Letter | Published:

Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1

Nature volume 430, pages 10311034 (26 August 2004) | Download Citation



Phyllotaxy describes the geometric pattern of leaves and flowers, and has intrigued botanists and mathematicians for centuries1,2. How these patterns are initiated is poorly understood, and this is partly due to the paucity of mutants3. Signalling by the plant hormone auxin appears to determine the site of leaf initiation; however, this observation does not explain how distinct patterns of phyllotaxy are initiated4. abphyl1 (abph1) mutants of maize initiate leaves in a decussate pattern (that is, paired at 180°), in contrast to the alternating or distichous phyllotaxy observed in wild-type maize and other grasses5. Here we show that ABPH1 is homologous to two-component response regulators and is induced by the plant hormone cytokinin. ABPH1 is expressed in the embryonic shoot apical meristem, and its spatial expression pattern changes rapidly with cytokinin treatment. We propose that ABPH1 controls phyllotactic patterning by negatively regulating the cytokinin-induced expansion of the shoot meristem, thereby limiting the space available for primordium initiation at the apex.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

    Phyllotaxis: A Systemic Study in Plant Morphogenesis (Cambridge Univ. Press, Cambridge, UK, 1994)

  2. 2.

    & Auxin and phyllotaxis. Trends Plant Sci. 6, 87–189 (2001)

  3. 3.

    Fibonacci's flowers. Nature 417, 595 (2002)

  4. 4.

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

  5. 5.

    & Control of phyllotaxy in maize by the ABPHYL1 gene. Development 126, 315–323 (1999)

  6. 6.

    & Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11, 118–131 (1957)

  7. 7.

    & Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 89–118 (2001)

  8. 8.

    Phosphorelay and transcription control in cytokinin signal transduction. Science 296, 1650–1652 (2002)

  9. 9.

    & Cytokinin signaling in Arabidopsis. Plant Cell 14(suppl.), S47–S59 (2002)

  10. 10.

    et al. The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Mol. Genet. Genom. 265, 2–13 (2001)

  11. 11.

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

  12. 12.

    et al. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519–1521 (2001)

  13. 13.

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

  14. 14.

    , , & The ABPHYL syndrome in Zea mays. II. Patterns of leaf initiation and the shape of the shoot meristem. Can. J. Bot. 56, 1545–1550 (1978)

  15. 15.

    , & Genetic evidence of Mutator-induced deletions in the short arm of chromosome 9 of maize. II. wd deletions. Genetics 136, 1143–1149 (1994)

  16. 16.

    et al. Molecular characterization of His-Asp phosphorelay signaling factors in maize leaves: Implications of the signal divergence by cytokinin-inducible response regulators in the cytosol and the nuclei. Plant Mol. Biol. 52, 331–341 (2003)

  17. 17.

    , , , & The two component signaling pathway of bacterial chemotaxis. Annu. Rev. Cell Dev. Biol. 13, 437–512 (1997)

  18. 18.

    , & 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)

  19. 19.

    , & Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Phys. 124, 1706–1717 (2000)

  20. 20.

    , , & Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14, 2771–2785 (2002)

  21. 21.

    & Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell 10, 1009–1019 (1998)

  22. 22.

    et al. A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 14, 337–344 (1998)

  23. 23.

    et al. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Lett. 429, 259–262 (1998)

  24. 24.

    , , & Regulation of plant growth by cytokinin. Proc. Natl Acad. Sci. USA 98, 10487–10492 (2001)

  25. 25.

    , , & Amp1—a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J. 4, 907–916 (1993)

  26. 26.

    et al. The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13, 2115–2125 (2001)

  27. 27.

    in Positional Controls In Plant Development (eds Barlow, P. W. & Carr, D. J.) (Cambridge Univ. Press, 1984)

  28. 28.

    & Organ positions and pattern formation in the shoot apex. Plant J. 6, 1–7 (1994)

  29. 29.

    Connecting gene and hormone action to form, pattern and organogenesis; biophysical transductions. J. Exp. Bot. 45, 1775–1788 (1994)

  30. 30.

    , , & The FASCIATED EAR2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15, 2755–2766 (2001)

Download references


We thank V. Chandler for Spm transposon lines, and members of the Jackson laboratory, C. Kidner, E. Vollbrecht and P. Sherwood, for comments on the manuscript. We also thank Z. Yuan and M. Krishnaswami for assistance with genetic screens, DNA isolations and Southern blotting, and T. Mulligan for help with plant propagation. Funding from the National Science Foundation (Plant and Animal Developmental Mechanisms) is also acknowledged.

Author information

Author notes

    • Anna Giulini

    Present address: Department of Plant Production, University of Milan, Via Celoria 2, 20133 Milan, Italy


  1. Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA


  1. Search for Anna Giulini in:

  2. Search for Jing Wang in:

  3. Search for David Jackson in:

Competing interests

The authors declare that they have no competing financial interests.

Corresponding author

Correspondence to David Jackson.

Supplementary information

Word documents

  1. 1.

    Supplementary Data

    This file contains Supplementary Figure S1 (Molecular characterization of abph1 alleles), which shows the molecular analysis of a number of abph1 alleles. These alleles include ones from transposon screens as well as spontaneous alleles. The demonstration of a molecular lesion in the candidate locus for each indicates that this locus encodes ABPH1. Supplementary Figure S2 (in situ hybridization analysis of ABPH1 expression), which shows the expression of ABPH1 by in situ hybridization in a transverse section of a seedling apex. Expression is in an arc of cells in the position of the incipient leaf primordium. Expression throughout the ear inflorescence apical meristem is also shown. Supplementary references are also provided.

About this article

Publication history






Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.