Skip to main content
SpringerLink
Log in

Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants

  • Biotic and Abiotic Stress
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Responses induced by Cd exposure were assessed in tobacco seedlings (Nicotiana tabacum L.) using macro and molecular indices. The 100 μM of Cd exposure reduced the total dry weight and chlorophyll index of the seedlings as much as the genuine Fe-deficiency. Concentration of Fe in the shoots decreased, whereas that in the roots increased by the Cd exposure, especially in the apoplasmic space. It is probable that Cd interferes mainly with the step of Fe-translocation from the roots to shoots and this sets the upper-part of the plant in a state of Fe-deficiency. The Cd exposure coordinately increased the expressions of the exogenous and the endogenous Fe-deficiency responsive genes, HvIDS2 pro ::GUS, NtFRO1 and NtIRT1 in the roots. This is the first data to demonstrate the responses of Cd-inducible Fe-deficiency at a molecular level.

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

Abbreviations

CaMV:

Cauliflower Mosaic Virus

GUS:

β-glucuronidase

ICP:

inductively coupled plasma atomic emission spectrometer

MU:

methylumbelliferone

4-MUG:

4-methylumbelliferyl-d-glucuronide

References

  • Bienfait HF, Van den Briel W, Mesland-Mul NT (1985) Free space iron pools in roots. Generation and mobilization. Plant Physiol 78:596–600

    Article  PubMed  CAS  Google Scholar 

  • Cataldo DA, Garland TR, Wildumg RE (1983) Cadmium uptake kinetics in intact soybean plants. Plant Physiol 73:844–848

    PubMed  CAS  Google Scholar 

  • Chaney RL (1989) Kinetic of ferric chelate reduction by roots of iron-deficient peanut (Arachis hypogea). Acta Bot Neerl 38:155–163

    CAS  Google Scholar 

  • Chaney RL, White MC, Simon PW (1975) Plant uptake of heavy metals from sewage sludge applied to land. In: Proc. Int Natl Conf Munic Sludge Manage, Rockville, USA, pp 167–178

  • Christensen TH (1984) Cadmium soil absorption at low concentrations: I. Effect of time, cadmium load, pH and calcium. Water, Air Soil Pollut 21:105–114

    Article  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486

    Article  PubMed  CAS  Google Scholar 

  • Cohen CK, Norvell WA, Kochian LV (1997) Induction of the root cell plasma membrane ferric reductase. Plant Physiol 114:1061–1069

    PubMed  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  PubMed  CAS  Google Scholar 

  • Cohen CK, Garvin DF, Kochian LV (2004) Kinetic properties of a micronutrient transporter from Pisum sativum indicate a primary function in Fe uptake from the soil. Planta 218:784–792

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt U, Mas Marques A, Buckhout TJ (2001) Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants. Plant Mol Biol 45:437–448

    Article  PubMed  CAS  Google Scholar 

  • Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159

    Article  CAS  Google Scholar 

  • Garty J, Karay Y, Harel J (1992) Effect of low pH, heavy metals and anions an chlorophyll degradation in the lichen Ramalina duriaei (de not) Bagl. Environ Exp Bot 32:229–241

    Article  CAS  Google Scholar 

  • Gothberg A, Greger M, Holm K, Bengtsson BE (2004) Influence of nutrient levels on uptake and effects of mercury, cadmium, and lead in water spinach. J Environ Qual 33:1247–1255

    Article  PubMed  Google Scholar 

  • Greger M, Örgren E (1991) Direct and indirect effects of Cd2+ on photosysnthesis in suger beet (Beta Vulgaris). Physiol Plant 83:129–135

    Article  CAS  Google Scholar 

  • Grusak MA (1995) Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): Relevance to iron nutrition of developing seeds. Planta 197:111–117

    Article  CAS  Google Scholar 

  • Grusak MA, Kochian LV, Welch RM (1993) Spatial and temporal development of iron(III)-reductase activity through out the life cycle of iron-grown Pisum sativum L. (Fabaceae): Relevance to iron nutrition of developing seeds. Planta 197:111–117

    Google Scholar 

  • Grusak MA, Pezeshgi S (1996) Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol 110:329–334

    PubMed  CAS  Google Scholar 

  • Haghiri F (1973) Cadmium uptake by plants. J Environ Qual 2:93–96

    CAS  Google Scholar 

  • Hanikenne M, Kramer U, Demoulin V, Baurain D (2005) A comparative inventory of metal transporters in the green alga Chlamydomonas reinhardtii and the red alga Cyanidioschizon merolae. Plant Physiol 137:428–46

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    CAS  Google Scholar 

  • John MK (1976) Interrelationship between plant cadmium and uptake of some other elements from culture solutions by oat and lettuce. Environ Pollut 11:85–95

    Article  CAS  Google Scholar 

  • Kahle H (1993) Response of roots of trees to heavy metals. Environ Exp Bot 33:99–119

    Article  Google Scholar 

  • Kim Y-Y, Yang Y-Y, Lee Y (2002) Pb and Cd uptake in rice roots. Physiol Plant 116:368–372

    Article  CAS  Google Scholar 

  • Kobayashi T, Yoshihara T, Jiang T, Goto F, Nakanishi H, Mori S, Nishizawa NK (2003a) Combined deficiency of iron and other divalent cations mitigates the symptoms of iron deficiency in tobacco plants. Physiol Plant 119:400–408

    Article  CAS  Google Scholar 

  • Kobayashi T, Nakayama Y, Itai RN, Nakanishi H, Yoshihara T, Mori S, Nishizawa NK (2003b) Identification of novel cis-acting elements, IDE1 and IDE2, pf the barley IDS2 gene promoter conferring iron-deficiency-inducible, root-specific expression in heterogeneous tobacco plants. Plant J 36:780–793

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi T, Suzuki M, Inoue H, Nakanishi IR, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron-acquisition-related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency-responsive elements. J Exp Bot [e-pub, Mar 21, 2005]

  • Kochian LV (1991) Mechanisms of micronutrient uptake and translocation in plants. In: Mortvert JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture, 2nd edn., Soil Science Society of America, Madison, WI, pp 229–296

    Google Scholar 

  • Korshnova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  Google Scholar 

  • Krupa Z, Baszynski T (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus—direct and indirect effect on light and dark reactions. Acta Physiol Plant 17:177–190

    CAS  Google Scholar 

  • Lee S, Moon JS, Ko TS, Petros D, Goldsbrough PB, Korban SS (2003) Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiol 131:656–63

    Article  PubMed  CAS  Google Scholar 

  • Liu JG, Liang JS, Li KQ, Zhang ZJ, Yu BY, Lu XL, Yang JC, Zhu QS (2003) Correlations between cadmium and mineral nutrients in absorption and accumulation in various genotypes of rice under cadmium stress. Chemosphere 52:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Lombi E, Tearall KL, Howarth JR, Zhao F-J, 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  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd edn., Academic press, London, UK

    Google Scholar 

  • Michalska M, Asp H (2001) Influence of lead and cadmium on growth, heavy metal uptake and nutrient concentration of three lettuce cultivars grown in hydroponic culture. Commun Soil Sci Plant Anal 32:571–583

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nakanishi H, Yamaguchi H, Sasakuma T, Nishizawa NK, Mori S (2000) Two dioxygenase genes, Ids3 and IDS2, from Hordeum vulgare are involved in the biosynthesis of mugineic acid family phytosiderophores. Plant Mol Biol 44:199–207

    Article  PubMed  CAS  Google Scholar 

  • Okumura N, Nishizawa NK, Umehara Y, Ohata T, Nakanishi H, Yamaguchi H, Chino M, Mori S (1994) A dioxygenase gene (IDS2) expressed under Fe deficiency conditions in the roots of Hordeum vulgare. Plant Mol Biol 25:705–719

    Article  PubMed  CAS  Google Scholar 

  • Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54:291–301

    Article  PubMed  CAS  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    Article  PubMed  CAS  Google Scholar 

  • Römheld V (1987) Existence of two different strategies for the acquisition of iron in higher plants. In: Winelmann G, Van der Helm D, Neilands JB (eds) Iron transports in microbes, plants and animals. VCH Verlag, Weinheim, FRG pp 353–374

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  Google Scholar 

  • Siegel SM (1977) The cytotoxic response of `Nicotiana' protoplasts to metal ions: A survey of the chemical elements. Water Air Soil Pollut 8:293–304

    Article  CAS  Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxidases in chlorophyll degradation. Physiol Plant 85:85–89

    Article  CAS  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. Proc Natl Acad Sci USA 97:4991–4996

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Grotz N, Dedaldechamp 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  PubMed  CAS  Google Scholar 

  • Vert GA, Briat JF, Curie C (2003) Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol 132:796–804

    Article  PubMed  CAS  Google Scholar 

  • Wagner GJ, Sutton TG, Yeargan R (1988) Root control of leaf cadmium accumulation in tobacco. Tob Sci 32:88–91

    Google Scholar 

  • Wallace A, Romney EM, Alexander GV, Soufi SM, Patel PM (1977) Some interactions in plants among cadmium other heavy metals and chelating agents. Agron J 69:18–20

    Article  CAS  Google Scholar 

  • Welch RM (1995) Micronutrient nutrition of plants. Crit Rev Plant Sci 14:49–82

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yoshihara T, Kobayashi T, Goto F, Masuda T, Higuchi K, Nakanishi H, Nishizawa NK, Mori S (2003) Regulation of the Fe-deficiency responsive gene, IDS2 of barley in tobacco, Plant Biotech 20:33–41

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Prof. N.K. Nishizawa and S. Mori (The University of Tokyo) for providing the HvIDS2 gene promoter. This research was supported in part by a research grant from the Grant-in-aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS) to TY.

Author information

Authors and Affiliations

  1. Plant Molecular Biology, Laboratory for Environmental Science, Central Research Institute of Electric Power Industry, 1646 Abiko, Abiko, Chiba 270-1194, Japan

    Toshihiro Yoshihara, Hirotaka Hodoshima, Yoshiyuki Miyano, Kazuhiro Shoji & Fumiyuki Goto

  2. Plant Molecular Biology and Molecular Genetics, Department of Biological Science and Technology, Science University of Tokyo, Yamazaki 2641, Noda, Chiba, 278-8510, Japan

    Hirotaka Hodoshima, Yoshiyuki Miyano & Hiroaki Shimada

Authors
  1. Toshihiro Yoshihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirotaka Hodoshima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoshiyuki Miyano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuhiro Shoji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroaki Shimada
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fumiyuki Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Toshihiro Yoshihara.

Additional information

Communicated by P.P. Kumar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshihara, T., Hodoshima, H., Miyano, Y. et al. Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep 25, 365–373 (2006). https://doi.org/10.1007/s00299-005-0092-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-005-0092-3

Keywords

Search

Navigation