Skip to main content
Log in

Identification and characterization of a novel iron deficiency and salt stress responsive transcription factor IDEF1 in Porteresia coarctata

  • Original papers
  • Published:
Biologia Plantarum

Abstract

Iron availability affects plant growth depending on soil type. Mangroves are characterized by alkaline soils in which the halophytic wild rice relative Porteresia coarctata thrives. Young plants of P. coarctata grew optimally in the presence of 150 mM NaCl in a hydroponic medium and tolerated iron deficiency and salt up to 21 d without showing any symptoms of stress. A homolog of the rice iron deficiency responsive cis-acting element binding factor (IDEF1) that functions at the base of an iron regulated network was isolated and characterized from P. coarctata. PcIDEF1 had a close paralog in P. coarctata genome and its transcript expression was upregulated by both iron deficient conditions and salt treated conditions for up to three weeks. Sub-cellular localization study suggests nuclear targeting PcIDEF1 protein in guard cells and root tissues of tobacco. In vitro assays for metal binding affinity and binding PcIDEF1 to iron deficiency responsive element 1 (IDE1)-like elements in the 5’ flanking region of an iron regulated transporter from P. coarctata suggest that PcIDEF1 could potentially sense iron content in a plant cell and regulate expression of iron responsive genes containing IDE1-like elements in their promoter region. This study provides evidence for a possible cross-talk between iron deficiency and salt responses.

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.

Similar content being viewed by others

Abbreviations

BPDS:

batho-phenanthroline disulphonic acid

dI-dC:

deoxyinosinic-deoxycytidylic

EMSA:

electrophoretic mobility shift assay

FRO:

ferric chelate reductase

GFP:

green fluorescent protein

His-6:

hexa-histidine

HN:

histidine-asparagine

IDE:

iron deficiency responsive element

IMAC:

immobilized metal ion affinity chromatography

MS:

Murashige and Skoog

ORF:

open reading frame

PcIDEF1 :

Porteresia coarctata iron deficiency responsive cis-acting element binding factor 1

PcIRT1 :

Porteresia coarctata iron regulated transporter 1

References

  • Arnon, D.I.: Copper enzymes in isolated chloroplasts: polyphenoxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bashir, K., Ishimaru, Y., Shimo, H., Kakei, Y., Senoura, T., Takahashi, R., Sato, Y., Sato, Y., Uozumi, N., Nakanishi, H., Nishizawa, N.K.: Rice phenolics efflux transporter2 (PEZ2) plays an important role in solubilising apoplasmic iron. — Soil Sci. Plant Nutr. 57: 803–812, 2011.

    Article  CAS  Google Scholar 

  • Bauer, P., Thiel, T., Klatte, M., Bereczky, Z., Brumbarova, T., Hell, R., Grosse, I.: Analysis of sequence, map position, and gene expression reveals conserved essential genes for iron uptake in Arabidopsis and tomato. — Plant Physiol. 136: 4169–4183, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benmoussa, H., Tyagi, R.D., Campbell, P.G.G.: Simultaneous sewage sludge digestion and metal leaching using an internal loop reactor. — Water Res. 31: 2638–2654, 1997.

    Article  CAS  Google Scholar 

  • Brumbarova, T., Bauer, P., Ivanov, R.: Molecular mechanisms governing Arabidopsis iron uptake. — Trends Plant Sci. 20: 124–133, 2015.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Connolly, E.L., Guerinot, M.L.: Iron stress in plants. — Genome Biol. 1024: 1024.1–1024.4, 2002.

    Google Scholar 

  • Conte, S.S., Walker, E.L.: Transporters contributing to iron trafficking in plants. — Mol. Plant. 4: 464–476, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Curie, C., Cassin, G., Couch, D., Divol, F., Higuchi, K., Jean, M.L., Misson, J., Schikora, A., Czernic, P., Stéphane, M.: Metal movement within the plant: contribution of nicotianamine and yellow-stripe 1-like transporters. — Ann. Bot. 103: 1–11, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Ducos, E., Fraysse, S., Boutry, M.: NtPDR3, an iron-deficiency inducible ABC transporter in Nicotiana tabacum. — FEBS Lett. 579: 6791–6795, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Eide, D., Broderius, M., Fett, J., Guerinot, M.L.: A novel ironregulated metal transporter from plants identified by functional expression in yeast. — Proc. nat. Acad. Sci. USA. 93: 5624–5628, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers, T.J., Flowers, S.A., Hajibagheri, M.A., Yeo, A.R.: Salt tolerance in the halophytic wild rice, Porteresia coarctata Tateoka. — New Phytol. 114: 675–684, 1990.

    Article  CAS  Google Scholar 

  • Fourcroy, P., Sisó-Terraza, P., Sudre, D., Savirón, M., Reyt, G., Gaymard, F., Abadía, A., Abadia, J., Alvarez-Fernández, A., Briat, J.F.: Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. — New Phytol. 201: 155–167, 2014.

    Article  CAS  PubMed  Google Scholar 

  • Giblin, A.E., Howarth, R.W.: Porewater evidence for a dynamic sedimentary iron cycle in salt marshes. — Limnol Oceanogr. 29: 47–63, 1984.

    Article  CAS  Google Scholar 

  • Gregory, A.V., Briat, J.F., Curie, C.: Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. — Plant Physiol. 132: 796–804, 2003.

    Article  Google Scholar 

  • Grillet, L., Mari, S., Schmidt, W.: Iron in seeds–loading pathways and subcellular localization. — Front. Plant Sci. 4: 1–8, 2014.

    Article  Google Scholar 

  • Holmer, M., Kristensen, E., Banta, G., Hansen, K., Jensen, M.H., Bussawarit, N.: Biogeochemical cycling of sulphur and iron in sediments of a south-east Asian mangrove, Phuket island, Thailand. — Biogeochemistry 26: 145–161, 1994.

    Article  CAS  Google Scholar 

  • Horsch, R.B., Fry, J.E., Hoffman, N.L., Eichholtz, D., Rogers, S.G., Fraley, R.T.: A simple and general method for transferring genes into plants. — Science 227: 1229–1231, 1985.

    Article  CAS  Google Scholar 

  • Ishimaru, Y., Suzuki, M., Tsukamoto, T., Suzuki, K., Nakazono, M., Kobayashi, T., Wada, Y., Watanabe, S., Matsuhashi, S., Takahashi, M., Nakanishi, H., Mori, S., Nishizawa, N.K.: Rice plants take up iron as an Fe3+ phytosiderophore and as Fe2+. — Plant J. 45: 335–346, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Ishimaru, Y., Kakei, Y., Shimo, H., Bashir, K., Sato, Y., Sato, Y., Uozumi, N., Nakanishi, H., Nishizawa, N.K.: A rice phenolic efflux transporter is essential for solubilising precipitated apoplasmic iron in the plant stele. — J. biol. Chem. 286: 24649–24655, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jagtap, T.G., Bhosale, S., Singh, C.: Characterization of Porteresia coarctata beds along the Goa coast, India. — Aquat. Bot. 84: 37–44, 2006.

    Article  Google Scholar 

  • Jeong, J., Guerinot, M.L.: Homing in on iron homeostasis in plants. — Trends Plant Sci. 14: 280–285, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Kanal, A.H.M., Short, F.: A new record of sea grass Halophila beccarii Ascherson in Bangladesh. — J. Natur. Sci. 8: 201–206, 2009.

    Google Scholar 

  • King, G.M., Klug, M.J., Wilgert, R.G., Chalmers, A.G.: Relation of soil water movement and sulphide concentration to Spartina alterniflora production in Georgia salt marsh. — Science 218: 61–63, 1982.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, T., Itai, R.N., Aung, M.S., Senoura, T., Nakanishi, H., Nishizawa, N.K.: The rice transcription factor IDEF1 directly binds to iron and other divalent metals for sensing cellular iron status. — Plant J. 69: 81–91, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, T., Itai, R.N., Ogo, Y., Kakei, Y., Nakanishi, H., Takahashi, M., Nishizawa, N.K.: The rice transcription factor IDEF1 is essential for the early response to iron deficiency, and induces vegetative expression of late embryogenesis abundant genes. — Plant J. 60: 948–961, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, T., Nagasaka, S., Senoura, T., Itai, R.N., Nakanishi, H., Nishizawa, N.K.: Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. — Nat. Commun. 4: 27–92, 2013.

    Google Scholar 

  • Kobayashi, T., Ogo, Y., Itai, R.N., Nakanishi, H., Takahashi, M., Mori, S., Nishizawa, N.K.: The transcription factor IDEF1 regulates the response to and tolerance of iron deficiency in plants. — Proc. nat. Acad. Sci. USA. 104: 19150–19155, 2007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, T., Suzuki, M., Inoue, H., Itai, R.N., Takahashi, M., Nakanishi, H., Mori, S., Nishizawa, N.K.: Expression of iron-acquisition related genes in iron-deficient rice is co-ordinately induced by partially conserved iron-deficiency responsive elements. — J. Exp. Bot. 56: 1305–1316, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S., Nishizawa, N.K.: OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. — Plant J. 39: 415–424, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Lindsay, W.L.: Soil and plant relationships associated with iron deficiency with emphasis on nutrient interactions. — J. Plant Nutr. 7: 489–500, 1984.

    Article  CAS  Google Scholar 

  • Liu, Y.G., Mitsukawa, N., Oosumi, T., Whittier, R.F.: Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. — Plant J. 8: 457–463, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Lu, B.R., Ge, S.: Oryza coarctata: the name that best reflects the relationships of Porteresia coarctata (Poaceae: Oryzeae). — Nord. J. Bot. 23: 5, 2004.

    Google Scholar 

  • Majee, M., Maitra, S., Dastidar, K.G., Pattnaik, S., Chatterjee, A., Hait, N.C.: A Novel salt-tolerant L-myo-inositol-1-phos-phate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice. — J. biol. Chem. 279: 28539–28552, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Majerus, V., Bertin, P., Swenden, V., Fortemps, A., Lobréaux, S., Lutts, S.: Organ-dependent responses of the African rice to short-term iron toxicity: ferritin regulation and antioxidative responses. — Biol. Plant. 51: 303–312, 2007.

    Article  CAS  Google Scholar 

  • Marchler-Bauer, A., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., He, S., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Liebert, C.A., Liu, C., Lu, F., Lu, S., Maechler, G.H., Mullokandov, M., Song, J.S., Tasneem, A., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N., Bryant, S.H.: CDD: specific functional annotation with the conserved domain database. — Nucl. Acids Res. 37: 205–210, 2009.

    Article  Google Scholar 

  • Marschner, H.: Mineral Nutrition of Higher Plants. 2nd Ed. - Academic Press, London 1995.

    Google Scholar 

  • Michiels, A., Van den Ende, W., Tucker, M., Van Riet, L., Van Laere, A.: Extraction of high quality genomic DNA from latex-containing plants. — Anal Biochem. 315: 85–89, 2003.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nozoye, T., Nagasaka, S., Kobayashi, T., Takahashi, M., Sato, Y., Uozumi, N., Nakanishi, H., Nishizawa, N.K.: Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. — J. biol Chem. 286: 5444–5454, 2011.

    Article  Google Scholar 

  • Rabhi, M., Barhoumi, Z., Ksouri, R., Abdelly, C., Gharsalli, M.: Interactive effects of salinity and iron deficiency in Medicago ciliaris. — Compt. rend. Biol. 330: 779–788, 2007.

    Article  CAS  Google Scholar 

  • Reef, R., Feller, I.C., Lovelock, C.E.: Nutrition of mangroves. — Tree Physiol. 30: 1148–1160, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Rellán-Alvarez, R., Giner-Martinez-Sierra, J., Orduna, J., Orera, I., Rodríguez-Castrillón, J.A., Garcia-Alonso, J.I., Abadía, J., Alvarez-Fernández, A.: Identification of a tri-iron (III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. — Plant Cell Physiol. 51: 91–102, 2010.

    Article  PubMed  Google Scholar 

  • Robinson, N.J., Proctor, C.M., Connolly, E.L., Guerinot, M.L.: A ferricchelate reductase for iron uptake from soils. — Nature 397: 694–697, 1996.

    Article  Google Scholar 

  • Rodriguez-Celma, J., Lin, W.D., Fu, G.M., Abadia, J., Lopez-Millan, A.F., Schmidt, E.: Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. — Plant Physiol. 162: 1473–1485, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romera, F.Z., Welch, R.M., Norwell, W.A., Schaefer, S.C.: Iron requirement for and effect of promoters and inhibitors of ethylene action on stimulation of ferric(III)-chelate reductase in roots of strategy I species. — Biometals 9: 45–50, 1996.

    CAS  Google Scholar 

  • Römheld, V., Marschner, H.: Evidence for a specific uptake system for iron phytosiderophores in roots and grasses. — Plant Physiol. 80: 175–180, 1986.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz, H., Conèjèro, G., Divol, F., Alcon, C., Verdeil, J.-L., Curie, C., Mori, S.: New insights into Fe localization in plant tissues. — Front. Plant Sci. 4: 350, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sambrook, J., Fritich, E.F., Maniatis, T.: Molecular Cloning: a Laboratory Manual. Vol. I. 2nd Ed. - Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1989.

    Google Scholar 

  • Santi, S., Schmidt, W.: Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. — New Phytol. 183: 1072–1084, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Sengupta, S., Majumder, A.L.: Porteresia coarctata (Roxb.) Tateoka, a wild rice: a potential model for studying saltstress biology in rice. — Plant Cell Environ. 33: 526–542, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, M., Morikawa, K.C., Nakanishi, H., Takahashi, M., Saigusa, M., Mori, S., Nishizawa, N.K.: Transgenic rice lines that include barley genes have increase tolerance to low iron availability in a calcareous paddy soil. — Soil Sci Plant Nutr. 54: 77–85, 2008.

    Article  CAS  Google Scholar 

  • Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K., Narusaka, Y., Narusaka, M., Zhu, J.-K., Shinozaki, K.: Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. — Plant Physiol. 135: 1697–1709, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi, S.: Naturally occurring iron-chelating compounds in oat and rice root washings. — Soil Sci. Plant Nutr. 22: 423–433, 1976.

    Article  CAS  Google Scholar 

  • Takahashi, M., Nakanishi, H., Kawasaki, S., Nishizawa, N.K., Mori, S.: Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. — Nat Biotechnol. 19: 466–469, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, M., Yamaguchi, H., Nakanishi, H., Shioiri, T., Nishizawa, N.K., Mori, S.: Cloning two genes for nicotianamine aminotransferase, a critical enzyme in iron acquisition (strategy II) in graminaceous plants. — Plant Physiol. 121: 947–956, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S.: MEGA6: molecular evolutionary genetics analysis version 6.0. — Mol. Biol. Evol. 30: 2725–2729, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda, E.K.M., Gout, P.W., Morganti, L.: Current and prospective applications of metal ion-protein binding. — J. Chromatogr. 988: 1–23, 2003.

    Article  CAS  Google Scholar 

  • Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., Curie, C.: IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. — Plant Cell 14: 1223–1233, 2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker, E.L., Connolly, E.L.: Time to pump iron: irondeficiency- signaling mechanisms of higher plants. — Curr. Opin. Plant Biol. 11: 530–535, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Yousfi, S., Wissal, M., Mahmoudi, H., Abdelly, C., Gharsalli, M.: Effect of salt on physiological responses of barley to iron deficiency. — Plant Physiol Biochem. 45: 309–314, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J.K.: Plant salt tolerance. — Trends Plant Sci. 6: 66–71, 2001.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Kumar Parida.

Additional information

Acknowledgement

The work presented in the manuscript was funded by the Department of Biotechnology, the Government of India. The clone for the green fluorescent protein (mGFP6) was kindly provided by Dr. Mark Curtis, the Institute of Plant Biology, Zurich, Switzerland. We also acknowledge the help of Dr. Sesha Bamini, the National Centre for Ultrafast Processing, Chennai, in confocal microscopy studies.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Purohit, D., Sankararamasubramanian, H.M., Kumar Pal, A. et al. Identification and characterization of a novel iron deficiency and salt stress responsive transcription factor IDEF1 in Porteresia coarctata . Biol Plant 60, 469–481 (2016). https://doi.org/10.1007/s10535-016-0616-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-016-0616-4

Additional key words

Navigation