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Hormonal control of the shoot stem-cell niche

Abstract

The classic phytohormones cytokinin and auxin play essential roles in the maintenance of stem-cell systems embedded in shoot and root meristems, and exhibit complex functional interactions1,2,3,4. Here we show that the activity of both hormones directly converges on the promoters of two A-type ARABIDOPSIS RESPONSE REGULATOR (ARR) genes, ARR7 and ARR15, which are negative regulators of cytokinin signalling5 and have important meristematic functions3. Whereas ARR7 and ARR15 expression in the shoot apical meristem (SAM) is induced by cytokinin, auxin has a negative effect, which is, at least in part, mediated by the AUXIN RESPONSE FACTOR5/MONOPTEROS (MP) transcription factor6. Our results provide a mechanistic framework for hormonal control of the apical stem-cell niche and demonstrate how root and shoot stem-cell systems differ in their response to phytohormones.

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Figure 1: ARR15 and ARR7 have important roles for SAM regulation.
Figure 2: Interaction of ARR7 and ARR15 with auxin signalling.
Figure 3: Regulatory and functional interaction of ARR15 and ARF5/MONOPTEROS.
Figure 4: Cross talk between auxin and cytokinin affects the stem-cell niche.

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References

  1. Müller, B. & Sheen, J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094–1097 (2008)

    Article  ADS  Google Scholar 

  2. Gordon, S. P., Chickarmane, V. S., Ohno, C. & Meyerowitz, E. M. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl Acad. Sci. USA 106, 16529–16534 (2009)

    Article  ADS  CAS  Google Scholar 

  3. 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 

  4. Heisler, M. G. et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15, 1899–1911 (2005)

    Article  CAS  Google Scholar 

  5. To, J. P. et al. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16, 658–671 (2004)

    Article  CAS  Google Scholar 

  6. 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 

  7. Mayer, K. F. et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815 (1998)

    Article  CAS  Google Scholar 

  8. Fletcher, J. C., Brand, U., Running, M. P., Simon, R. & Meyerowitz, E. M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911–1914 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644 (2000)

    Article  CAS  Google Scholar 

  10. Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. & Simon, R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617–619 (2000)

    Article  ADS  CAS  Google Scholar 

  11. Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M. & Matsubayashi, Y. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chem. Biol. 5, 578–580 (2009)

    Article  CAS  Google Scholar 

  12. Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003)

    Article  ADS  CAS  Google Scholar 

  13. Kurakawa, T. et al. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445, 652–655 (2007)

    Article  CAS  Google Scholar 

  14. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. & Murray, J. A. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541–1544 (1999)

    Article  ADS  CAS  Google Scholar 

  15. Giulini, A., Wang, J. & Jackson, D. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430, 1031–1034 (2004)

    Article  ADS  CAS  Google Scholar 

  16. Dello Ioio, R. et al. A genetic framework for the control of cell division and differentiation in the root meristem. Science 322, 1380–1384 (2008)

    Article  ADS  CAS  Google Scholar 

  17. 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 

  18. Cheng, Y., Dai, X. & Zhao, Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 20, 1790–1799 (2006)

    Article  CAS  Google Scholar 

  19. Yanai, O. et al. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566–1571 (2005)

    Article  CAS  Google Scholar 

  20. Jasinski, S. et al. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15, 1560–1565 (2005)

    Article  CAS  Google Scholar 

  21. Furutani, M. et al. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131, 5021–5030 (2004)

    Article  CAS  Google Scholar 

  22. Kieber, J. J. in The Arabidopsis Book (American Society of Plant Biologists, 2002)

    Google Scholar 

  23. Hwang, I. & Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383–389 (2001)

    Article  ADS  CAS  Google Scholar 

  24. Schmid, M. et al. A gene expression map of Arabidopsis thaliana development. Nature Genet. 37, 501–506 (2005)

    Article  MathSciNet  CAS  Google Scholar 

  25. Guilfoyle, T. J. & Hagen, G. Auxin response factors. Curr. Opin. Plant Biol. 10, 453–460 (2007)

    Article  CAS  Google Scholar 

  26. Schlereth, A. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–917 (2010)

    Article  ADS  CAS  Google Scholar 

  27. Skoog, F. & Miller, C. O. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 54, 118–130 (1957)

    Google Scholar 

  28. Vidaurre, D. P., Ploense, S., Krogan, N. T. & Berleth, T. AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134, 2561–2567 (2007)

    Article  CAS  Google Scholar 

  29. Andersen, S. U. et al. Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20, 88–100 (2008)

    Article  CAS  Google Scholar 

  30. 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 

  31. Weigel, D. & Glazebrook, J. Arabidopsis: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 2002)

    Google Scholar 

  32. Wu, Z., Irizarry, R., 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  Google Scholar 

  33. Speed, T. P. Statistical Analysis of Gene Expression Microarray Data (CRC Press, 2003)

    Book  Google Scholar 

  34. Nordstrom, A. et al. Derivatization for LC-electrospray ionization-MS: a tool for improving reversed-phase separation and ESI responses of bases, ribosides, and intact nucleotides. Anal. Chem. 76, 2869–2877 (2004)

    Article  Google Scholar 

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Acknowledgements

We thank G. Jürgens, K. Schneitz and D. Weigel for reading the manuscript, and I. Weißwange for imaging. This work was supported by a Human Frontier Science Program Career Development Award, an EMBO Young Investigator Award, the SFB446 (all to J.U.L.), a Carlsberg Foundation fellowship (to S.U.A.), a Czech Ministry of Education grant (MSM 6198959216) (to K.D.) and the Max Planck Society.

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Contributions

S.U.A. established the AM7/15 line and performed the microarray experiment, K.L. and K.D. quantified cytokinin content, A.M. performed ChIP experiments, S.J.S performed bioinformatic analyses and Z.Z. performed all other experiments. Z.Z and J.U.L. designed experiments and wrote the paper.

Corresponding author

Correspondence to Jan U. Lohmann.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-16 with legends, Supplementary Table 1 and a Reference. (PDF 4262 kb)

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Zhao, Z., Andersen, S., Ljung, K. et al. Hormonal control of the shoot stem-cell niche. Nature 465, 1089–1092 (2010). https://doi.org/10.1038/nature09126

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