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MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor

Abstract

Acquisition of cell identity in plants relies strongly on positional information1, hence cell–cell communication and inductive signalling are instrumental for developmental patterning. During Arabidopsis embryogenesis, an extra-embryonic cell is specified to become the founder cell of the primary root meristem, hypophysis, in response to signals from adjacent embryonic cells2. The auxin-dependent transcription factor MONOPTEROS (MP) drives hypophysis specification by promoting transport of the hormone auxin from the embryo to the hypophysis precursor. However, auxin accumulation is not sufficient for hypophysis specification, indicating that additional MP-dependent signals are required3. Here we describe the microarray-based isolation of MP target genes that mediate signalling from embryo to hypophysis. Of three direct transcriptional target genes, TARGET OF MP 5 (TMO5) and TMO7 encode basic helix–loop–helix (bHLH) transcription factors that are expressed in the hypophysis-adjacent embryo cells, and are required and partially sufficient for MP-dependent root initiation. Importantly, the small TMO7 transcription factor moves from its site of synthesis in the embryo to the hypophysis precursor, thus representing a novel MP-dependent intercellular signal in embryonic root specification.

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Figure 1: Identification of TARGET OF MONOPTEROS (TMO ) genes.
Figure 2: TMO genes are direct MP targets.
Figure 3: TMO5 and TMO7 act downstream of MP in root initiation.
Figure 4: TMO5 and TMO7 proteins perform spatially separate functions during root formation.

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

The microarray dataset is deposited in the Gene Expression Omnibus (GEO) with accession number GSE13881.

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Acknowledgements

We acknowledge P. van Oorschot, A. van Haperen and S. Heilbronner for technical assistance, C. Arsene for plant care, S. de Folter and O. Mathieu for advice on ChIP, M. Wunderlich and G. Bijl for help with qPCR, G. Hooiveld for help with statistical analysis of the microarray data and the Nottingham Arabidopsis Stock Centre for mutant and transgenic seeds. We thank P. Maier, S. de Vries, A. Koltunow, A. Lokerse, S. Saiga, V. Willemsen and M. Tsiantis for discussions and comments on the manuscript. This work was supported by grants from the Netherlands Organization for Scientific Research (NWO; VIDI 864.06.012 to D.W.), from the Deutsche Forschungsgemeinschaft (DFG; SFB446 to G.J.) and the Netherlands Proteomics Centre (NPC; D.W., grant awarded to S. de Vries).

Author Contributions A.S. established conditions for the microarray experiment, which was performed together with M.S., validated the array data by qPCR, generated most transgenic lines for expression analysis and functional studies of TMO genes, which was done together with B.M. M.K. performed in situ hybridizations, J.F. and D.W. performed ChIP, and W.L. generated and analysed TMO7 downregulation and TMO7-LIKE1 reporter lines. B.M. performed MP overexpression, and suspensor-specific TMO7 expression experiments, and generated pMP–GFP lines. E.H.R. identified the suspensor-specific At1g34170 gene, and generated pSUSP-GFP lines. D.W. and G.J. conceived and supervised the study. D.W. wrote the paper with input from G.J., A.S. and B.M.

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Correspondence to Gerd Jürgens or Dolf Weijers.

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Schlereth, A., Möller, B., Liu, W. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916 (2010). https://doi.org/10.1038/nature08836

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