Abstract

Shoot apical meristems are stem cell niches that balance proliferation with the incorporation of daughter cells into organ primordia. This balance is maintained by CLAVATA–WUSCHEL feedback signaling between the stem cells at the tip of the meristem and the underlying organizing center. Signals that provide feedback from organ primordia to control the stem cell niche in plants have also been hypothesized, but their identities are unknown. Here we report FASCIATED EAR3 (FEA3), a leucine-rich-repeat receptor that functions in stem cell control and responds to a CLAVATA3/ESR-related (CLE) peptide expressed in organ primordia. We modeled our results to propose a regulatory system that transmits signals from differentiating cells in organ primordia back to the stem cell niche and that appears to function broadly in the plant kingdom. Furthermore, we demonstrate an application of this new signaling feedback, by showing that weak alleles of fea3 enhance hybrid maize yield traits.

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NCBI Reference Sequence

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Acknowledgements

The fea3-0 allele was kindly provided by V. Shcherbak (Krasnodar Research Institute of Agriculture). We also thank U. Hernandez for assistance with cloning, A. Masson for assistance with peptide assays, and members of the Jackson laboratory for comments on the manuscript. We acknowledge funding from a collaborative agreement with DuPont Pioneer and from NSF Plant Genome Research program grant IOS-1238202 and grant MCB-1027445 and from Agriculture and Food Research Initiative competitive grant 2016-67013-24572 of the USDA National Institute of Food and Agriculture. The study also received support from the Gatsby Charitable Foundation (GAT3395/PR4) and the Swedish Research Council (VR2013-4632) to H.J. and through the Next-Generation BioGreen 21 Program (SSAC; project PJ01184302) from the Rural Development Administration, Republic of Korea.

Author information

Author notes

    • Andrea L Eveland

    Present address: Donald Danforth Plant Science Center, St. Louis, Missouri, USA.

    • Jeremy Gruel
    •  & Young Koung Lee

    These authors contributed equally to this work.

Affiliations

  1. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, New York, USA.

    • Byoung Il Je
    • , Young Koung Lee
    • , Peter Bommert
    • , Edgar Demesa Arevalo
    • , Andrea L Eveland
    • , Qingyu Wu
    • , Alexander Goldshmidt
    •  & David Jackson
  2. Sainsbury Laboratory, University of Cambridge, Cambridge, UK.

    • Jeremy Gruel
    •  & Henrik Jönsson
  3. Agricultural Biotechnology, DuPont Pioneer, Johnston, Iowa, USA.

    • Robert Meeley
  4. Department of Biology, University of Massachusetts, Amherst, Massachusetts, USA.

    • Madelaine Bartlett
  5. Agricultural Biotechnology, DuPont Pioneer, Wilmington, Delaware, USA.

    • Mai Komatsu
    •  & Hajime Sakai
  6. Computational Biology and Biological Physics Group, Lund University, Lund, Sweden.

    • Henrik Jönsson

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Contributions

B.I.J. performed all experimental procedures except for those listed below, prepared figures, and wrote the draft of the manuscript. Y.K.L. and P.B. mapped and cloned FEA3. J.G. performed computational modeling, supervised by H.J. E.D.A. analyzed transactivation lines, using constructs generated by Q.W. A.L.E. performed expression analyses. A.G. performed ZmWUS1 reporter line construction and characterization. R.M. provided the ZmFCP1 mutants. M.B. performed phylogenetic analyses. M.K. and H.S. provided field genetics and mapping support and analysis. D.J. supervised the research and co-wrote the manuscript.

Competing interests

The authors (B.I.J., Y.K.L., D.J., M.K., and H.S., on behalf of Cold Spring Harbor Laboratory and DuPont Pioneer) have obtained patent US20150047071 A1 based in part on this work from the US Patent and Trademark Office.

Corresponding author

Correspondence to David Jackson.

Integrated supplementary information

Supplementary information

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  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–15, Supplementary Table 1 and Supplementary Note.

  2. 2.

    Supplementary Data 2

    Genotype data.

  3. 3.

    Supplementary Data 3

    CLE alignments 2+2.

Excel files

  1. 1.

    Supplementary Table 2

    List of primers and oligonucleotide sequences.

  2. 2.

    Supplementary Table 3

    List of peptides.

  3. 3.

    Supplementary Data 1

    Data corresponding to Supplementary Table 1.

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DOI

https://doi.org/10.1038/ng.3567

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