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Science 311 (5757): 94-98

Copyright © 2006 by the American Association for the Advancement of Science

Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development

Ari Pekka Mähönen,1 Anthony Bishopp,1* Masayuki Higuchi,2* Kaisa M. Nieminen,1 Kaori Kinoshita,2 Kirsi Törmäkangas,1 Yoshihisa Ikeda,3 Atsuhiro Oka,4 Tatsuo Kakimoto,2{dagger} Ykä Helariutta1,5,6{dagger}

Abstract: The cell lineages that form the transporting tissues (xylem and phloem) and the intervening pluripotent procambial tissue originate from stem cells near the root tip. We demonstrate that in Arabidopsis, cytokinin phytohormones negatively regulate protoxylem specification. AHP6, an inhibitory pseudophosphotransfer protein, counteracts cytokinin signaling, allowing protoxylem formation. Conversely, cytokinin signaling negatively regulates the spatial domain of AHP6 expression. Thus, by controlling the identity of cell lineages, the reciprocal interaction of cytokinin signaling and its spatially specific modulator regulates proliferation and differentiation of cell lineages during vascular development, demonstrating a previously unrecognized regulatory circuit underlying meristem organization.

1 Plant Molecular Biology Laboratory, Institute of Biotechnology, POB 56, FI-00014, University of Helsinki, Finland.
2 Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan.
3 Laboratory of Plant Molecular Biology, Rockefeller University, New York, NY 10021, USA.
4 Laboratory of Molecular Biology, Institute for Chemical Research, Kyoto University, Uji 611-0011, Japan.
5 Department of Biology, FI-20014, University of Turku, Finland.
6 Umeå Plant Science Center, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83, Umeå, Sweden.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: kakimoto{at}bio.sci.osaka-u.ac.jp (T.K.); yhelariu{at}operoni.helsinki.fi (Y.H.)

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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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A. Hahn, R. Zimmermann, D. Wanke, K. Harter, and H. G. Edelmann (2008)
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   Abstract »    Full Text »    PDF »
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K. Ishida, T. Yamashino, A. Yokoyama, and T. Mizuno (2008)
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   Abstract »    Full Text »    PDF »
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B. Parizot, L. Laplaze, L. Ricaud, E. Boucheron-Dubuisson, V. Bayle, M. Bonke, I. De Smet, S. R. Poethig, Y. Helariutta, J. Haseloff, et al. (2008)
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   Abstract »    Full Text »    PDF »
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J. P.C. To, J. Deruere, B. B. Maxwell, V. F. Morris, C. E. Hutchison, F. J. Ferreira, G. E. Schaller, and J. J. Kieber (2007)
PLANT CELL 19, 3901-3914
   Abstract »    Full Text »    PDF »
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L. Laplaze, E. Benkova, I. Casimiro, L. Maes, S. Vanneste, R. Swarup, D. Weijers, V. Calvo, B. Parizot, M. B. Herrera-Rodriguez, et al. (2007)
PLANT CELL 19, 3889-3900
   Abstract »    Full Text »    PDF »
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J. Lopez-Bucio, M. Millan-Godinez, A. Mendez-Bravo, A. Morquecho-Contreras, E. Ramirez-Chavez, J. Molina-Torres, A. Perez-Torres, M. Higuchi, T. Kakimoto, and L. Herrera-Estrella (2007)
Plant Physiology 145, 1703-1713
   Abstract »    Full Text »    PDF »
Involvement of hormones and KNOXI genes in early Arabidopsis seedling development.
P. Soucek, P. Klima, A. Rekova, and B. Brzobohaty (2007)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Advances in Cytokinin Signaling.
B. Muller and J. Sheen (2007)
Science 318, 68-69
   Abstract »    Full Text »    PDF »
Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY.
K. Ohashi-Ito and D. C. Bergmann (2007)
Development 134, 2959-2968
   Abstract »    Full Text »    PDF »
The SERK1 gene is expressed in procambium and immature vascular cells.
M. A. C. J. Kwaaitaal and S. C. de Vries (2007)
J. Exp. Bot. 58, 2887-2896
   Abstract »    Full Text »    PDF »
Abnormal Root and Nodule Vasculature in R50 (sym16), a Pea Nodulation Mutant which Accumulates Cytokinins.
A. N. Pepper, A. P. Morse, and F. C. Guinel (2007)
Ann. Bot. 99, 765-776
   Abstract »    Full Text »    PDF »
Overexpression of a Type-A Response Regulator Alters Rice Morphology and Cytokinin Metabolism.
N. Hirose, N. Makita, M. Kojima, T. Kamada-Nobusada, and H. Sakakibara (2007)
Plant Cell Physiol. 48, 523-539
   Abstract »    Full Text »    PDF »
Type-B ARR Transcription Factors, ARR10 and ARR12, are Implicated in Cytokinin-Mediated Regulation of Protoxylem Differentiation in Roots of Arabidopsis thaliana.
A. Yokoyama, T. Yamashino, Y.-I. Amano, Y. Tajima, A. Imamura, H. Sakakibara, and T. Mizuno (2007)
Plant Cell Physiol. 48, 84-96
   Abstract »    Full Text »    PDF »
The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis Regulates CUP-SHAPED COTYLEDON 1 at the Transcriptional Level and Controls Cotyledon Development.
Y. Ikeda, H. Banno, Q.-W. Niu, S. H. Howell, and N.-H. Chua (2006)
Plant Cell Physiol. 47, 1443-1456
   Abstract »    Full Text »    PDF »
The Arabidopsis Histidine Phosphotransfer Proteins Are Redundant Positive Regulators of Cytokinin Signaling.
C. E. Hutchison, J. Li, C. Argueso, M. Gonzalez, E. Lee, M. W. Lewis, B. B. Maxwell, T. D. Perdue, G. E. Schaller, J. M. Alonso, et al. (2006)
PLANT CELL 18, 3073-3087
   Abstract »    Full Text »    PDF »
Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis.
K. Miyawaki, P. Tarkowski, M. Matsumoto-Kitano, T. Kato, S. Sato, D. Tarkowska, S. Tabata, G. Sandberg, and T. Kakimoto (2006)
PNAS 103, 16598-16603
   Abstract »    Full Text »    PDF »
Galactoglucomannans Increase Cell Population Density and Alter the Protoxylem/Metaxylem Tracheary Element Ratio in Xylogenic Cultures of Zinnia.
A. Benova-Kakosova, C. Digonnet, F. Goubet, P. Ranocha, A. Jauneau, E. Pesquet, O. Barbier, Z. Zhang, P. Capek, P. Dupree, et al. (2006)
Plant Physiology 142, 696-709
   Abstract »    Full Text »    PDF »
The genome of black cottonwood, Populus trichocarpa (Torr. & Gray)..
G. A. Tuskan, S. DiFazio, S. Jansson, J. Bohlmann, I. Grigoriev, U. Hellsten, N. Putnam, S. Ralph, S. Rombauts, A. Salamov, et al. (2006)
Science 313, 1596-1604
   Abstract »    Full Text »    PDF »
Signs of change: hormone receptors that regulate plant development..
A. Bishopp, A. P. Mahonen, and Y. Helariutta (2006)
Development 133, 1857-1869
   Abstract »    Full Text »    PDF »

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