Station Circ 347:1–39

    Google Scholar 

  • Horst WJ, Wagner A, Marschner H (1982) Mucilage protects root meristems from aluminium injury. Z Pflanzenphysio 105:435–444

    Article  CAS  Google Scholar 

  • Horst WJ, Püschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192:23–30

    Article  CAS  Google Scholar 

  • Iijima M, Morita S, Barlow PW (2008) Structure and function of the root cap. Plant Prod Sci 11:17–27

    Article  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry: principles and practices. Freeman and Co, London

    Google Scholar 

  • Kováčik J, Klejdus B, Hedbavny J, Bakor M (2010) Tolerance of Silene vulgaris to copper: population-related comparison of selected physiological parameters. Environ Toxicol 25:581–592

    Article  PubMed  Google Scholar 

  • Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    Article  Google Scholar 

  • Krzesłowska M, Lenartowska M, Samardakiewicz S, Bilski H, Wozny A (2010) Lead deposited in the cell wall of Funaria hygrometrica protonemata is not stable– a remobilization can occur. Environ Pollut 158:325–338

    Article  PubMed  Google Scholar 

  • Lequeux H, Hermans C, Lutts S, Verbruggen N (2010) Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile. Plant Physiol Biochem 48:673–682

    Article  CAS  PubMed  Google Scholar 

  • Llugany M, Lombini A, Poschenrieder C, Dinelli E, Barceló J (2003) Different mechanisms account for enhanced copper resistance in Silene armeria ecotypes from mine soil and serpentine sites. Plant Soil 251:55–63

    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 

  • Madejon P, Ramirez-Benitez JE, Corrales I, Barceló J, Poschenrieder C (2009) Copper-induced oxidative damage and enhanced antioxidant defenses in the root apex of maize cultivars differing in Cu tolerance. Env Exp Bot 67:415–420

    Article  CAS  Google Scholar 

  • Maksymiec W (1998) Effect of copper on cellular processes in higher plants. Photosynthetica 34:321–342

    Article  Google Scholar 

  • Martinka M, Lux A (2004) Response of roots of three populations of Silene dioica to cadmium treatment. Biologia 59:185–189

    CAS  Google Scholar 

  • Morel JL, Mench M, Guckert A (1986) Measurement of Pb2+, Cu2+ and Cd2+ binding with mucilage exudates from maize (Zea mays L.) roots. Biol Fert Soils 2:29–34

    Article  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM (2004) Root structural aspects associated with copper toxicity in oregano (Origanum vulgare subsp. hirtum). Plant Sci 166:1497–1504

    Article  CAS  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM, Karataglis S (2001) Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Ann Bot-London 88:207–214

    Article  CAS  Google Scholar 

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223

    Article  CAS  Google Scholar 

  • Pignattelli S, Colzi I, Buccianti A, Cecchi L, Arnetoli M, Monnanni R, Gabbrielli R, Gonnelli C (2012) Exploring element accumulation patterns of a metal excluder plant naturally colonizing a highly contaminated soil. J Haz Mat 227:362–369

    Article  Google Scholar 

  • Pignattelli S, Colzi I, Buccianti A, Cattani I, Beonec GM, Schat H, Gonnelli C (2013) A multielement analysis of Cu induced changes in the mineral profiles of Cu sensitive and tolerant populations of Silene paradoxa L. Environ Exp Bot 96:20–27

    Article  CAS  Google Scholar 

  • Pirselova B, Matuskova I (2013) Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiol Plant 35:635–644

    Article  CAS  Google Scholar 

  • Qin R, Hirano Y, Brunner I (2007) Exudation of organic acid anions from poplar roots after exposure to Al, Cu and Zn. Tree Physiol 27:313–320

    Article  CAS  PubMed  Google Scholar 

  • Samardakiewicz S, Krzesłowska M, Bilski H, Bartosiewicz R, Woźny A (2012) Is callose a barrier for lead ions entering Lemna minor L. root cells? Protoplasma 249:347–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki M, Yamamoto Y, Matsumoto H (1996) Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiol Plant 96:193–198

    Article  CAS  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    CAS  Google Scholar 

  • Sheldon AR, Menzies NW (2005) The effect of copper toxicity on the growth and root morphology of Rhodes grass (Chloris gayana Knuth.) in resin buffered solution culture. Plant Soil 278:341–349

    Article  CAS  Google Scholar 

  • Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maed T, Mori T, Volkmann D, Matsumoto H (2000) Al induced 1- to 3-b-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. a new mechanism of Al toxicity in plants. Plant Physiol 124:991–1005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith E, Naik D, Cumming JR (2011) Genotypic variation in aluminum resistance, cellular aluminum fractions, callose and pectin formation and organic acid accumulation in roots of Populus hybrids. Environ Exp Bot 72:182–193

    Article  CAS  Google Scholar 

  • Souza VL, de Almeida AAF, de Souza SJ, Mangabeira PAO, de Jesus RM, Pirovani CP, Ahnert D, Baligar VC, Loguercio LL (2014) Altered physiology, cell structure, and gene expression of Theobroma cacao seedlings subjected to Cu toxicity. Environ Sci Pollut Res 21:1217–1230

    Article  CAS  Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Tahara K, Norisada M, Hogetsu T, Kojima K (2005) Aluminum tolerance and aluminum-induced deposition of callose and lignin in the root tips of Melaleuca and Eucalyptus species. J Forest Res 10:325–333

    Article  CAS  Google Scholar 

  • Vaculík M, Lux A, Luxova M, Tanimoto E, Lichtscheidle I (2009) Silicon mitigates cadmium inhibitory effects in young maize plants. Environ Exp Bot 67:52–58

    Article  Google Scholar 

  • van de Mortel JE, Almar Villanueva L, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Loren V, van Themaat E, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    Article  PubMed Central  PubMed  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, Loren V, van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsitsiani S, Aarts MGM (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 31:301–324

    Article  PubMed  Google Scholar 

  • Willats WGT, McCartney L, Knox JP (2001) In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213(1):37–44

    Article  CAS  PubMed  Google Scholar 

  • Zelko I, Lux A (2004) Effect of cadmium on Karwinskia humboldtiana roots. Biologia 59:205–209

    CAS  Google Scholar 

Download references

Acknowledgments

University of Firenze (Fondi di Ateneo 2011-2013) funded this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessio Papini.

Additional information

Responsible Editor: Henk Schat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Colzi, I., Pignattelli, S., Giorni, E. et al. Linking root traits to copper exclusion mechanisms in Silene paradoxa L. (Caryophyllaceae). Plant Soil 390, 1–15 (2015). https://doi.org/10.1007/s11104-014-2375-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2375-3

Keywords

Navigation