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MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor

Nature volume 464, pages 913–916 (2010)Cite this article

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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.

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Primary accessions

Gene Expression Omnibus

Data deposits

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

References

  1. Scheres, B. Plant cell identity. The role of position and lineage. Plant Physiol. 125, 112–114 (2001)

    Article  CAS  Google Scholar 

  2. Hamann, T., Mayer, U. & Jürgens, G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387–1395 (1999)

    Article  CAS  Google Scholar 

  3. Weijers, D. et al. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265–270 (2006)

    Article  CAS  Google Scholar 

  4. Weigel, D. & Jürgens, G. Stem cells that make stems. Nature 415, 751–754 (2002)

    Article  ADS  CAS  Google Scholar 

  5. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998)

    Article  CAS  Google Scholar 

  6. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Activation and repression of transcription by auxin-response factors. Proc. Natl Acad. Sci. USA 96, 5844–5849 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Hamann, T., Benkova, E., Bäurle, I., Kientz, M. & Jürgens, G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610–1615 (2002)

    Article  CAS  Google Scholar 

  8. Dharmasiri, N. et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109–119 (2005)

    Article  CAS  Google Scholar 

  9. Weijers, D. et al. Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. 24, 1874–1885 (2005)

    Article  CAS  Google Scholar 

  10. Tian, Q., Uhlir, N. J. & Reed, J. W. Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14, 301–319 (2002)

    Article  CAS  Google Scholar 

  11. Okushima, Y. et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17, 444–463 (2005)

    Article  CAS  Google Scholar 

  12. Riechmann, J. L. et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110 (2000)

    Article  ADS  CAS  Google Scholar 

  13. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A. & Tasaka, M. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis . Plant Cell 19, 118–130 (2007)

    Article  CAS  Google Scholar 

  14. Donner, T. J., Sherr, I. & Scarpella, E. Regulation of preprocambial cell state acquisition by auxin signalling in Arabidopsis leaves. Development 136, 3235–3246 (2009)

    Article  CAS  Google Scholar 

  15. Galinha, C. et al. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053–1057 (2007)

    Article  ADS  CAS  Google Scholar 

  16. Rashotte, A. M. et al. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl Acad. Sci. USA 103, 11081–11085 (2006)

    Article  ADS  CAS  Google Scholar 

  17. Lee, S. et al. Overexpression of PRE1 and its homologous genes activates gibberellin-dependent responses in Arabidopsis thaliana . Plant Cell Physiol. 47, 591–600 (2006)

    Article  CAS  Google Scholar 

  18. Wang, H. et al. Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 21, 3781–3791 (2009)

    Article  CAS  Google Scholar 

  19. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Dimerization and DNA binding of auxin response factors. Plant J. 19, 309–319 (1999)

    Article  CAS  Google Scholar 

  20. Cole, M. et al. DORNRÖSSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development 136, 1643–1651 (2009)

    Article  CAS  Google Scholar 

  21. Toledo-Ortiz, G., Huq, E. & Quail, P. H. The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749–1770 (2003)

    Article  CAS  Google Scholar 

  22. Nakajima, K., Sena, G., Nawy, T. & Benfey, P. N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311 (2001)

    Article  ADS  CAS  Google Scholar 

  23. Massari, M. E. & Murre, C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20, 429–440 (2000)

    Article  CAS  Google Scholar 

  24. Takada, S. & Jürgens, G. Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134, 1141–1150 (2007)

    Article  CAS  Google Scholar 

  25. Wesley, S. V. et al. Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581–590 (2001)

    Article  CAS  Google Scholar 

  26. Weijers, D. et al. An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128, 4289–4299 (2001)

    Article  CAS  Google Scholar 

  27. Schwab, R., Ossowski, S., Riester, M., Warthmann, N. & Weigel, D. Highly specific gene silencing by artificial microRNAs in Arabidopsis . Plant Cell 18, 1121–1133 (2006)

    Article  CAS  Google Scholar 

  28. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . Plant J. 16, 735–743 (1998)

    Article  CAS  Google Scholar 

  29. van den Bosch, H. M. et al. Gene expression of transporters and phase I/II metabolic enzymes in murine small intestine during fasting. BMC Genomics 8, 267 (2007)

    Article  Google Scholar 

  30. Wu, Z., Irizarry, R. A., Gentleman, R., Martinez-Murillo, F. & Spencer, F. A model-based background adjustment for oligonucleotide expression arrays. J. Am. Stat. Assoc. 99, 909–917 (2004)

    Article  MathSciNet  MATH  Google Scholar 

  31. Dai, M. et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175 (2005)

    Article  Google Scholar 

  32. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article–3 (2004)

    Article  MathSciNet  MATH  Google Scholar 

  33. Sartor, M. A. et al. Intensity-based hierarchical Bayes method improves testing for differentially expressed genes in microarray experiments. BMC Bioinformatics 7, 538 (2006)

    Article  Google Scholar 

  34. Leibfried, A. et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172–1175 (2005)

    Article  ADS  CAS  Google Scholar 

  35. Aker, J., Borst, J. W., Karlova, R. & de Vries, S. C. The Arabidopsis AAA protein CDC48A interacts in vivo with the somatic embryogenesis receptor-like kinase 1 receptor at the plasma membrane. J. Struct. Biol. 156, 62–71 (2006)

    Article  CAS  Google Scholar 

  36. Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997)

    Article  CAS  Google Scholar 

Download references

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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  1. Alexandra Schlereth

    Present address: Present address: Syngenta Crop Protection, CH-4332 Stein, Switzerland.,

Authors and Affiliations

  1. Entwicklungsgenetik, Zentrum für Molekularbiologie der Pflanzen (ZMBP), Universität Tübingen, Auf der Morgenstelle 3, 72076 Tübingen, Germany ,

    Alexandra Schlereth, Marika Kientz, Gerd Jürgens & Dolf Weijers

  2. Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, 6703 HA Wageningen, the Netherlands ,

    Barbara Möller, Weilin Liu, Jacky Flipse, Eike H. Rademacher & Dolf Weijers

  3. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Spemannstrasse 37–39, 72076 Tübingen, Germany,

    Markus Schmid

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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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