The development of multicellular organisms relies on the coordinated control of cell divisions leading to proper patterning and growth1,2,3. The molecular mechanisms underlying pattern formation, particularly the regulation of formative cell divisions, remain poorly understood. In Arabidopsis, formative divisions generating the root ground tissue are controlled by SHORTROOT (SHR) and SCARECROW (SCR)4,5,6. Here we show, using cell-type-specific transcriptional effects of SHR and SCR combined with data from chromatin immunoprecipitation-based microarray experiments, that SHR regulates the spatiotemporal activation of specific genes involved in cell division. Coincident with the onset of a specific formative division, SHR and SCR directly activate a D-type cyclin; furthermore, altering the expression of this cyclin resulted in formative division defects. Our results indicate that proper pattern formation is achieved through transcriptional regulation of specific cell-cycle genes in a cell-type- and developmental-stage-specific context. Taken together, we provide evidence for a direct link between developmental regulators, specific components of the cell-cycle machinery and organ patterning.
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Lewis, J. From signals to patterns: space, time, and mathematics in developmental biology. Science 322, 399–403 (2008)
Herranz, H. & Milan, M. Signalling molecules, growth regulators and cell cycle control in Drosophila. Cell Cycle 7, 3335–3337 (2008)
Blilou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005)
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)
Helariutta, Y. et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000)
Heidstra, R., Welch, D. & Scheres, B. Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 18, 1964–1969 (2004)
Foe, V. E. Mitotic domains reveal early commitment of cells in Drosophila embryos. Development 107, 1–22 (1989)
Hartwell, L. H. & Kastan, M. B. Cell cycle control and cancer. Science 266, 1821–1828 (1994)
Schiefelbein, J. Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74–78 (2003)
Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003)
Aida, M. et al. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120 (2004)
Wu, L. et al. The E2F1–3 transcription factors are essential for cellular proliferation. Nature 414, 457–462 (2001)
Blilou, I. et al. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev. 16, 2566–2575 (2002)
Andersen, S. U. et al. Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20, 88–100 (2008)
Ebel, C., Mariconti, L. & Gruissem, W. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429, 776–780 (2004)
Weigmann, K., Cohen, S. M. & Lehner, C. F. Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. Development 124, 3555–3563 (1997)
De Smet, I. et al. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322, 594–597 (2008)
Benfey, P. N. et al. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119, 57–70 (1993)
Pysh, L. D., Wysocka-Diller, J. W., Camilleri, C., Bouchez, D. & Benfey, P. N. The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18, 111–119 (1999)
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)
Gallagher, K. L., Paquette, A. J., Nakajima, K. & Benfey, P. N. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847–1851 (2004)
Gallagher, K. L. & Benfey, P. N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 57, 785–797 (2009)
Sabatini, S., Heidstra, R., Wildwater, M. & Scheres, B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354–358 (2003)
Levesque, M. P. et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4 e143 10.1371/journal.pbio.0040143 (2006)
Cui, H. et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425 (2007)
Birnbaum, K. et al. A gene expression map of the Arabidopsis root. Science 302, 1956–1960 (2003)
Paquette, A. J. & Benfey, P. N. Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol. 138, 636–640 (2005)
Menges, M., de Jager, S. M., Gruissem, W. & Murray, J. A. Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 41, 546–566 (2005)
Brady, S. M. et al. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801–806 (2007)
Haseloff, J. GFP variants for multispectral imaging of living cells. Methods Cell Biol. 58, 139–151 (1998)
Fukaki, H. et al. Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J. 14, 425–430 (1998)
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998)
Bougourd, S., Marrison, J. & Haseloff, J. Technical advance: an aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryos. Plant J. 24, 543–550 (2000)
Casamitjana-Martinez, E. et al. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 13, 1435–1441 (2003)
Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004)
Tusher, V. G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA 98, 5116–5121 (2001)
Orlando, D. A., Brady, S. M., Koch, J. D., Dinneny, J. R. & Benfey, P. N. Manipulating large scale Arabidopsis microarray expression data: identifying dominant expression patterns and biological process enrichment. Methods Mol. Biol. 553, 57–77 (2009)
Busch, W. et al. Transcriptional control of a plant stem cell niche. Dev. Cell 18, 849–861 (2010)
We thank D. Orlando and R. Twigg for generating the list of probes for the ChIP-array; J. Nieuwland, S. Maughan and C. Collins for construction of the CYCD6;1 reporter line and assistance in isolation of the cycd6;1 mutant; L. Sanz, F. Patell and S. Scofield for isolation of the cycd2;1 and cycd5;1 mutants; J. Dinneny, M. Noor and members of the Benfey laboratory for their comments on the manuscript. Funding to M.A.M.-R. is provided by the Ministerio de Ciencia y Innovacion (Spain). W.D. and J.A.H.M. were funded by a Biotechnology and Biological Sciences Research Council grant (BB/E022383) and the European Research Area in Plant Genomics network on Plant Stem Cells (BB/E024858). This work was funded by grants to P.N.B. from the NIH (RO1-GM043778 and P50-GM081883) and from the NSF (AT2010 0618304).
The authors declare no competing financial interests.
This file contains legends for Supplementary Tables S1-S13, legends for Supplementary Movies 1-2, Supplementary References, Supplementary Figures S1-S18 with legends, and Supplementary Tables S1-S13. (PDF 9417 kb)
This movie shows the in vivo periclinal divisions occurring in pSHR::SHR:GR shr-2-J0571 plants treated for 6 hours with Dex (see Supplementary Information file for full legend). (MOV 743 kb)
This movie shows Col-0 and cycd6;1 seed germination. To monitor seed germination, images were taken with an infrared camera every 15’ for 48 hours (see Supplementary Information file for full legend). (MOV 2152 kb)
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Sozzani, R., Cui, H., Moreno-Risueno, M. et al. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466, 128–132 (2010). https://doi.org/10.1038/nature09143
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