Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants

Abstract

Previous research showed that auxin, ethylene, and nitric oxide (NO) can activate the expression of iron (Fe)-acquisition genes in the roots of Strategy I plants grown with low levels of Fe, but not in plants grown with high levels of Fe. However, it is still an open question as to how Fe acts as an inhibitor and which pool of Fe (e.g., root, phloem, etc.) in the plant acts as the key regulator for gene expression control. To further clarify this, we studied the effect of the foliar application of Fe on the expression of Fe-acquisition genes in several Strategy I plants, including wild-type cultivars of Arabidopsis [Arabidopsis thaliana (L.) Heynh], pea [Pisum sativum L.], tomato [Solanum lycopersicon Mill.], and cucumber [Cucumis sativus L.], as well as mutants showing constitutive expression of Fe-acquisition genes when grown under Fe-sufficient conditions [Arabidopsis opt3-2 and frd3-3, pea dgl and brz, and tomato chln (chloronerva)]. The results showed that the foliar application of Fe blocked the expression of Fe-acquisition genes in the wild-type cultivars and in the frd3-3, brz, and chln mutants, but not in the opt3-2 and dgl mutants, probably affected in the transport of a Fe-related repressive signal in the phloem. Moreover, the addition of either ACC (ethylene precursor) or GSNO (NO donor) to Fe-deficient plants up-regulated the expression of Fe-acquisition genes, but this effect did not occur in Fe-deficient plants sprayed with foliar Fe, again suggesting the existence of a Fe-related repressive signal moving from leaves to roots.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylic acid

EDDHA:

N,N′-ethylenebis[2-(2-hydroxyphenyl)-glycine]

Ferrozine:

3-(2-Pyridyl)-5,6-bis(4-phenyl-sulfonic acid)-1,2,4-triazine

NA:

Nicotianamine

GSNO:

S-nitrosoglutathione

References

  1. Bacaicoa E, Mora V, Zamarreño AM, Fuentes M, Casanova E, García-Mina JM (2011) Auxin: a major player in the shoot-to-root regulation of root Fe-stress physiological responses to Fe deficiency in cucumber plants. Plant Physiol Biochem 49:545–556

    PubMed  Article  CAS  Google Scholar 

  2. Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106:8067–8072

    PubMed  Article  CAS  Google Scholar 

  3. Bienfait HF, De Weger LA, Kramer D (1987) Control of development of iron-efficiency reactions in potato as a response to iron deficiency is located in the roots. Plant Physiol 83:244–247

    PubMed  Article  CAS  Google Scholar 

  4. Brumbarova T, Bauer P (2005) Iron-mediated control of the basic helix-loop-helix protein FER, a regulator of iron uptake in tomato. Plant Physiol 137:1018–1026

    PubMed  Article  CAS  Google Scholar 

  5. Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    PubMed  Article  Google Scholar 

  6. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol 154:810–819

    PubMed  Article  CAS  Google Scholar 

  7. Clark RJ, Tan CC, Preza GC, Nemeth E, Ganz T, Craik DJ (2011) Understanding the structure/activity relationships of the iron regulatory peptide hepcidin. Chem Biol 18:336–343

    PubMed  Article  CAS  Google Scholar 

  8. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    PubMed  Article  CAS  Google Scholar 

  9. Enomoto Y, Hodoshima H, Shimada H, Shoji K, Yoshihara T, Goto F (2007) Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta 227:81–89

    PubMed  Article  CAS  Google Scholar 

  10. García MJ, Lucena C, Romera FJ, Alcántara E, Pérez-Vicente R (2010) Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J Exp Bot 61:3885–3899

    PubMed  Article  Google Scholar 

  11. García MJ, Suárez V, Romera FJ, Alcántara E, Pérez-Vicente R (2011) A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants. Plant Physiol Biochem 49:537–544

    PubMed  Article  Google Scholar 

  12. Germain H, Chevalier E, Matton DP (2006) Plant bioactive peptides: an expanding class of signaling molecules. Can J Bot 84:1–19

    Article  CAS  Google Scholar 

  13. Graziano M, Lamattina L (2007) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  15. Grusak MA, Welch RM, Kochian LV (1990) Physiological characterization of a single-gene mutant of Pisum sativum exhibiting excess iron accumulation. I. Root iron reduction and iron uptake. Plant Physiol 93:976–981

    PubMed  Article  CAS  Google Scholar 

  16. Han ZH, Han CQ, Xu XF, Wang Q (2005) Relationship between iron deficiency stress and endogenous hormones in iron-efficient versus inefficient apple genotypes. J Plant Nutr 28:1887–1895

    Article  CAS  Google Scholar 

  17. Ivanov R, Brumbarova T, Bauer P (2011) Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Mol Plant 5:27–42

    PubMed  Article  Google Scholar 

  18. Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607–621

    PubMed  Article  CAS  Google Scholar 

  19. Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150:257–271

    PubMed  Article  CAS  Google Scholar 

  20. Kneen BE, LaRue T, Welch RM, Weeden NF (1990) Pleiotropic effects of brz. A mutation in Pisum sativum (L.) cv ‘Sparkle’ conditioning decreased nodulation and increased iron uptake and leaf necrosis. Plant Physiol 93:717–722

    PubMed  Article  CAS  Google Scholar 

  21. Landsberg EC (1984) Regulation of iron-stress-response by whole plant activity. J Plant Nutr 7:609–621

    Article  CAS  Google Scholar 

  22. Lei M, Zhu C, Liu Y, Karthikeyan AS, Bressan RA, Raghothama KG, Liu D (2011) Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol 189:1084–1095

    PubMed  Article  CAS  Google Scholar 

  23. Li C, Zhu X, Zhang F (2000) Role of shoot in regulation of iron deficiency responses in cucumber and bean plants. J Plant Nutr 23:1809–1818

    Article  CAS  Google Scholar 

  24. Ling HQ, Koch G, Baumlein H, Ganal MW (1999) Map-based cloning of chloronerva, a gene involved in iron uptake of higher-plants encoding nicotianamine synthase. Proc Natl Acad Sci USA 96:7098–7103

    PubMed  Article  CAS  Google Scholar 

  25. Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P (2011) Interaction between the bHLH transcription factor FIT and the ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23:1815–1829

    PubMed  Article  CAS  Google Scholar 

  26. Liu TY, Chang CY, Chiou TJ (2009) The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12:312–319

    PubMed  Article  CAS  Google Scholar 

  27. Lubkowitz M (2011) The oligopeptide transporters: a small gene family with a diverse group of substrates and functions? Mol Plant 4:407–415

    PubMed  Article  CAS  Google Scholar 

  28. Lucena C, Waters BM, Romera FJ, García MJ, Morales M, Alcántara E, Pérez-Vicente R (2006) Ethylene could influence ferric reductase, iron transporter, and H+-ATPase gene expression by affecting FER (or FER-like) gene activity. J Exp Bot 57:4145–4154

    PubMed  Article  CAS  Google Scholar 

  29. Lucena C, Romera FJ, Rojas CL, García MJ, Alcántara E, Pérez-Vicente R (2007) Bicarbonate blocks the expression of several genes involved in the physiological responses to Fe deficiency of Strategy I plants. Funct Plant Biol 34:1002–1009

    Article  CAS  Google Scholar 

  30. Maas FM, van de Wetering DAM, van Beusichem Ml, Bienfait HF (1988) Characterization of phloem iron and its possible role in the regulation of Fe-efficiency reactions. Plant Physiol 87:167–171

    PubMed  Article  CAS  Google Scholar 

  31. Marentes E, Grusak MA (1998) Mass determination of low-molecular-weight proteins in phloem sap using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. J Exp Bot 49:903–911

    CAS  Google Scholar 

  32. Marentes E, Stephens BW, Grusak MA (1997) Characterization of a phloem mobile chelator involved in the phloem transport of iron from vegetative tissues to developing seeds of pea. Abstract 9th International Symposium on Iron Nutrition and Interactions in Plants, Stuttgart/Germany, p 74

  33. Meiser J, Lingam S, Bauer P (2011) Post-translational regulation of the Fe deficiency bHLH transcription factor FIT is affected by iron and nitric oxide. Plant Physiol 157:2154–2166

    PubMed  Article  CAS  Google Scholar 

  34. Pich A, Manteuffel R, Hillmer S, Scholz G, Schmidt W (2001) Fe homeostasis in plant cells: Does nicotianamine play multiple roles in the regulation of cytoplasmic Fe concentration? Planta 213:967–976

    PubMed  Article  CAS  Google Scholar 

  35. Ramírez L, Simontacchi M, Murgia I, Zabaleta E, Lamattina L (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. Plant Sci 181:582–592

    PubMed  Article  Google Scholar 

  36. Rodriguez-Castrillón JA, Moldovan M, García JI, Lucena JJ, García-Tomé ML, Hernández-Apaolaza L (2008) Isotope pattern deconvolution as a tool to study iron metabolism in plants. Anal Bioanal Chem 390:579–590

    PubMed  Article  Google Scholar 

  37. Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799

    PubMed  Article  CAS  Google Scholar 

  38. Romera FJ, Alcántara E, De la Guardia MD (1992) Role of roots and shoots in the regulation of the Fe efficiency responses in sunflower and cucumber. Physiol Plant 85:141–146

    Article  CAS  Google Scholar 

  39. Romera FJ, García MJ, Alcántara E, Pérez-Vicente R (2011) Latest findings about the interplay of auxin, ethylene and nitric oxide in the regulation of Fe deficiency responses by Strategy I plants. Plant Signal Behav 6:167–170

    PubMed  Article  CAS  Google Scholar 

  40. Roschzttardtz H, Séguéla-Arnaud M, Briat JF, Vert G, Curie C (2011) The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. Plant Cell 23:2725–2737

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  42. Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H+-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant Physiol Biochem 43:287–292

    PubMed  Article  CAS  Google Scholar 

  43. Schmidke I, Krüger C, Frömmichen R, Scholz G, Stephan UW (1999) Phloem loading and transport characteristics of iron in interaction with plant-endogenous ligands in castor bean seedlings. Physiol Plant 106:82–89

    Article  CAS  Google Scholar 

  44. Scholz G, Schlesier G, Seifert K (1985) Effect of nicotianamine on iron uptake by the tomato mutant ‘chloronerva’. Physiol Plant 63:99–104

    Article  CAS  Google Scholar 

  45. Schuler M, Rellán-Álvarez R, Fink-Straube C, Abadía J, Bauer P (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24:2380–2400

    PubMed  Article  CAS  Google Scholar 

  46. Stacey MG, Osawa H, Patel A, Gassmann W, Stacey G (2006) Expression analyses of Arabidopsis oligopeptide transporters during seed germination, vegetative growth and reproduction. Planta 223:291–305

    PubMed  Article  CAS  Google Scholar 

  47. Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601

    PubMed  Article  CAS  Google Scholar 

  48. Stephan UW, Scholz G (1993) Nicotianamine: mediator of transport of iron and heavy metals in the phloem? Physiol Plant 88:522–529

    Article  CAS  Google Scholar 

  49. Venkatraju K, Marschner H (1981) Inhibition of iron-stress reactions in sunflower by bicarbonate. Z Pflanzenernähr Bodenkd 144:339–355

    Article  CAS  Google Scholar 

  50. Walker EL, Connolly EL (2008) Time to pump iron: iron-deficiency-signaling mechanisms of higher plants. Curr Opin Plant Biol 11:530–535

    PubMed  Article  CAS  Google Scholar 

  51. Waters BM, Lucena C, Romera FJ, Jester GG, Wynn AN, Rojas CL, Alcántara E, Pérez-Vicente R (2007) Ethylene involvement in the regulation of the H+-ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants. Plant Physiol Biochem 45:293–301

    PubMed  Article  CAS  Google Scholar 

  52. Wu T, Zhang HT, Wang Y, Jia WS, Xu XF, Zhang XZ, Han ZH (2012) Induction of root Fe(III) reductase activity and proton extrusion by iron deficiency is mediated by auxin-based systemic signalling in Malus xiaojinensis. J Exp Bot 63:859–870

    PubMed  Article  CAS  Google Scholar 

  53. Yuan YX, Wu HL, Wang N, Li J, Zhao WN, Du J, Wang DW, Ling HQ (2008) FIT interacts with AtbHLH038 and AtbHLH039 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res 18:385–397

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr Michael Grusak (USDA/ARS, Houston, Texas, USA), Dr Ross Welch (USDA/ARS, Ithaca, New York, USA), and Dr Petra Bauer (Saarland University, Saarbrücken, Germany) for kindly providing seeds of the Sparkle [dgl,dgl] mutant, the brz mutant, and the chloronerva mutant. We also thank the Arabidopsis Biological Resource Center (Ohio State University, USA) for providing seeds of the frd3-3 mutant. This work was supported by the European Regional Development Fund from the European Union, the “Ministerio de Educación y Ciencia” (Projects AGL2007-64372 and AGL2010-17121), and the “Junta de Andalucía” (Research Groups AGR115 and BIO159, and Project AGR-3849). Funding to MGS and GS was provided by a Grant from the USA National Science Foundation Plant Genome Program (Award #0820769).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Francisco J. Romera.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

García, M.J., Romera, F.J., Stacey, M.G. et al. Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants. Planta 237, 65–75 (2013). https://doi.org/10.1007/s00425-012-1757-0

Download citation

Keywords

  • dgl
  • Ethylene
  • Iron
  • Nitric oxide
  • opt3
  • Peptide
  • Phloem