Article | Published:

IRON MAN is a ubiquitous family of peptides that control iron transport in plants

Nature Plantsvolume 4pages953963 (2018) | Download Citation

Abstract

Iron (Fe) is an essential mineral nutrient that severely affects the growth, yield and nutritional quality of plants if not supplied in sufficient quantities. Here, we report that a short C-terminal amino-acid sequence consensus motif (IRON MAN; IMA) conserved across numerous, highly diverse peptides in angiosperms is essential for Fe uptake in plants. Overexpression of the IMA sequence in Arabidopsis induced Fe uptake genes in roots, causing accumulation of Fe and manganese in all plant parts including seeds. Silencing of all eight IMA genes harboured in the Arabidopsis genome abolished Fe uptake and caused severe chlorosis; increasing the Fe supply or expressing IMA1 restored the wild-type phenotype. IMA1 is predominantly expressed in the phloem, preferentially in leaves, and reciprocal grafting showed that IMA1 peptides in shoots positively regulate Fe uptake in roots. IMA homologues are highly responsive to the Fe status and functional when heterologously expressed across species. IMA constitutes a novel family of peptides that are critical for the acquisition and cellular homeostasis of Fe across land plants.

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Data availability

RNAseq data of IMA1 Ox and Fe-deficient wild-type Col-0 transcriptomes have been deposited to the Gene Expression Omnibus database and are available under the accession numbers GSE87745 and GSE87760, respectively. Information about IMA gene accession numbers and loci position are given in Supplementary Table 2.

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Acknowledgements

We thank T. J. Buckhout (Humboldt University, Germany) and M. Matzke (IPMB, Academia Sinica) for valuable suggestions and critical comments on the manuscript. We further thank S. Mari and C. Curie (INRA-SUPAGRO, France) for helpful discussions and I. C. Vélez-Bermúdez for help with cross-sectioning. We are grateful to J. Bailey-Serres for kindly providing ribosome profiling data of IMA genes and J.-K. Zhu for providing the Cas9 vector that we used as a template. RNA sequencing was performed by the High Throughput Genomics Core Facility with the assistance of M.-Y. Lu, supported by Academia Sinica. We thank L.-Y. Kuang and S.-M. Chen from the Transgenic Plant Laboratory of IPMB for performing tomato and Arabidopsis transformations, M.-J. Fang from the IPMB Live Cell Imaging Core Laboratory for the help with confocal imaging, W.-D. Lin and Y.-I Lin from the Bioinformatics Core Laboratory at IPMB for bioinformatics support, Y.-R. Chen and Y.-C. Huang from the Metabolomics Core Laboratory of the Agricultural Biotechnology Research Center for the support with the electrospray ionization mass spectrometry. Elemental analysis were conducted through the use of ICP-MS by P.L. supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB15030103) and the Project of Priority and Key Areas, ISSCAS (ISSASIP1605). This work was supported by an Academia Sinica Investigator Award to W.S.

Author information

Author notes

  1. These authors contributed equally to this work: Louis Grillet, Ping Lan.

Affiliations

  1. Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan

    • Louis Grillet
    • , Ping Lan
    • , Wenfeng Li
    • , Girish Mokkapati
    •  & Wolfgang Schmidt
  2. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China

    • Ping Lan
  3. Collaborative Innovation Center of Sustainable Forestry in Southern China of Jiangsu Province, Nanjing Forestry University, Nanjing, China

    • Wenfeng Li
  4. Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan

    • Girish Mokkapati
    •  & Wolfgang Schmidt
  5. Molecular Biology and Agricultural Sciences Program, Taiwan International Graduate program, Academia Sinica and National ChungHsing University, Taipei, Taiwan

    • Girish Mokkapati
  6. Genome and Systems Biology Degree Program, College of Life Science, National Taiwan University, Taipei, Taiwan

    • Wolfgang Schmidt

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Contributions

W.S., L.G. and P.L. designed the research; L.G., P.L., W.S., W.L. and G.M. performed and analysed experiments; W.S. and L.G. wrote the manuscript.

Competing interests

There is a potential competing interest as a provisional application for a patent concerning the use of IMA peptides to produce iron-enriched plants has been filed (US 20150315250 A1).

Corresponding author

Correspondence to Wolfgang Schmidt.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–15 and Supplementary Tables 1–5

  2. Reporting Summary

  3. Supplementary Data Set 1

    RNA-seq transcriptome analysis of IMA1 Ox and Fe-deficient WT Col-0

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https://doi.org/10.1038/s41477-018-0266-y