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Science 313 (5788): 842-845

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

Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation

Yasuko Ito,1* Ikuko Nakanomyo,1* Hiroyasu Motose,1{dagger} Kuninori Iwamoto,1 Shinichiro Sawa,1 Naoshi Dohmae,2 Hiroo Fukuda1{ddagger}

Abstract: In plants and animals, small peptide ligands that signal in cell-cell communication have been suggested to be a crucial component of development. A bioassay of single-cell transdifferentation demonstrates that a dodecapeptide with two hydroxyproline residues is the functional product of genes from the CLE family, which includes CLAVATA3 in Arabidopsis. The dodecapeptide suppresses xylem cell development at a concentration of 10–11 M and promotes cell division. An application, corresponding to all 26 Arabidopsis CLE protein family members, of synthetic dodecapeptides reveals two counteracting signaling pathways involved in stem cell fate.

1 Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
2 Biomolecular Characterization Team, RIKEN, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan.

* These authors contributed equally to this work.

{dagger} Present address: Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo 153-8902, Japan.

{ddagger} To whom correspondence should be addressed. E-mail: fukuda{at}biol.s.u-tokyo.ac.jp


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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. Kinoshita, Y. Nakamura, E. Sasaki, J. Kyozuka, H. Fukuda, and S. Sawa (2007)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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Y. Amano, H. Tsubouchi, H. Shinohara, M. Ogawa, and Y. Matsubayashi (2007)
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   Abstract »    Full Text »    PDF »
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Z. Minic, E. Jamet, L. Negroni, P Arsene der Garabedian, M. Zivy, and L. Jouanin (2007)
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   Abstract »    Full Text »    PDF »
Flowering and determinacy in Arabidopsis.
R. Sablowski (2007)
J. Exp. Bot. 58, 899-907
   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
The Arabidopsis Unannotated Secreted Peptide Database, a Resource for Plant Peptidomics.
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   Abstract »    Full Text »    PDF »
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R. Simon and Y. Stahl (2006)
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   Abstract »    Full Text »    PDF »
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T. Kondo, S. Sawa, A. Kinoshita, S. Mizuno, T. Kakimoto, H. Fukuda, and Y. Sakagami (2006)
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   Abstract »    Full Text »    PDF »

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