Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake

Abstract

Frequently, crop plants do not take up adequate amounts of iron from the soil, leading to chlorosis, poor yield and decreased nutritional quality. Extremely limited soil bioavailability of iron has led plants to evolve two distinct uptake strategies: chelation, which is used by the world's principal grain crops1,2; and reduction, which is used by other plant groups3,4,5. The chelation strategy involves extrusion of low-molecular-mass secondary amino acids (mugineic acids) known as ‘phytosiderophores’, which chelate sparingly soluble iron6. The Fe(iii)-phytosiderophore complex is then taken up by an unknown transporter at the root surface7,8. The maize yellow stripe1 (ys1) mutant is deficient in Fe(iii)-phytosiderophore uptake7,8,9,10, therefore YS1 has been suggested to be the Fe(iii)-phytosiderophore transporter. Here we show that ys1 is a membrane protein that mediates iron uptake. Expression of YS1 in a yeast iron uptake mutant restores growth specifically on Fe(iii)-phytosiderophore media. Under iron-deficient conditions, ys1 messenger RNA levels increase in both roots and shoots. Cloning of ys1 is an important step in understanding iron uptake in grasses, and has implications for mechanisms controlling iron homeostasis in all plants.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The Ac-induced yellow stripe mutation.
Figure 2: ys1 sequence analysis.
Figure 3: Growth test in the yeast iron uptake mutant.
Figure 4: Regulation of ys1 mRNA levels by iron availability in young maize plantlets.

Similar content being viewed by others

References

  1. Briat, J. -F. & Lobreaux, S. Iron transport and storage in plants. Trends Plant Sci. 2, 187– 193 (1997).

    Article  Google Scholar 

  2. Mori, S. Iron acquisition by plants. Curr. Opin. Plant Biol. 2, 250–253 (1999).

    Article  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Yi, Y. & Guerinot, M. L. Genetic evidence that induction of root Fe[iii] chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J. 10, 835–844 (1996).

    Article  CAS  PubMed  Google Scholar 

  5. Robinson, N. J., Procter, C. M., Connolly, E. L. & Guerinot, M. L. A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Tagaki, S., Nomoto, K. & Takemoto, T. Physiological aspect of mugineic acid, a possible phytosiderophore of graminaceous plants. J. Plant Nutr. 7, 469–477 (1984).

    Article  Google Scholar 

  7. von Wiren, N., Mori, S., Marschner, H. & Romheld, V. Iron inefficiency in maize mutant ys1 (Zea mays L. cv Yellow-Stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol. 106, 71–77 ( 1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. von Wiren, N., Marchner, H. & Romheld, V. Uptake kinetics of iron-phytosiderophores in two maize genotypes differing in iron efficiency. Physiol. Plant. 93, 611–616 (1995).

    Article  CAS  Google Scholar 

  9. Hopkins, B. G., Jolley, V. D. & Brown, J. C. Plant utilization of iron solubilized by oat phytosiderophore. J. Plant Nutr. 15, 1599– 1612 (1992).

    Article  CAS  Google Scholar 

  10. Jolley, V. D. & Brown, J. C. Differential response of Fe-efficient corn and Fe-inefficient corn and oat to phytosiderophore released by Fe-efficient Coker 227 oat. J. Plant Nutr. 14, 45– 58 (1991).

    Article  CAS  Google Scholar 

  11. Dellaporta, S. L. & Moreno, M. in The Maize Handbook (eds Freeling, M. & Walbot, V.) 219–233 (Springer, New York, 1993).

    Google Scholar 

  12. Loulergue, C., Lebrun, M. & Briat, J. F. Expression cloning in Fe2+ transport defective yeast of a novel maize MYC transcription factor. Gene 225, 47–57 ( 1998).

    Article  CAS  PubMed  Google Scholar 

  13. Pao, S. S., Paulsen, I. T. & Saier, M. H. Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62, 1–34 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D. & Dancis, A. A permease–oxidase complex involved in high affinity iron uptake in yeast. Science 271, 1552–1557 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Mori, S. et al. Why are young rice plants highly susceptible to iron deficiency? Plant Soil 130, 143–156 (1991).

    Article  CAS  Google Scholar 

  16. von Wiren, N. et al. Nicotianamine chelates both Fe[iii] and Fe[ii ]. Implications for metal transport in plants. Plant Physiol. 119, 1107–1114 ( 1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Stephan, U. W., Schmidke, I. & Pich, A. Phloem translocation of Fe, Cu, Mn, and Zn in Ricinus seedlings in relation to the concentrations of nicotianamine, an endogenous chelator of divalent metal-ions, in different seedling parts. Plant Soil 165, 181–188 (1994).

    Article  CAS  Google Scholar 

  18. Stephan, U. W., Schmidke, I., Stephan, V. W. & Scholz, G. The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 9, 84– 90 (1996).

    Article  CAS  Google Scholar 

  19. Minet, M., Dufour, M. E. & Lacroute, F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2, 417–422 (1992).

    CAS  PubMed  Google Scholar 

  20. von Wiren, N., Gibrat, R. & Briat, J.-F. In vitro characterization of iron-phytosiderophore interaction with maize root plasma membranes: evidences for slow association kinetics. Biochem. Biophys. Acta 1371, 143– 155 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Thoiron, S., Pascal, N. & Briat, J.-F. Impact of iron deficiency and iron re-supply during the early stages of vegetative development in maize (Zea mays L.). Plant Cell Env. 20, 1051–1060 (1997).

    Article  CAS  Google Scholar 

  22. Hirokawa, T., Boon-Chieng, S. & Mitaku, S. SOSUI: Classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378–379 (1998).

    Article  CAS  PubMed  Google Scholar 

  23. Bagnaresi, P. et al. Cloning and characterization of a maize cytochrome-b 5 reductase with Fe3+-chelate reduction capability. Biochem. J. 338, 499–505 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are indebted to S. Kawai for the gift of mugineic acid and to M. L. Guerinot for the gift of IRT1 cDNA. This work was supported by a USDA NRICGP Plant Responses to the Environment Award to ELW and an NIH Award to SLD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elsbeth L. Walker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Curie, C., Panaviene, Z., Loulergue, C. et al. Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346–349 (2001). https://doi.org/10.1038/35053080

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35053080

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing