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WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators

Naturevolume 438, pages1172–1175 (2005)Cite this article

Abstract

Plants continuously maintain pools of totipotent stem cells in their apical meristems from which elaborate root and shoot systems are produced. InArabidopsis thaliana, stem cell fate in the shoot apical meristem is controlled by a regulatory network that includes the CLAVATA (CLV) ligand–receptor system and the homeodomain protein WUSCHEL (WUS)1,2. Phytohormones such as auxin and cytokinin are also important for meristem regulation3. Here we show a mechanistic link between the CLV/WUS network and hormonal control. WUS, a positive regulator of stem cells, directly represses the transcription of several two-componentARABIDOPSIS RESPONSE REGULATOR genes (ARR5,ARR6,ARR7 andARR15), which act in the negative-feedback loop of cytokinin signalling4,5. These data indicate thatARR genes might negatively influence meristem size and that their repression by WUS might be necessary for proper meristem function. Consistent with this hypothesis is our observation that a mutantARR7 allele, which mimics the active, phosphorylated form, causes the formation of aberrant shoot apical meristems. Conversely, a loss-of-function mutation in a maizeARR homologue was recently shown to cause enlarged meristems6.

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Figure 1:Expression profiles ofARR5,ARR6,ARR7 andARR15.
Figure 2:Expression patterns ofARR7 andWUS in response to meristematic signals.
Figure 3:Direct interaction of WUS with regulatory sequences ofARR7.
Figure 4:Phenotypes of type-AARR mutant plants.

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Acknowledgements

We thank A. Greenland for providing theAlcA system, J. Palatnik for sharing unpublished results, R. Schwab for establishing thein situ protocol, R. Chen for preparing the WUS antiserum, K. Harter and D. Weigel for discussion, and K. Bomblies, I. Lohmann, M. Schmid, J. Palatnik and D. Weigel for reading the manuscript critically. This work was supported by a Career Development Award of the International Human Frontier Science Program (HFSP) Organization (J.U.L.), a Ph.D. fellowship of the Cusanuswerk (W.B.), grants from the NSF and the NIH (J.J.K.) and the Max Planck Society (J.U.L).Author Contributions A.L. performedin situ hybridizations and qRT–PCRs, constructed reporter genes, the mutated alleles ofARR7 and performed electron microscopy; J.P.C.T. and J.J.K. generated and analysed thearr double and septuple mutants; W.B. performed the ChIP experiments; S.S. generated constructs and transgenic lines ofARR genes; A.K. generatedAlcA::CLV3 plants; M.D. performed qRT–PCRs; and J.U.L. carried out the microarray experiment and analysis, performed gel-shifts and wrote the paper. All authors discussed the results and commented on the manuscript.

Author information

Author notes

  1. Wolfgang Busch and Sandra Stehling: These authors contributed equally to this work

Authors and Affiliations

  1. Max Planck Institute for Developmental Biology, AG Lohmann, D-72076, Tübingen, Germany

    Andrea Leibfried, Wolfgang Busch, Sandra Stehling, Andreas Kehle, Monika Demar & Jan U. Lohmann

  2. Department of Biology, University of North Carolina, North Carolina, 27599, Chapel Hill, USA

    Jennifer P. C. To & Joseph J. Kieber

Authors
  1. Andrea Leibfried
  2. Jennifer P. C. To
  3. Wolfgang Busch
  4. Sandra Stehling
  5. Andreas Kehle
  6. Monika Demar
  7. Joseph J. Kieber
  8. Jan U. Lohmann

Corresponding author

Correspondence toJan U. Lohmann.

Ethics declarations

Competing interests

Microarray data have been deposited at ArrayExpress (http://www.ebi.ac.uk/arrayexpress/) under accession number E-MEXP-432. Reprints and permissions information is available atnpg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

Expression patterns ofARR7 RNA. (PDF 105 kb)

Supplementary Figure 2

Activity ofARR5, ARR6, ARR7 andARR15GUS reporter genes. (PDF 65 kb)

Supplementary Figure 3

Direct interaction of WUS with regulatory sequences ofARR7. (PDF 81 kb)

Supplementary Table 1

Genes responsive toWUSinduction. (PDF 57 kb)

Supplementary Table 2

Oligonucleotides used in Leibfriedet al. (PDF 60 kb)

Supplementary Methods

Additional information on mutants and ChIP. (PDF 68 kb)

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Leibfried, A., To, J., Busch, W.et al. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators.Nature438, 1172–1175 (2005). https://doi.org/10.1038/nature04270

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Editorial Summary

Plant growth controls

In plants the apical meristem at the tip of each shoot contains a population of stem cells ready to proliferate and direct plant growth when they receive the command. Comparative microarray experiments inArabidopsis plants carrying inducible mutations of meristem regulators now show how plant hormones such as cytokinins can communicate with the meristem via a network of transcriptional activators and repressors. The homeobox protein WUSCHEL, known to control stem cell fate, has been found to act directly on a series of signalling proteins previously shown to participate in cytokinin signalling, thus providing a negative feedback loop for maintaining the size of the apical meristem.

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