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A regulated auxin minimum is required for seed dispersal in Arabidopsis

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Abstract

Local hormone maxima are essential for the development of multicellular structures and organs. For example, steroid hormones accumulate in specific cell types of the animal fetus to induce sexual differentiation1 and concentration peaks of the plant hormone auxin direct organ initiation and mediate tissue patterning2,3,4. Here we provide an example of a regulated local hormone minimum required during organogenesis. Our results demonstrate that formation of a local auxin minimum is necessary for specification of the valve margin separation layer where Arabidopsis fruit opening takes place. Consequently, ectopic production of auxin, specifically in valve margin cells, leads to a complete loss of proper cell fate determination. The valve margin identity factor INDEHISCENT (IND) is responsible for forming the auxin minimum by coordinating auxin efflux in separation-layer cells. We propose that the simplicity of formation and maintenance make local hormone minima particularly well suited to specify a small number of cells such as the stripes at the valve margins.

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Figure 1: An auxin minimum forms at the valve margin of Arabidopsis fruit.
Figure 2: IND regulates auxin transport.
Figure 3: IND mediates PIN delocalization.
Figure 4: IND directly regulates PID and WAG2 expression.

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Acknowledgements

We thank E. York and K. Findlay for assistance on SEM analysis, G. Calder for assistance with confocal microscopy, P. Pople for graphics assistance, and H. F. Klee for the pMON518 plasmid containing the iaaM gene. We also wish to thank G. S. Ditta, L. Dolan, S. Fuentes, J. Kleine-Vehn, R. Sablowski, P. Stephenson and T. Wood for carefully reading the manuscript and constructive criticism. P.R was the recipient of a postdoctoral fellowship from the Spanish government. This work was supported by grants from FWO (Odysseus program) to J.F., from The Netherlands Organisation for Scientific Research (ALW-NWO) to R.O., from the National Science Foundation to M.F.Y., and from the Biotechnological and Biological Sciences Research Council as well as core strategic funds from the John Innes Centre to L.Ø.

Author Contributions This project was conceived by K.S., M.F.Y. and L.Ø. Experiments were designed by K.S. and L.Ø. K.S. performed the confocal microscopy and expression analyses, T.G. carried out the chromatin immunoprecipitations, L.Ø. made the IND::IND:iaaM lines and performed plant sections and tissue staining, K.L. performed the IAA measurements, P.R. made the 35S::IND:GR transgenic line, S.J.L. characterized the 35S::IND lines and took the 35S::IND SEM image shown, and C.S.G.-A., J.F. and R.O. analysed the effect of WAG2 activity on PIN localization. K.S. and L.Ø. analysed the data and wrote the paper.

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Authors and Affiliations

  1. Crop Genetics Department, John Innes Centre, Norwich Research Park, Colney Lane, Norwich, Norfolk NR4 7UH, UK,

    Karim Sorefan, Thomas Girin & Lars Østergaard

  2. Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, California 92093-0116, USA ,

    Sarah J. Liljegren, Pedro Robles & Martin F. Yanofsky

  3. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA,

    Sarah J. Liljegren

  4. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, S-901 83 Umeå, Sweden

    Karin Ljung

  5. División de Genética e Instituto de Bioingeniería, Universidad Miguel Hernández, Campus de Elche, 03202, Alicante, Spain ,

    Pedro Robles

  6. Department of Molecular and Developmental Genetics, Institute of Biology, Leiden University, Wassenaarseweg 64, 2333 AL Leiden, The Netherlands,

    Carlos S. Galván-Ampudia & Remko Offringa

  7. Department of Plant Systems Biology, and Department of Plant Biotechnology and Genetics, VIB, Ghent University, 9052 Gent, Belgium

    Jiří Friml

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  1. Karim Sorefan
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Correspondence to Lars Østergaard.

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Sorefan, K., Girin, T., Liljegren, S. et al. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459, 583–586 (2009). https://doi.org/10.1038/nature07875

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