Abstract
Long-distance signals generated in shoots are thought to be associated with the regulation of iron uptake from roots; however, the signaling mechanism is still unknown. To elucidate whether the signal regulates iron uptake genes in roots positively or negatively, we analyzed the expressions of two representative iron uptake genes: NtIRT1 and NtFRO1 in tobacco (Nicotiana tabacum L.) roots, after shoots were manipulated in vitro. When iron-deficient leaves were treated with Fe(II)-EDTA, the expressions of both genes were significantly reduced; nevertheless iron concentration in the roots maintained a similar level to that in roots grown under iron-deficient conditions. Next, all leaves from tobacco plants grown under the iron-deficient condition were excised. The expression of two genes were quickly reduced below half within 2 h after the leaf excision and gradually disappeared by the end of a 24-h period. The NtIRT1 expression was compared among the plants whose leaves were cut off in various patterns. The expression increased in proportion to the dry weight of iron-deficient leaves, although no relation was observed between the gene expression and the position of excised leaves. Interestingly, the NtIRT1 expression in hairy roots increased under the iron-deficient condition, suggesting that roots also have the signaling mechanism of iron status as well as shoots. Taken together, these results indicate that the long-distance signal generated in iron-deficient tissues including roots is a major factor in positive regulation of the expression of NtIRT1 and NtFRO1 in roots, and that the strength of the signal depends on the size of plants.
Similar content being viewed by others
References
Baldwin IT, Schmelz EA, Ohnmeiss TE (1994) Wound-induced changes in root and shoot jasmonic acid pools correlate with induced nicotine synthesis in Nicotiana sylvestris spegazzini and comes. J Chem Ecol 20:2139–2157
Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664
Bienfait HF (1989) Prevention of stress in iron metabolism of plants. Acta Bot Neerl 38:105–129
Brumbarova T, Bauer P (2005) Iron-mediated control of the basic helix-loop-helix protein FER, a regulator of uptake in tomato. Plant Physiol 137:1018–1026
Canevascini S, Caderas D, Mandel T, Fleming AJ, Dupuis I, Kuhlemeier C (1996) Tissue-specific expression and promoter analysis of the tobacco ltp1 Gene. Plant Physiol 112:513–524
Chow B, McCourt P (2006) Plant hormone receptors: perception is everything. Genes Dev 20:1998–2008
Clemens S (2001) Molecular mechanism of plant metal tolerance and homeostasis. Planta 212:475–486
Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 12:3400–3412
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
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
Forde BG (2002) The role of long-distance signalling in plant responses to nitrate and other nutrients. J Exp Bot 53:39–43
Golz JF (2006) Signalling between the shoot apical meristem and developing lateral organs. Plant Mol Biol 60:889–903
Grusak MA (1995) Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L.(Fabaceae): relevance to the iron nutrition of developing seeds. Planta 197:111–117
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
Hell R, Stephan UW (2003) Iron uptake, trafficking and homeostasis in plants. Planta 216:541–551
Herbik A, Giritch A, Horstmann C, Becker R, Balzer HJ, Baumlein H, Stephan UW (1996) Iron and copper nutrition-dependent changes in protein expression in a tomato wild type and the nicotianamine-free mutant chloronerva. Plant Physiol 111:533–540
Hodoshima H, Enomoto Y, Shoji K, Shimada H, Goto F, Yoshihara T (2007) Differential regulation of cadmium-inducible expression of iron-deficiency-responsive genes in tobacco and barley. Physiol Plant 129:622–634
Jackson MB (2002) Long-distance signalling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–181
Jakoby M, Wang HY, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS 577:528–534
Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193
Landsberg EC (1984) Regulation of iron-stress-response by whole-plant activity. J Plant Nutr 7:609–621
León J, Rojo E, Sánchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52:1–9
Li CJ, Zhu XP, Zhang FS (2000) Role of shoot in regulation of iron deficiency responses in cucumber and bean plants. J Plant Nutr 23:1809–1818
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. PNAS 96:7098–7103
Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. PNAS 99:13938–13943
Maas FM, van de Wetering DA, 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
Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Pena A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567
Mori S (1999) Iron acquisition by plants. Plant Biol 2:250–253
Murashige T, Skoog F (1962) A revised medium for rapid growth bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Negishi T, Nakanishi H, Yazaki J, Kishimoto N, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kikuchi S, Mori S, Nishizawa NK (2002) cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore Fe-deficient barley roots. Plant J 30:83–94
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
Rahayu YS, Walch-Liu P, Neumann G, Romheld V, von Wiren N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3-induced stimulation of leaf growth. J Exp Bot 56:1143–1152
Raven PH, Evert RF, Eichhorn SE (1999) Biology of plants, 6th edn. Freeman WH, New York, pp 729–730
Royo J, Vancanneyt G, Pérez AG, Sanz C, Störmann K, Rosahl S, Sánchez-Serrano JJ (1996) Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem 271:21012–21009
Schmidt W (2003) Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8:188–193
Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118
Staiger D (2002) Chemical strategies for iron acquisition in plants. Angew Chem Int Ed 41:2259–2264
Thimm O, Essigmann B, Kloska S, Altmann T, Buckhout TJ (2001) Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol 127:1030–1043
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
Yoshihara T, Kobayashi T, Goto F, Masuda T, Higuchi K, Nakanishi H, Nishizawa NK, Mori S (2003) Regulation of the iron-deficiency responsive gene, ids2, of barley in tobacco. Plant Biotechnol 20:33–41
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
Yuan YX, Zhang J, Wang DW, Ling HQ (2005) AtbHLH29 of Arabidopsis thaliana is a functional ortholog of tomato FER involved in controlling iron acquisition in strategy I plants. Cell Res 15:613–621
Acknowledgments
The authors thank Bienfait, H. Frits for critical discussion, Yamamoto, Naomi for experimental assistance. This work was in part supported by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (No.16380232).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Enomoto, Y., Hodoshima, H., Shimada, H. et al. Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots. Planta 227, 81–89 (2007). https://doi.org/10.1007/s00425-007-0596-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-007-0596-x