Skip to main content
SpringerLink
Log in

Modeling uptake of cadmium from solution outside of root to cell wall of shoot in rice seedling

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

It has long been recognized that the plasma membranes (PMs) play significant roles in the transport of ions across PMs, but kinetics of cadmium (Cd) transport between root and shoot via internal membrane system is not clear. Our experimental results showed that Cd2+ flux across the root PMs was well fitted by the Michaelis–Menten kinetics and the high-Cd-accumulation (HCA) variety displayed much higher maximum flux rate (Fmax) than the low-Cd-accumulation (LCA) variety. After Cd2+ was internalized, its flux into shoot PMs was linearly correlated with Cd2+ concentration in soluble fraction (FIII) of root cells. The efflux of Cd2+ across shoot PMs into cell wall was linearly correlated with Cd2+ concentration in shoot FIII. Only little amount of Cd2+ in cytosol was transported into organelles. The HCA variety displayed higher Cd2+ concentrations in FIII of root and shoot cells as well as higher Cd2+ flux rate by trans-cellular pathway than the LCA variety. However, efflux rate across shoot PMs to cell wall in the LCA variety was higher than that in the HCA variety. The low influx across PMs of root cells and high efflux across PMs of shoot cells probably are the special detoxification defense mechanisms of the LCA variety.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Barberon M, Geldner N (2014) Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiol 166:528–537

    Article  PubMed  PubMed Central  Google Scholar 

  • Benitez-Alfonso Y (2014) Symplastic intercellular transport from a developmental perspective. J Exp Bot 65:1857–1863

    Article  CAS  PubMed  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 Int 20(8):5665–5672

    Article  CAS  PubMed  Google Scholar 

  • Chen D, Xu Y, Zheng W, Huang D, Wong W, Tai WC, Cho Y, Lau ATY (2015) Proteomic analysis of secreted proteins by human bronchial epithelial cells in response to cadmium toxicity. Proteomics 15:3075–3086

    Article  CAS  PubMed  Google Scholar 

  • Degryse F, Shahbazi A, Verheyen L, Smolders E (2012) Diffusion limitations in root uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis constant. Plant Physiol 160:1097–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49:684–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erfurt C, Roussa E, Thèvenod F (2003) Apoptosis by Cd2+ or CDMT in proximal tubule cells: different uptake routes and permissive role of endo/lysosomal CdMT uptake. Am J Physiol Cell Physiol 285:C1367–C1376

    Article  CAS  PubMed  Google Scholar 

  • Etxeberria E, Pozueta-Romero J, Gonzalez P (2012) In and out of the plant storage vacuole. Plant Sci 190:52–61

    Article  CAS  PubMed  Google Scholar 

  • Fu HH, Luan S (1998) AtKUP1: a dual-affinity K+ transporter from Arabidopsis. The Plant Cell 10:63–73

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujimaki S, Suzui N, Ishioka NS, Kawachi N, Ito S, Chino M, Nakamura S (2010) Tracing cadmium from culture to spikelet: noninvasive imaging and quantitative characterization of absorption, transport, and accumulation of cadmium in an intact rice plant. Plant Physiol 152:1796–1806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halimaa P, Lin Y-F, Ahonen VH, Blande D, Clemens S, Gyenesei A, Häikiö E, Kärenlampi SO, Laiho A, Aarts MGM, Pursiheimo J-P, Schat H, Schmidt H, Tuomainen MH, Tervahauta AI (2014) Gene expression differences between noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109:19166–19171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ju X, Zhang C, Song Z, Han L, Lu Z, Wang J, Liu Z (2014) Changes in cadmium accumulation in rice organs during grain development and their relationship with genotype and cadmium levels in soil. Plant Physiol J 50:634–640

    CAS  Google Scholar 

  • Kerkhove EV, Pennemans V, Swennen Q (2010) Cadmium and transport of ions and substances across cell membranes and epithelia. Biometals 23:823–855

    Article  CAS  PubMed  Google Scholar 

  • Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi NI, Tanoi K, Hirose A, Nakanishi TM (2013) Characterization of rapid intervascular transport of cadmium in rice stem by radioisotope imaging. J Exp Bot 64:507–517

    Article  CAS  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 

  • Langelueddecke C, Lee WK, Thévenod F (2014) Differential transcytosis and toxicity of the hNGAL receptor ligandscadmium-metallothionein and cadmium-phytochelatin in colon-likeCaco-2 cells: implications for in vivo cadmium toxicity. Toxicol Lett 226:228–235

    Article  CAS  PubMed  Google Scholar 

  • Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199

    Article  CAS  PubMed  Google Scholar 

  • Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34:994–1008

    Article  CAS  PubMed  Google Scholar 

  • Petraglia A, Benedictis MD, Degola F, Pastore G, Calcagno M, Ruotolo R, Mengoni A, Toppi LS (2014) The capability to synthesize phytochelatins and the presence of constitutive and functional phytochelatin synthases are ancestral (plesiomorphic) characters for basal land plants. J Exp Bot 65:1153–1163

    Article  CAS  PubMed  Google Scholar 

  • Qiao X, Wang P, Shi G, Yang H (2015) Zinc conferred cadmium tolerance in Lemna minor L. via modulating polyamines and proline metabolism. Plant Growth Regul 77:1–9

    Article  CAS  Google Scholar 

  • Robbins NE II, Trontin C, Duan L, Dinneny JR (2014) Beyond the barrier: communication in the root through the endodermis. Plant Physiol 166:551–559

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Yamaji N, Ma JF (2014) Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65:6013–6021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagoto Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2012) Mutations in rice (Oryza sativa) heavy metal ATPase1 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224

    Article  CAS  PubMed  Google Scholar 

  • Siemianowski O, Barabasz A, Kendziorek M, Ruszczyńska A, Bulska E, Williams LE, Antosiewicz DM (2014) HMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J Exp Bot 65:1125–1139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh S, Prasad SM (2015) IAA alleviates Cd toxicity on growth, photosynthesis and oxidative damages in eggplant seedlings. Plant Growth Regul 77:87–98

    Article  CAS  Google Scholar 

  • Sterckeman T, Redjala T, Morel JL (2011) Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. Environ Exp Bot 74:131–139

    Article  CAS  Google Scholar 

  • Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62:4843–4850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107:16500–16505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno D, Koyama E, Yamaji N, Ma JF (2011) Physiological, genetic, and molecular characterization of a high-Cd-accumulating rice cultivar, Jarjan. J Exp Bot 62:2265–2272

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi S, Fujiwara T (2013) Rice breaks ground for cadmium-free cereals. Curr Opin Plant Biol 16:328–334

    Article  CAS  PubMed  Google Scholar 

  • Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA 108:20959–20964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Kinraide TB, Zhou D, Kopittke PM, Peijnenburg WJGM (2011) Plasma membrane surface potential: dual effects upon ion uptake and toxicity. Plant Physiol 155:808–820

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Gao Y, Feng Y, Li X, Wei Q et al (2014) Cadmium stress disrupts the endomembrane organelles and endocytosis during Picea wilsonii pollen germination and tube growth. PLoS ONE 9(4):e94721. doi:10.1371/journal.pone.0094721

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu H, Chen C, Du J, Liu H, Cui Y, Zhang Y, He Y, Wang Y, Chu C, Feng Z, Li J, Ling H-Q (2012) Co-overexpression FIT with AtbHLH38 or AtbHLH39 in Arabidopsis-enhanced cadmium tolerance via increased cadmium sequestration in roots and improved iron homeostasis of shoots. Plant Physiol 158:790–800

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Xiang Z, Zhu Y, Wang J, Yang Z, Yang Z (2013) Subcellular and molecular distribution of cadmium in two rice genotypes with different levels of cadmium accumulation. J Plant Nutr 35:71–84

    Article  CAS  Google Scholar 

  • Zelazny E, Vert G (2014) Plant nutrition: root transporters on the move. Plant Physiol 166:500–508

    Article  PubMed  PubMed Central  Google Scholar 

  • Zelazny E, Vert G (2015) Regulation of iron uptake by IRT1: endocytosis pulls the trigger. Mol Plant 8:977–979

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Chen Z, Zhu C (2012) Endogenous nitric oxide mediates alleviation of cadmium toxicity induced by calcium in rice seedlings. J Environ Sci 24:940–948

    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 

  • Zwiewka M, Nodzynski T, Robert S, Vanneste S, Friml J (2015) Osmotic stress modulates the balance between exocytosis and Clathrin-mediated endocytosis in Arabidopsis thaliana. Mol Plant 8:1175–1187

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work has been jointly financed by Funds for Science and Technology Innovation Project from the Chinese Academy of Agricultural Sciences and The Special Fund for Agro-scientific Research in the Public Interest (Grant No. 201403015). We thank Dr. Changrong Wang for manuscript editing.

Author information

Authors and Affiliations

  1. Agro-Environmental Protection Institute, Ministry of Agriculture, Tianjin, 300191, China

    Yanling Zhao, ShenJun Zhang, Na Wen, Changbo Zhang & Zhongqi Liu

  2. College of Life Sciences, Tianjin Normal University, Tianjin, 300384, China

    ShenJun Zhang, Na Wen & Jingan Wang

Authors
  1. Yanling Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. ShenJun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Na Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Changbo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jingan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhongqi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongqi Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Zhang, S., Wen, N. et al. Modeling uptake of cadmium from solution outside of root to cell wall of shoot in rice seedling. Plant Growth Regul 82, 11–20 (2017). https://doi.org/10.1007/s10725-016-0233-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-016-0233-4

Keywords

Search

Navigation