Play all audios:
ABSTRACT 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
through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal
Receive 51 print issues and online access $199.00 per year only $3.90 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may
be subject to local taxes which are calculated during checkout ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support
SIMILAR CONTENT BEING VIEWED BY OTHERS COORDINATION OF SHOOT APICAL MERISTEM SHAPE AND IDENTITY BY APETALA2 DURING FLORAL TRANSITION IN ARABIDOPSIS Article Open access 13 August 2024
SPECIFICATION OF LEAF DORSIVENTRALITY VIA A PREPATTERNED BINARY READOUT OF A UNIFORM AUXIN INPUT Article 22 March 2022 A NETWORK OF CLAVATA RECEPTORS BUFFERS AUXIN-DEPENDENT MERISTEM
MAINTENANCE Article 07 August 2023 REFERENCES * Jean, R. _Phyllotaxis: A Systemic Study in Plant Morphogenesis_ (Cambridge Univ. Press, Cambridge, UK, 1994) Book Google Scholar *
Kuhlemeier, C. & Reinhardt, D. Auxin and phyllotaxis. _Trends Plant Sci._ 6, 87–189 (2001) Article Google Scholar * Klar, A. Fibonacci's flowers. _Nature_ 417, 595 (2002) Article
ADS CAS Google Scholar * Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. _Nature_ 426, 255–260 (2003) Article ADS CAS Google Scholar * Jackson, D. &
Hake, S. Control of phyllotaxy in maize by the _ABPHYL1_ gene. _Development_ 126, 315–323 (1999) CAS PubMed Google Scholar * Skoog, F. & Miller, C. O. Chemical regulation of growth
and organ formation in plant tissues cultured _in vitro_. _Symp. Soc. Exp. Biol._ 11, 118–131 (1957) CAS PubMed Google Scholar * Mok, D. W. & Mok, M. C. Cytokinin metabolism and
action. _Annu. Rev. Plant Physiol. Plant Mol. Biol._ 52, 89–118 (2001) Article MathSciNet CAS Google Scholar * Sheen, J. Phosphorelay and transcription control in cytokinin signal
transduction. _Science_ 296, 1650–1652 (2002) Article ADS CAS Google Scholar * Hutchison, C. E. & Kieber, J. J. Cytokinin signaling in _Arabidopsis_. _Plant Cell_ 14(suppl.), S47–S59
(2002) Article CAS Google Scholar * Lohrmann, J. 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) Article CAS Google Scholar * Hwang, I. & Sheen, J. Two-component circuitry in _Arabidopsis_ cytokinin
signal transduction. _Nature_ 413, 383–389 (2001) Article ADS CAS Google Scholar * Sakai, H. et al. ARR1, a transcription factor for genes immediately responsive to cytokinins. _Science_
294, 1519–1521 (2001) Article ADS CAS Google Scholar * To, J. P. C. 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 * Greyson, R. I., Walden, D. B., Hume, J. A. & Erickson, R. O. 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) Article Google Scholar * Robertson, D., Stinard, P. & Maguire, M. Genetic evidence of
Mutator-induced deletions in the short arm of chromosome 9 of maize. II. wd deletions. _Genetics_ 136, 1143–1149 (1994) CAS PubMed PubMed Central Google Scholar * Asakura, Y. 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) Article CAS Google Scholar * Falke, J., Bass, R., Butler, S., Cherviotz, S. & Danielson, M. The two component signaling pathway of
bacterial chemotaxis. _Annu. Rev. Cell Dev. Biol._ 13, 437–512 (1997) Article Google Scholar * 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 * D'Agostino, I. B., Deruere, J. &
Kieber, J. J. Characterization of the response of the _Arabidopsis_ response regulator gene family to cytokinin. _Plant Phys._ 124, 1706–1717 (2000) Article CAS Google Scholar * Che, P.,
Gingerich, D. J., Lall, S. & Howell, S. H. Global and hormone-induced gene expression changes during shoot development in _Arabidopsis_. _Plant Cell_ 14, 2771–2785 (2002) Article CAS
Google Scholar * Brandstatter, I. & Kieber, J. J. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in _Arabidopsis_. _Plant
Cell_ 10, 1009–1019 (1998) Article CAS Google Scholar * Sakakibara, H. et al. A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in
maize. _Plant J._ 14, 337–344 (1998) Article CAS Google Scholar * Taniguchi, M. et al. Expression of _Arabidopsis_ response regulator homologs is induced by cytokinins and nitrate. _FEBS
Lett._ 429, 259–262 (1998) Article CAS Google Scholar * Werner, T., Motyka, V., Strnad, M. & Schmèulling, T. Regulation of plant growth by cytokinin. _Proc. Natl Acad. Sci. USA_ 98,
10487–10492 (2001) Article ADS CAS Google Scholar * Chaudhury, A. M., Letham, S., Craig, S. & Dennis, E. S. 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) Article CAS Google Scholar * Helliwell, C. A. et al. The _Arabidopsis_
AMP1 gene encodes a putative glutamate carboxypeptidase. _Plant Cell_ 13, 2115–2125 (2001) Article CAS Google Scholar * Schwabe, W. W. in _Positional Controls In Plant Development_ (eds
Barlow, P. W. & Carr, D. J.) (Cambridge Univ. Press, 1984) Google Scholar * Callos, J. D. & Medford, J. I. Organ positions and pattern formation in the shoot apex. _Plant J._ 6, 1–7
(1994) Article Google Scholar * Green, P. B. Connecting gene and hormone action to form, pattern and organogenesis; biophysical transductions. _J. Exp. Bot._ 45, 1775–1788 (1994) Article
CAS Google Scholar * Taguchi-Shiobara, F., Yuan, Z., Hake, S. & Jackson, D. 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) Article CAS Google Scholar Download references ACKNOWLEDGEMENTS 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 AUTHORS AND AFFILIATIONS
* Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York, 11724, USA Anna Giulini, Jing Wang & David Jackson Authors * Anna Giulini View author publications You
can also search for this author inPubMed Google Scholar * Jing Wang View author publications You can also search for this author inPubMed Google Scholar * David Jackson View author
publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to David Jackson. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare
that they have no competing financial interests. SUPPLEMENTARY INFORMATION 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. (DOC 687 kb) RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE
Giulini, A., Wang, J. & Jackson, D. Control of phyllotaxy by the cytokinin-inducible response regulator homologue _ABPHYL1_. _Nature_ 430, 1031–1034 (2004).
https://doi.org/10.1038/nature02778 Download citation * Received: 25 April 2004 * Accepted: 22 June 2004 * Issue Date: 26 August 2004 * DOI: https://doi.org/10.1038/nature02778 SHARE THIS
ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard
Provided by the Springer Nature SharedIt content-sharing initiative