Skip to main content

Advertisement

SpringerLink
Log in

Transcriptional and physiological changes in relation to Fe uptake under conditions of Fe-deficiency and Cd-toxicity in roots of Vigna radiata L.

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

We investigated transcriptional and physiological changes in relation to Fe transport and uptake under various conditions of iron (Fe)-deficiency and cadmium (Cd) toxicity. Responses to four such Fe/Cd conditions were evaluated, revealing that oxidative stress was generated in the presence of Cd, followed by a decrease in Fe and an increase in Cd concentrations in green gram (Vigna radiata) material, whereas supplementation with Fe had a protective effect against Cd toxicity. The involvement of enzymes in Fe-uptake for the formation of root-nodules was largely reduced in the presence of Cd toxicity, a condition recovered by Fe-supplementation. Insufficient ferric chelate reducing activity in Fe-deprived roots in the presence of Cd was also largely improved by Fe supplementation. The expression of Fe2+ transporters (IRT1, IRT2, and IRT3), Fe(III) chelate reductase (FRO1–FRO8) and phytochelatin synthase (PCS1, PCS2 and PCS3) genes was up regulated for the first 5 days and decreased after 10 days in roots in the presence of Cd toxicity, but was sustained with Fe-supplementation. Additionally, root biomass was fully recovered in plants in the presence of Fe during Cd toxicity. Our results suggest that Fe-status plays a significant role in ameliorating the damage in Fe transport for chelation and its uptake caused by Cd toxicity. This supports the hypothesis that leguminous plants, particularly those that are sensitive to Fe such as green gram, can cope to some extent with Cd toxicity by improving the uptake and transport of Fe.

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

IRTs :

Iron regulated transporter

FROs :

Ferric reductase oxidase

PCS :

Phytochelatin synthase

Lb:

Leghemoglobin

References

  • Ali MB, Hahn EJ, Paek KY (2005) Effects of temperature on oxidative stress defense systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis. Plant Physiol Biochem 43:213–223

    Article  PubMed  CAS  Google Scholar 

  • Astolfi S, Zuchi S, Neumann G, Cesco S, Sanita di Toppi L, Pinton R (2012) Response of barley to Fe deficiency and Cd contamination as affected by S starvation. J Exp Bot 63:1241–1250

    Article  PubMed  CAS  Google Scholar 

  • Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cohen CK, Gravin 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 transcript and protein accumulation. Plant Cell 14:1347–1357

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110

  • Curie C, Briat JF (2003) Iron transport and signaling in plants. Annu Rev Plant Biol 54:183–206

    Article  PubMed  CAS  Google Scholar 

  • Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93:5624–5628

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci USA 84:439–443

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guerinot ML (2001) Improving rice yields—ironing out the details. Nature Biotechnol 19:417–418

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free Radicals in Biology and Medicine. Oxford University Press, New York

    Google Scholar 

  • Hashem HA (2013) Cadmium toxicity induces lipid peroxidation and alters cytokinin content and antioxidant enzyme activities in soybean. Botany 92:1–7

    Article  Google Scholar 

  • Heiss S, Wachter A, Bogs J, Cobbett C, Rausch T (2003) Phytochelatin synthase (PCS) protein induced in Brassica juncea leaves after prolonged Cd exposure. J Exp Bot 54:1833–1839

    Article  PubMed  CAS  Google Scholar 

  • Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551

    PubMed  CAS  Google Scholar 

  • Kerkeb L, Mukherjee I, Chatterjee I, Lahner B, Salt DE, Connolly EL (2008) Iron-induced turnover of the Arabidopsis IRON-REGULATED TRANSPORTER1 metal transporter requires lysine residues. Plant Physiol 146:1964–1973

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kobayashi K, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron acquisition related genes in iron deficient rice is coordinately induced by partially conserved iron-deficiency responsive elements. J Exp Bot 56:1305–1316

    Article  PubMed  CAS  Google Scholar 

  • Korshunova 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  PubMed  CAS  Google Scholar 

  • Krouma A, Abdelly C (2003) Importance of iron use efficiency in common bean (Phaseolus vulgaris L.) for iron chlorosis resistance. J Plant Nutr Soil Sci 4:525–528

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • LaRue TA, Child JJ (1979) Sensitive fluorometric assay for leghemoglobin. Ann Biochem 92:11–15

    Article  CAS  Google Scholar 

  • Lee BR, Jung WJ, Jin YL, Avice JC, Ourry A, Kim TH (2009) Water deficit-induced oxidative stress and the activation of antioxidative enzymes in white clover leaves. Biol Plant 53:505–510

    Article  Google Scholar 

  • Lin CC, Kao CH (2001) Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant Soil 230:135–143

    Article  CAS  Google Scholar 

  • Lodwig EM, Hosie AHF, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino-acid cycling drives nitrogen fixation in the legume-rhizobium symbiosis. Nature 422:722–726

    Article  PubMed  CAS  Google Scholar 

  • López-Millán AF, Sagardoy R, Solanas M, Abadía A, Abadía J (2009) Cadmium toxicity in tomato (Lycopersicon esculentum) plants grown in hydroponics. Environ Exp Bot 65:376–385

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, New York

    Google Scholar 

  • Meda AR, Scheuermann EB, Prechsl UE, Erenoglu B, Schaaf G, Hayen H, Weber G, Wiren NV (2007) Iron acquisition by phytosiderophores contributes to cadmium tolerance. Plant Physiol 143:1761–1773

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Menguer PK, Farthing E, Peaston KA, Ricachenevsky FK, Fett JP, Williams LE (2013) Functional analysis of rice vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mori S, Nishizawa N (1987) Methionine as a dominant precursor of phytosiderophores in Graminea plants. Plant Cell Physiol 28:1081–1092

    CAS  Google Scholar 

  • Mukherjee I, Campbell NH, Ash JS, Connolly EL (2006) Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper. Planta 223:1178–1190

    Article  PubMed  CAS  Google Scholar 

  • Muneer S, Kim TH, Qureshi MI (2012) Fe modulates Cd-induced oxidative stress and the expression of stress response proteins in the nodules of Vigna radiata. Plant Growth Regul 68:421–433

    Article  CAS  Google Scholar 

  • Muneer S, Ahmad J, Qureshi MI (2013) Involvement of Fe nutrition in modulating oxidative stress and the expression of stress response proteins in leaves of Vigna radiata L. Aust J Crop Sci 7:1333–1342

    Google Scholar 

  • Muneer S, Hakeem KR, Mohamed R, Lee JH (2014) Cadmium toxicity induced alterations in the root proteome of green gram in contrasting response towards iron supplement. Int J Mol Sci 15:6343–6355

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Qadir S, Qureshi MI, Javed S, Abdin MZ (2004) Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd-stress. Plant Sci 167:1171–1181

    Article  CAS  Google Scholar 

  • Qureshi MI, Amici GMD, Fagioni M, Rinalducci S, Zolla L (2010) Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. J Plant Physiol 167:761–770

    Article  PubMed  CAS  Google Scholar 

  • Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontome C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118

    Article  PubMed  CAS  PubMed Central  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  PubMed  CAS  Google Scholar 

  • Romheld V, Marschner H (1986) Fine regulation of iron uptake by the Fe-efficient plant Helianthus annuus. In: Harley JL, Russell RS (eds) The soil-root interface. Academic press, London, pp 405–417

    Google Scholar 

  • Roskams AJ, Connor JR (1994) Iron, transferrin, and ferritin in the rat brain during development and aging. J Neurochem 63:709–716

    Article  PubMed  CAS  Google Scholar 

  • Rubio MI, Escrig I, Martinez-Cortina C, Lopez-Benet FJ, Sanz A (1994) Cadmium and nickel accumulation in rice plants. Effect on mineral nutrition and possible interaction of abscisic and giberellic acids. Plant Growth Regul 14:151–157

    Article  CAS  Google Scholar 

  • Sánchez-Pardo B, Carpena RO, Zornoza P (2013) Cadmium in white lupin nodules: impact on nitrogen and carbon metabolism. J Plant Physiol 170:265–271

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193

    Article  PubMed  CAS  Google Scholar 

  • Shanmugam V, Lo JC, Wu CL, Wang SL, Lai CC, Connolly EL, Huang JL, Yeh KC (2011) Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana —the role in zinc tolerance. New Phytol 190:125–137

    Article  PubMed  CAS  Google Scholar 

  • Siedlecka A, Krupa Z (1999) Cd/Fe interaction in higher plants—its consequences for the photosynthetic apparatus. Photosynthetica 36:321–331

    Article  CAS  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 apoplastic barrier. J Exp Bot 65:1125–1139

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • van der Mark F, de Lange T, Bienfait HF (1981) The role of ferritin in developing primary bean leaves under various light conditions. Planta 153:338–342

    Article  PubMed  Google Scholar 

  • Vert G, Briat JF, Curie C (2002a) Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J 26:181–189

    Article  Google Scholar 

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

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Vivares D, Arnoux P, Pignol D (2005) A papain-like enzyme at work: native and acyl-enzyme intermediate structure in phytochelatin synthesis. Proc Natl Acad Sci USA 102:18848–18853

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wallace A, Wallace GA, Cha JW (1992) Some modifications in trace metal toxicities and deficiencies in plants resulting from interactions with other elements and chelating agents-the special case of iron. J Plant Nutr 15:1589–1598

    Article  CAS  Google Scholar 

  • Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a Pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Welch RM, Norvell WA, Schaefer SC, Shaff JE, Kochian LV (1993) Induction of iron(III) and copper(II) reduction in pea (Pisum satinum 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 

  • Williams L, Salt DE (2009) The plant ionome coming into focus. Cur Opin Plant Biol 12:247–249

    Article  CAS  Google Scholar 

  • Yoshihara T, Hodoshima H, Miyano Y, Shoji K, Shimada H, Goto F (2006) Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep 25:365–373

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank iPET (Korea Institute of Planning & Evaluation for Technology in Food, Agriculture, Forestry and Fisheries), Ministry for Food, Agriculture, Forestry and Fisheries, and RDA (Ruler developmental Administration), Republic of Korea for providing financial support. We also thank Dr. Lee Farrand for proofreading of the manuscript.

Conflict of interest

Authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Horticultural Sciences and Applied Biotechnology, Institute of Agricultural Science and Technology, College of Agriculture and Life Science, Chonnam National University, Buk-Gwangju, P.O. Box 205, Gwangju, 500-600, Korea

    Sowbiya Muneer & Jeong Hyun Lee

  2. Department of Horticulture, Division of Applied Life Science (BK21 Plus), Graduate School, Gyeongsang National University, Jinju, 660-701, Korea

    Byoung Ryong Jeong & Prabhakaran Soundararajan

  3. Institute of Agriculture and Life Science, Gyeongsang National University, Jinju, 660-701, South Korea

    Sowbiya Muneer, Byoung Ryong Jeong & Prabhakaran Soundararajan

  4. Division of Applied Life Science (BK21 Program), Graduate School, Gyeongsang National University, Jinju, 660-701, South Korea

    Sowbiya Muneer & Byoung Ryong Jeong

  5. Department of Animal Science, Institute of Agricultural Science and Technology, College of Agriculture and Life Science, Chonnam National University, Buk-Gwangju, P.O. Box 205, Gwangju, 500-600, Korea

    Tae-Hwan Kim

Authors
  1. Sowbiya Muneer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Byoung Ryong Jeong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tae-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeong Hyun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Prabhakaran Soundararajan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sowbiya Muneer.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muneer, S., Jeong, B.R., Kim, TH. et al. Transcriptional and physiological changes in relation to Fe uptake under conditions of Fe-deficiency and Cd-toxicity in roots of Vigna radiata L.. J Plant Res 127, 731–742 (2014). https://doi.org/10.1007/s10265-014-0660-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-014-0660-0

Keywords

Search

Navigation