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Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii

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Abstract

Background and aims

The role of polysaccharide modification in metal accumulation in hyperaccumulators is still unknown. Our aim was to compare the differences in the role of root cell-wall polysaccharides in cadmium (Cd) accumulation between hyperaccumulating (HE) and non-hyperaccumulating ecotype (NHE) of Sedm alfredii.

Methods

Hydroponic experiments were performed to characterize root-to-shoot Cd translocation, cadmium species and polysaccharide modification in root cell-wall of S. alfredii using stable isotope tracing, X-ray absorption near edge structure and immunofluorescence localization techniques.

Results

Cd absorbed was more readily available for transport to the shoots by the HE roots than by the NHE roots, which is confirmed by a 6-fold higher 113Cd concentration in xylem sap. Root Cd efflux originated mainly from the cell walls. The concentration of cell-wall polysaccharides and activity of pectin methylesterase were higher in the NHE than in the HE in the absence of Cd, and even higher in the presence of Cd. More pectins were methylated in the HE than in the NHE, indicating more free pectic acid residues in the NHE. The cell-wall-bound Cd was retained more tightly in the NHE than in the HE.

Conclusions

Cadmium hyperaccumulation by HE of S. alfredii is associated with its enhanced Cd flux into the xylem, which is partly regulated by cell-wall polysaccharide modification in roots.

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Abbreviations

Cd:

Cadmium

HC1:

Hemicellulose 1

HC2:

Hemicellulose 2

HE:

Hyperaccumulating ecotype

ICP-MS:

Inductively coupled plasma mass spectrometry

LCF:

Linear-combination fitting

NHE:

Non-hyperaccumulating ecotype

PME:

Pectin methylesterase

XANES:

X-ray absorption near edge structure

References

  • Bernard C, Roosens N, Czernic P, Lebrun M, Verbruggen N (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148

    Article  CAS  PubMed  Google Scholar 

  • Bert V, Bonnin I, Saumitou-Laprade P, de Laguerie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    Article  CAS  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative-determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  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 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Courbot M, Willems G, Motte P, Arvidsson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Douchiche O, Rihouey C, Schaumann A, Driouich A, Morvan C (2007) Cadmium-induced alterations of the structural features of pectins in flax hypocotyl. Planta 225:1301–1312

    Article  CAS  PubMed  Google Scholar 

  • Ebbs SD, Zambrano MC, Spiller SM, Newville M (2009) Cadmium sorption, influx, and efflux at the mesophyll layer of leaves from ecotypes of the Zn/Cd hyperaccumulator Thlaspi caerulescens. New Phytol 181:626–636

    Article  CAS  PubMed  Google Scholar 

  • Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting P-IB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136(3):3712–3723

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ 28:1410–1420

  • Gao J, Sun L, Yang XE, Liu JX (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS ONE 8(6):e64643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    Article  CAS  PubMed  Google Scholar 

  • Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Environ Exp Bot 72:53–63

    Article  CAS  Google Scholar 

  • Krzeslowska 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  CAS  Google Scholar 

  • Krzeslowska 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  CAS  PubMed  Google Scholar 

  • Lasat MM, Baker AJM, Kochian LV (1998) Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens. Plant Physiol 118:875–883

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li TQ, Yang XE, Meng FH, Lu LL (2007) Zinc adsorption and desorption characteristics in root cell wall involving zinc hyperaccumulation in Sedum alfredii Hance. J Zhejiang Univ Sci B 8:111–115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li TQ, Tao Q, Liang CF, Shohag MJI, Yang XE, Sparks DL (2013) Complexation with dissolved organic matter and mobility control of heavy metals in the rhizosphere of hyperaccumulator Sedum alfredii. Environ Pollut 182:248–255

    Article  CAS  PubMed  Google Scholar 

  • Lu LL, Tian SK, Yang XE, Wang XC, Brown P, Li TQ, He ZL (2008) Enhanced root-to-shoot translocation of cadmium in the hyperaccumulating ecotype of Sedum alfredii. J Exp Bot 59:3203–3213

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu LL, Tian SK, Zhang J, Yang X, Labavitch JM, Webb SM, Latimer M, Brown PH (2013) Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii. New Phytol 198:721–731

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419

    Article  CAS  PubMed  Google Scholar 

  • Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P-1B-ATPase allowing Cd/Zn/Co/Pb vacuolar sorage in Arabidopsis. Plant Physiol 149(2):894–904

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mori S, Kawasaki A, Ishikawa S, Arao T (2009) A new method for evaluating symplastic cadmium absorption in the roots of Solanum melongena using enriched isotopes 113Cd and 114Cd. Soil Sci Plant Nutr 55:294–299

    Article  CAS  Google Scholar 

  • Ni TH, Wei YZ (2003) Subcellular distribution of cadmium in mining ecotype Sedum alfredii. Acta Bot Sin 45:925–928

    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 

  • Nyquist J, Greger M (2007) Uptake of Zn, Cu, and Cd in metal loaded Elodea canadensis. Environ Exp Bot 60:219–226

    Article  CAS  Google Scholar 

  • Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  CAS  PubMed  Google Scholar 

  • Pence NS, Larsen PB, Ebbs SD, Letham DBL, Lasat MM, Garvin DF, Eide D, Kochian LV (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci U S A 97:4956–4960

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56

    Article  CAS  Google Scholar 

  • Schmohl N, Pilling J, Fisahn J, Horst WJ (2000) Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol Plant 109:419–427

    Article  CAS  Google Scholar 

  • Shi Z, Di Toro DM, Allen HE, Sparks DL (2008) A WHAM-based kinetics model for Zn adsorption and desorption to soils. Environ Sci Technol 42:5630–5636

    Article  CAS  PubMed  Google Scholar 

  • Sousa AI, Cacador I, Lillebo AI, Pardal MA (2008) Heavy metal accumulation in Halimione portulacoides: intra- and extra-cellular metal binding sites. Chemosphere 70:850–857

    Article  CAS  PubMed  Google Scholar 

  • Tang YT, Qiu RL, Zeng XW, Fang XH, Yu FM, Zhou XY, Wu YD (2009) Zn and Cd hyperaccumulating characteristics of Picris divaricata Vant. Int J Environ Pollut 38:26–38

    Article  Google Scholar 

  • Tian SK, Lu LL, Yang XO, Webb SM, Du YH, Brown PH (2010) Spatial imaging and speciation of lead in the accumulator plant Sedum alfredii by microscopically focused synchrotron X-ray investigation. Environ Sci Technol 44:5920–5926

    Article  CAS  PubMed  Google Scholar 

  • Tian SK, Lu LL, Labavitch J, Yang XE, He ZL, Hu HN, Sarangi R, Newville M, Commisso J, Brown P (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157:1914–1925

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tsednee M, Yang SC, Lee DC, Yeh KC (2014) Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiol 166:839–852

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ueno D, Milner MJ, Yamaji N, Yokosho K, Koyama E, Clemencia Zambrano M, Kaskie M, Ebbs S, Kochian LV, Ma JF (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi S, Kiyono M, Sakamoto T, Watanabe I, Kuno K (2009) Contributions of apoplasmic cadmium accumulation, antioxidative enzymes and induction of phytochelatins in cadmium tolerance of the cadmium-accumulating cultivar of black oat (Avena strigosa Schreb.). Planta 230:267–276

    Article  CAS  PubMed  Google Scholar 

  • van de Mortel JE, Schat H, Moerland PD, Loren V, van Themaat E, van der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MG (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 

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

    Article  CAS  PubMed  Google Scholar 

  • Vogel-Mikus K, Drobne D, Regvar M (2005) Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ Pollut 133:233–242

    Article  CAS  PubMed  Google Scholar 

  • Vollenweider P, Cosio C, Guenthardt-Goerg MS, Keller C (2006) Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.) Part II Microlocalization and cellular effects of cadmium. Environ Exp Bot 58:25–40

    Article  CAS  Google Scholar 

  • Webb SM (2005) SIXpack: a graphical user interface for XAS analysis using IFEFFIT. Phys Scr 115:1011–1014

    Article  Google Scholar 

  • Wei L, Shu WS, Lan CY (2004) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin Sci Bull 49:29–32

    Article  Google Scholar 

  • Wei SH, Zhou QX, Wang X, Zhang KS, Guo GL, Ma QYL (2005) A newly-discovered Cd-hyperaccumulator Solanum nigrum L. Chin Sci Bull 50:33–38

    Article  CAS  Google Scholar 

  • White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899

  • Wierzbicka M (1998) Lead in the apoplast of Allium cepa L. root tips ultrastructural studies. Plant Sci 133:105–119

    Article  CAS  Google Scholar 

  • Willats WGT, Knox JP, Mikkelsen JD (2006) Pectin: new insights into an old polymer are starting to gel. Trends Food Sci Technol 17:97–104

    Article  CAS  Google Scholar 

  • Xiong J, Lu H, Lu KX, Duan YX, An LY, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610

    Article  CAS  PubMed  Google Scholar 

  • Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189

    Article  CAS  Google Scholar 

  • Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155:1885–1892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654

    Article  CAS  PubMed  Google Scholar 

  • Zhong HL, Lãuchli A (1993) Changes of cell-wall composition and polymer size in primary roots of cotton seedlings under high salinity. J Exp Bot 44:773–778

    Article  CAS  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 236:989–997

    Article  CAS  PubMed  Google Scholar 

  • Zhu QH, Huang DY, Liu SL, Luo ZC, Rao ZX, Cao XL, Ren XF (2013) Accumulation and subcellular distribution of cadmium in ramie (Boehmeria nivea L. Gaud.) planted on elevated soil cadmium contents. Plant Soil Environ 59:57–61

    CAS  Google Scholar 

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Acknowledgments

This study was financially supported by the National Natural Science Foundation of China (41271333, 21477104), and the National Key Technology R&D Program of China (2012BAC17B04). Portions of this work were performed at Beamline 11-2, Stanford Synchrotron Radiation Laboratory (SSRL), Stanford, USA. The monoclonal antibodies specific for pectins (JIM5 and JIM7) were purchased from CarboSource Services of University of Georgia. The authors are grateful to Prof. Dr. Hans Lambers of the University of Western Australia for his instructive comments on and critical reading of this manuscript. We thank the anonymous reviewers for their valuable comments and suggestions.

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Authors and Affiliations

  1. Ministry of Education Key Laboratory of Environmental Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, China

    Tingqiang Li, Qi Tao, Md Jahidul Islam Shohag, Xiaoe Yang & Yongchao Liang

  2. Department of Plant and Soil Sciences, University of Delaware, Newark, DE, 19717, USA

    Donald L. Sparks

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  1. Tingqiang Li
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  2. Qi Tao
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  3. Md Jahidul Islam Shohag
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  4. Xiaoe Yang
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  5. Donald L. Sparks
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  6. Yongchao Liang
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Correspondence to Yongchao Liang.

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Responsible Editor: Juan Barcelo.

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Li, T., Tao, Q., Shohag, M.J.I. et al. Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii . Plant Soil 389, 387–399 (2015). https://doi.org/10.1007/s11104-014-2367-3

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  • DOI: https://doi.org/10.1007/s11104-014-2367-3

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