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Intercellular movement of the putative transcription factor SHR in root patterning

Abstract

Positional information is pivotal for establishing developmental patterning in plants1,2,3, but little is known about the underlying signalling mechanisms. The Arabidopsis root radial pattern is generated through stereotyped division of initial cells and the subsequent acquisition of cell fate4. short-root (shr) mutants do not undergo the longitudinal cell division of the cortex/endodermis initial daughter cell, resulting in a single cell layer with only cortex attributes5,6. Thus, SHR is necessary for both cell division and endodermis specification5,6. SHR messenger RNA is found exclusively in the stele cells internal to the endodermis and cortex, indicating that it has a non-cell-autonomous mode of action6. Here we show that the SHR protein, a putative transcription factor, moves from the stele to a single layer of adjacent cells, where it enters the nucleus. Ectopic expression of SHR driven by the promoter of the downstream gene SCARECROW (SCR) results in autocatalytic reinforcement of SHR signalling, producing altered cell fates and multiplication of cell layers. These results support a model in which SHR protein acts both as a signal from the stele and as an activator of endodermal cell fate and SCR-mediated cell division.

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Figure 1: SHR protein localization.
Figure 2: Analysis of SCRpro::SHR transgenic roots.
Figure 3: Correlation between the presence of SHR protein and cell fates in SCRpro::SHR roots.
Figure 4: SCR acts downstream of SHR.

References

  1. van den Berg, C., Willemsen, V., Hage, W., Weisbeek, P. & Scheres, B. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378, 62–65 (1995).

    Article  ADS  CAS  Google Scholar 

  2. van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P. & Scheres, B. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287–289 (1997).

    Article  ADS  CAS  Google Scholar 

  3. Kidner, C., Sundaresan, V., Roberts, K. & Dolan, L. Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate. Planta 211, 191–199 (2000).

    Article  CAS  Google Scholar 

  4. Dolan, L. et al. Cellular organisation of the Arabidopsis thaliana root. Development 119, 71–84 (1993).

    CAS  Google Scholar 

  5. Benfey, P. N. et al. Root development in Arabidopsis: Four mutants with dramatically altered root morphogenesis. Development 119, 57–70 (1993).

    CAS  Google Scholar 

  6. Helariutta, Y. et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000).

    Article  CAS  Google Scholar 

  7. Di Laurenzio, L. et al. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423–433 (1996).

    Article  CAS  Google Scholar 

  8. Knox, J. P., Linstead, P. J., King, J., Cooper, C. & Roberts, K. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apieces. Planta 181, 512–521 (1990).

    Article  CAS  Google Scholar 

  9. Freshour, G. et al. Developmental and tissue-specific structural alterations of the cell wall polysaccharides of Arabidopsis thaliana roots. Plant Physiology 110, 1413–1429 (1996).

    Article  CAS  Google Scholar 

  10. Esau, K. Anatomy of Seed Plants 215–242 (Wiley, New York, 1977).

    Google Scholar 

  11. Malamy, J. & Benfey, P. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33–44 (1997).

    CAS  Google Scholar 

  12. Masucci, J. D. et al. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253–1260 (1996).

    CAS  Google Scholar 

  13. Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999).

    Article  CAS  Google Scholar 

  14. Lucas, W. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983 (1995).

    Article  ADS  CAS  Google Scholar 

  15. Perbal, M., Haughn, G., Saedler, H. & Schwarz-Sommer, Z. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122, 3433–3441 (1996).

    CAS  Google Scholar 

  16. Sessions, A., Yanofsky, M. F. & Weigel, D. Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 287, 419–421 (2000).

    Article  Google Scholar 

  17. Jackson, D., Veit, B. & Hake, S. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120, 405–413 (1994).

    CAS  Google Scholar 

  18. von Arnim, A. G., Deng, X.-W. & Stacey, M. G. Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene 221, 35–43 (1998).

    Article  CAS  Google Scholar 

  19. 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 

  20. Wysocka-Diller, J., Helariutta, Y., Fukaki, H., Malamy, J. & Benfey, P. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127, 595–603 (2000).

    CAS  Google Scholar 

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Acknowledgements

We thank K. Roberts for the JIM13 antibody; M. Hahn for the CCRC-M2 antibody; B. Scheres for the QC46 marker line; J. Schiefelbein for the GL2::GUS line; A. von Arnim for the GFP plasmid; M. Aida for the pBIH vector; and M. Starz for the assistance with confocal microscopy. Multi-photon confocal images were taken with assistance by J. Feijo and N. Moreno. K.N. was supported by a fellowship from Japan Society for the Promotion of Science. This work was supported by a grant to P.N.B. from the NIH.

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Correspondence to Philip N. Benfey.

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3 figures with legends

Video 1

Three-dimensional reconstruction of the root tip of the SHR::GFP fusion protein line, obtained through sequential longitudinal multiphoton optical sections.

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Nakajima, K., Sena, G., Nawy, T. et al. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311 (2001). https://doi.org/10.1038/35095061

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