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Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis

Abstract

Plant stem-cell pools, the source for all organs, are first established during embryogenesis. It has been known for decades that cytokinin and auxin interact to control organ regeneration in cultured tissue1. Auxin has a critical role in root stem-cell specification in zygotic embryogenesis2,3, but the early embryonic function of cytokinin is obscure4,5,6. Here, we introduce a synthetic reporter to visualize universally cytokinin output in vivo. Notably, the first embryonic signal is detected in the hypophysis, the founder cell of the root stem-cell system. Its apical daughter cell, the precursor of the quiescent centre, maintains phosphorelay activity, whereas the basal daughter cell represses signalling output. Auxin activity levels, however, exhibit the inverse profile. Furthermore, we show that auxin antagonizes cytokinin output in the basal cell lineage by direct transcriptional activation of ARABIDOPSIS RESPONSE REGULATOR genes, ARR7 and ARR15, feedback repressors of cytokinin signalling. Loss of ARR7 and ARR15 function or ectopic cytokinin signalling in the basal cell during early embryogenesis results in a defective root stem-cell system. These results provide a molecular model of transient and antagonistic interaction between auxin and cytokinin critical for specifying the first root stem-cell niche.

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Figure 1: Sensitive and specific response of TCS.
Figure 2: Inverse correlation between cytokinin and auxin signalling.
Figure 3: ARR7 and ARR15 mediate auxin control of cytokinin signalling.
Figure 4: Function of differential phosphorelay output for root stem-cell establishment.

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Acknowledgements

We thank T. Kakimoto and C. Ueguchi for providing ahk mutant seeds; J. Friml for the DR5::GFP plasmid and DR5::GFP seeds; E. Lam for providing the AlcA/AlcR vector; A. Jazwinska for help with mRNA in situ hybridizations; and S. Riku for help with plant growth and protoplast experiments. We also thank C. Ping, S. Howell, Y. Guo, Y. Tan, G. Selvaraj, T. Mizuno, J. Zuo, D. Jackson and J. To for sharing unpublished results. This work was supported by a Fellowship for Prospective Researchers by the Swiss National Science Foundation, a Long Term Fellowship of the International Human Frontier Science Program organization to B.M., and grants from the National Science Foundation and National Institutes of Health to J.S.

Author Contributions B.M. initiated the project, performed the experiments and analysed the data; B.M. and J.S. discussed the results, planned the experiments and wrote the manuscript.

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Correspondence to Bruno Müller or Jen Sheen.

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Müller, B., Sheen, J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094–1097 (2008). https://doi.org/10.1038/nature06943

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