Skip to main content

Advertisement

SpringerLink
Log in

Iron supply prevents Cd uptake in Arabidopsis by inhibiting IRT1 expression and favoring competition between Fe and Cd uptake

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

Abstract

Background and aims

Cadmium (Cd) is a heavy metal that is highly toxic to organisms. Studies have shown that an increasing Fe supply decreases Cd accumulation in plants. In this study, we investigated the mechanism underlying the effect of Fe on Cd uptake.

Methods

We compared the effects of Fe application on Cd levels in wild-type Arabidopsis thaliana Col-0 and IRT1-null mutant irt1 (loss in function of Fe2+ uptake).

Results

In the Fe-Cd alternative rotation treatment, which ensured asynchronous uptake of Fe2+ and Cd2+, the irt1 mutants had a lower Cd level than the Col-0 plants. In addition, an increase in the Fe supply decreased the Cd level in Col-0 plants, accompanied by an inhibition of IRT1 expression in roots. Furthermore, both Col-0 and irt1 plants grown in Fe-Cd alternative rotation treatment, showed higher Cd uptake than those grown in another rotation treatment, which allowed synchronous uptake of Fe2+ and Cd2+. Nevertheless, the differences in Cd uptake between the two rotation treatments were greater in Col-0 plants than in irt1 mutants.

Conclusions

Inhibition of IRT1-mediated Cd uptake and enhancement of antagonism between Fe and Cd uptake are two mechanisms involved in the inhibition of Cd uptake by Fe supply.

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

Similar content being viewed by others

References

  • Bughio N, Yamaguchi H, Nishizawa NK, Nakanishi H, Mori S (2002) Cloning an iron-regulated metal transporter from rice. J Exp Bot 53:1677–1682

    Article  CAS  PubMed  Google Scholar 

  • Chen HM, Zheng CR, Tu C, Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99

    Article  CAS  PubMed  Google Scholar 

  • Clemens S, Antosiewicz DM, Ward JM, Schachtman DP, Schroeder JI (1998) The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast. P Natl Acad Sci USA 95:12043–12048

    Article  CAS  Google Scholar 

  • Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280

    Article  CAS  PubMed  Google Scholar 

  • Das P, Samantaray S, Rout GR (1997) Studies on cadmium toxicity in plants: a review. Environ Pollut 98:29–36

    Article  CAS  PubMed  Google Scholar 

  • Di Toppi LS, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105–130

    Article  CAS  Google Scholar 

  • Fan SK, Fang XZ, Guan MY, Ye YQ, Lin XY, Du ST, Jin CW (2014) Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5:1–8

    Article  CAS  Google Scholar 

  • Fang XZ, Tian WH, Liu XX, Lin XY, Jin CW, Zheng SJ (2016) Alleviation of proton toxicity by nitrate uptake specifically depends on nitrate transporter 1.1 in Arabidopsis. New Phytol 211:149–158

    Article  CAS  PubMed  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JH et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Fukao Y, Ferjani A, Tomioka R, Nagasaki N, Kurata R, Nishimori Y, Fujiwara M, Maeshima M (2011) iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiol 155:1893–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerinot ML (2000) The ZIP family of metal transporters. BBA-Biomembranes 1465:190–198

    Article  CAS  PubMed  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Wang NS, Hu XJ, Lin XY, Feng Y, Jin CW (2013) Nitrate nutrition enhances nickel accumulation and toxicity in Arabidopsis plants. Plant Soil 371:105–115

    Article  CAS  Google Scholar 

  • Jeong J, Guerinot ML (2009) Homing in on iron homeostasis in plants. Trends Plant Sci 14:280–285

    Article  CAS  PubMed  Google Scholar 

  • Jin CW, Du ST, Chen WW et al (2009) Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato. Plant Physiol 150:272–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin CW, Mao QQ, Luo BF, Lin XY, Du ST (2013) Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress. Plant Soil 371:387–396

    Article  CAS  Google Scholar 

  • Khan FI, Husain T, Hejazi R (2004) An overview and analysis of site remediation technologies. J Environ Manag 71:95–122

    Article  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Ma Z, van der Kuijp TJ, Yuan Z, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853

    Article  PubMed  Google Scholar 

  • Lin XY, Ye YQ, Fan SK, Jin CW, Zheng SJ (2016) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiol 170:907–920

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Zhou Q, An J, Sun Y, Liu R (2010) Variations in cadmium accumulation among Chinese cabbage cultivars and screening for Cd-safe cultivars. J Hazard Mater 173:737–743

    Article  CAS  PubMed  Google Scholar 

  • Lombi E, Tearall KL, Howarth JR, Zhao FJ, Hawkesford MJ, McGrath SP (2002) Influence of iron status on cadmium and zinc uptake by different ecotypes of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 128:1359–1367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Song S, Wang RT et al (2015) Impacts of soil and water pollution on food safety and health risks in China. Environ Int 77:5–15

    Article  CAS  PubMed  Google Scholar 

  • Luo BF, Du ST, Lu KX, Liu WJ, Lin XY, Jin CW (2012) Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. J Exp Bot 63:3127–3136

    Article  CAS  PubMed  PubMed Central  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 

  • Mao QQ, Guan MY, Lu KX, Du ST, Fan SK, Ye YQ, Lin XY, Jin CW (2014) Inhibition of nitrate transporter 1.1-controlled nitrate uptake reduces cadmium uptake in Arabidopsis. Plant Physiol 166:934–944

    Article  PubMed  PubMed Central  Google Scholar 

  • Meharg AA, Norton G, Deacon C et al (2013) Variation in rice cadmium related to human exposure. Environ Sci Technol 47:5613–5618

    Article  CAS  PubMed  Google Scholar 

  • Mendoza-Cózatl DG, Jobe TO, Hauser F, Schroeder JI (2011) Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol 14:554–562

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendoza-Cózatl DG, Xie Q, Akmakjian GZ et al (2014) OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds. Mol Plant 7:1455–1469

    Article  PubMed  PubMed Central  Google Scholar 

  • MEP&MLR (Ministry of Environment Protection and Ministry of Land Resources of the People’s Republic of China) (2014) Nationwide soil pollution survey report. Ministry of Environment Protection and Ministry of Land Resources of the People’s Republic of China

  • Muehe EM, Adaktylou IJ, Obst M, Zeitvogel F, Behrens S, Planer-Friedrich B, Kraemer U, Kappler A (2013) Organic carbon and reducing conditions lead to cadmium immobilization by secondary Fe mineral formation in a pH-neutral soil. Environ Sci Technol 47:13430–13439

    Article  CAS  PubMed  Google Scholar 

  • Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52:464–469

    Article  CAS  Google Scholar 

  • Nightingale ER Jr (1959) Phenomenological theory of ion solvation. Effective radii of hydrated ions. J Phys Chem 63:1381–1387

    Article  CAS  Google Scholar 

  • Niu Y, Jin C, Jin G, Zhou Q, Lin X, Tang C, Zhang Y (2011) Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh. under elevated CO2. Plant Cell Environ 34:1304–1317

    Article  CAS  PubMed  Google Scholar 

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  CAS  PubMed  Google Scholar 

  • Rodecap KD, Tingey DT, Lee EH (1994) Iron nutrition influence on cadmium accumulation by Arabidopsis thaliana (L.) Heynh. J Environ Qual 23:239–246

    Article  CAS  Google Scholar 

  • Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937

    CAS  PubMed  Google Scholar 

  • Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wirén N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Kumar R, Schroeder JI, Marsh EL (1997) Molecular and functional characterization of a novel low-affinity cation transporter (LCT1) in higher plants. P Natl Acad Sci USA 94:11079–11084

    Article  CAS  Google Scholar 

  • Shao G, Chen M, Wang W, Mou R, Zhang G (2007) Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regul 53:33–42

    Article  CAS  Google Scholar 

  • Sharma SS, Kaul S, Metwally A, Goyal KC, Finkemeier I, Dietz KJ (2004) Cadmium toxicity to barley (Hordeum vulgare) as affected by varying Fe nutritional status. Plant Sci 166:1287–1295

    Article  CAS  Google Scholar 

  • Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, 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 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. P Natl Acad Sci USA 97:4991–4996

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:364–372

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, Briat JF, Curie C (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker WM, Miller JE, Hassett JJ (1977) Effect of lead and cadmium upon the calcium, magnesium, potassium, and phosphorus concentration in young corn plants. Soil Sci 124:145–151

    Article  CAS  Google Scholar 

  • Welch RM, Norvell WA, Schaefer SC, Shaff JE, Kochian LV (1993) Induction of iron (III) and copper (II) reduction in pea (Pisum sativum L.) roots by Fe and Cu status: does the root-cell plasmalemma Fe (III)-chelate reductase perform a general role in regulating cation uptake? Planta 190:555–561

    Article  CAS  Google Scholar 

  • Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe (III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844

    Article  CAS  PubMed  Google Scholar 

  • Zhai Z, Gayomba SR, Jung HI et al (2014) OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis. Plant Cell 26:2249–2264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Natural Science Foundation of China (31622051 and 31670258), the National Key Research and Development Program (2016YFD0200103), and the Zhejiang Province Natural Science Foundation (LR13C130001).

Author information

Authors and Affiliations

  1. State Key Laboratory of Plant Physiology and Biochemistry, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, China

    Xiao Lin He, Shi Kan Fan, Jun Zhu, Mei Yan Guan, Xing Xing Liu, Yong Song Zhang & Chong Wei Jin

Authors
  1. Xiao Lin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shi Kan Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei Yan Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xing Xing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yong Song Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chong Wei Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chong Wei Jin.

Additional information

Responsible Editor: Jian Feng Ma.

Electronic supplementary material

ESM 1

(DOCX 130 kb)

ESM 2

(DOCX 199 kb)

ESM 3

(DOCX 189 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, X.L., Fan, S.K., Zhu, J. et al. Iron supply prevents Cd uptake in Arabidopsis by inhibiting IRT1 expression and favoring competition between Fe and Cd uptake. Plant Soil 416, 453–462 (2017). https://doi.org/10.1007/s11104-017-3232-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3232-y

Keywords

Search

Navigation