Skip to main content
Log in

Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The physiological and molecular mechanisms leading to the competitive interactions between phosphorus (P) and metal elements are a matter of debate. In this study, we found that P deficiency can alleviate cadmium (Cd) toxicity in Arabidopsis thaliana (Col-0). Under P deficiency (−P), less Cd was accumulated in the plants and the root cell walls, indicating the operation of a P-deficiency-induced Cd exclusion mechanism. However, organic acid efflux was similar under −P+Cd and +Cd treatments, suggesting that organic acid efflux is not responsible for the Cd exclusion. Interestingly, P deficiency significantly decreased cell wall polysaccharides (pectin and hemicellulose) contents and pectin methylesterase activity, and decreased the Cd retained by the extracted root cell wall. Therefore, we conclude that the modification of cell wall composition is responsible for the Cd exclusion of the root under P deficiency.

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
Fig. 7

Similar content being viewed by others

Abbreviations

Cd:

Cadmium

P:

Phosphorus

PME:

Pectin methylesterase

HC1:

Hemicellulose 1

SPAD:

Soil plant analysis development

MDA:

Malondialdehyde

CK:

Control check

AO:

Alcohol oxidase

TBA:

Thiobarbituric acid

TFA:

Trifluoroacetic acid

References

  • Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeonpea and its role in cropping systems of Indian subcontinent. Science 248:477–480

    Article  PubMed  CAS  Google Scholar 

  • Ae N, Otani T, Makino T, Tazawa J (1996) Role of cell wall of groundnut roots in solubilizing sparingly soluble phosphorus in soil. Plant Soil 186:197–204

    Article  CAS  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) An improved method for the assay of hydroxylysine. Anal Biochem 56:10–15

    Article  PubMed  CAS  Google Scholar 

  • Carrier P, Baryla A, Havaux M (2003) Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmium-contaminated soil. Planta 216:939–950

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Douchiche O, Driouich A, Morvan C (2010) Spatial regulation of cell-wall structure in response to heavy metal stress: Cadmium induced alteration of the methyl-esterification pattern of homogalacturonans. Ann Bot 105:481–491

    Article  PubMed  CAS  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Gardner WK, Barber DA, Parberry DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in soil/root interface is enhanced. Plant Soil 70:107–124

    Article  CAS  Google Scholar 

  • Gessa C, Deiana S, Premoli A, Ciurli A (1997) Redox activity of caffeic acid towards iron (III) complexed in a polygalacturonate network. Plant Soil 190:289–299

    Article  CAS  Google Scholar 

  • Hall JL (1969) Histochemical localization of β-glycerophosphatase activity in young root tips. Ann Bot 33:399–406

    CAS  Google Scholar 

  • Hirsch J, Marin E, Floriani M, Chiarenza S, Richaud P, Nussaume L, Thibaud MC (2006) Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88:1767–1771

    Article  PubMed  CAS  Google Scholar 

  • Lee RB (1982) Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Ann Bot 50:429–449

    CAS  Google Scholar 

  • Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol 85:315–317

    Article  PubMed  CAS  Google Scholar 

  • Lozano-Rodríguez E, Hernández LE, Bonay P, Carpena RO (1997) Distribution of Cd in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48:123–128

    Article  Google Scholar 

  • Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97:46–51

    Article  PubMed  CAS  Google Scholar 

  • Meharg AA, Macnair MR (1992) Suppression of the high-affinity phosphate-uptake system: a mechanism of arsenate tolerance on Holcus lanatus L. J Exp Bot 43:519–524

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–496

    Article  CAS  Google Scholar 

  • Nagarajah S, Posner AM, Quirk JP (1970) Competitive adsorption of phosphate with polygalacturonate and other organic anions on kaolinate and oxide surface. Nature 228:83–84

    Article  PubMed  CAS  Google Scholar 

  • Nishizona H, Zchikawa H, Suzuki S, Ishii F (1987) The role of the root cell wall in heavy metal tolerance of Athyrium yokosense. Plant Soil 101:15–20

    Article  Google Scholar 

  • Øbro J, Harholt J, Scheller HV, Orfila C (2004) Rhamnogalacturonan I in Solanum tuberosum tubers contains complex arabinogalactan structures. Phytochemistry 65:1429–1438

    Article  PubMed  Google Scholar 

  • Otani T, Ae N, Tanaka H (1996) (P) uptake mechanisms of crop grown in soils with low P status. II. Significance of organic acids in root exudates of pigeonpea. Soil Sci Plant Nutr 42:533–560

    Google Scholar 

  • Pammenter NW, Woolhouse HW (1975) The utilization of P–N compounds by plants. II. The role of extracellular root phosphatases. Ann Bot 39:347–361

    CAS  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  PubMed  CAS  Google Scholar 

  • Sample EC, Soper RJ, Racz GJ (1980) Reaction of phosphate fertilizer in souls. In: Khasawneh FE, Sample EC, Kamprath EJ (eds) The role of phosphorus in agriculture. American Society of Agronomy, Madison, pp 263–310

    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 

  • Tewari RK, Kumar P, Sharma PN (2006) Antioxidant responses to enhanced generation of superoxide anion radical and hydrogen peroxide in the copper-stressed mulberry plants. Planta 223:1145–1153

    Article  PubMed  CAS  Google Scholar 

  • Vázquez S, Goldsbrough P, Carpena RO (2006) Assessing the relative contributions of phytochelatins and the cell wall to cadmium resistance in white lupin. Physiol Plant 128:487–495

    Article  Google Scholar 

  • Wagner GJ (1993) Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51:173–212

    Article  CAS  Google Scholar 

  • Wang JR, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Liu YG, Zeng GM, Chai LY, Song XC, Min ZY, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) Guad. Environ Exp Bot 63:389–395

    Article  Google Scholar 

  • Yan F, Zhu Y, Müller C, Zörb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots white lupin under phosphate deficiency. Plant Physiol 129:50–63

    Article  PubMed  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  CAS  Google Scholar 

  • Yang ZB, Eticha D, Rao IM, Horst WJ (2010) Alteration of cell-wall porosity is involved in osmotic stress-induced enhancement of aluminium resistance in common bean (Phaseolus vulgaris L.). J Exp Bot 61:3245–3258

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zheng LQ, Huang FL, Narsai R, He F, Giraud E, Wu JJ, Cheng LJ, Wang F, Wu P, Whelan J, Shou HX (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151:262–274

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zhu Y, Yan F, Zörb C, Schubert S (2005) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions? Plant Cell Physiol 46:892–901

    Article  PubMed  CAS  Google Scholar 

  • Zhu XF, Zheng C, Hu YT, Jiang T, Liu Y, Dong NY, Yang JL, Zheng SJ (2011) Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant Cell Environ 34:1055–1064

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Changjiang Scholarship and Changjiang Innovation Team (IRT1185), Natural Science Foundation of China (No. 30830076), and the Fundamental Research Funds for the Central Universities. We thank Yun Rong Wu for providing the P deficient acidic soil. Thanks are also given to three anonymous reviewers for their valuable comments and suggestions to improve the quality of the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gui Xin Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhu, X.F., Lei, G.J., Jiang, T. et al. Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana . Planta 236, 989–997 (2012). https://doi.org/10.1007/s00425-012-1652-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1652-8

Keywords

Navigation