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Science 313 (5788): 845-848

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

A Plant Peptide Encoded by CLV3 Identified by in Situ MALDI-TOF MS Analysis

Tatsuhiko Kondo,1* Shinichiro Sawa,2*{dagger} Atsuko Kinoshita,2 Satoko Mizuno,1 Tatsuo Kakimoto,3 Hiroo Fukuda,2 Youji Sakagami1{dagger}

Abstract: The Arabidopsis CLAVATA3 (CLV3) gene encodes a stem cell–specific protein presumed to be a precursor of a secreted peptide hormone. Matrix-assisted laser desorption/ionization–time-of-flight mass spectrometry (MALDI-TOF MS) applied to in situ Arabidopsis tissues determined the structure of a modified 12–amino acid peptide (MCLV3), which was derived from a conserved motif in the CLV3 sequence. Synthetic MCLV3 induced shoot and root meristem consumption as cells differentiated into other organs, displaying the typical phenotype of transgenic plants overexpressing CLV3. These results suggest that the functional peptide of CLV3 is MCLV3.

1 Graduate School of Bio-Agricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan.
2 Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Tokyo, 113-0033, Japan.
3 Graduate School of Science, Osaka University, Machikaneyama-Cho, Toyonaka, 560-0043, Japan.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: sawa{at}biol.s.u-tokyo.ac.jp (S.S.); ysaka{at}agr.nagoya-u.ac.jp (Y.S.)

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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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   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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