Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

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} (S.S.); ysaka{at} (Y.S.)

CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner.
T. Araya, M. Miyamoto, J. Wibowo, A. Suzuki, S. Kojima, Y. N. Tsuchiya, S. Sawa, H. Fukuda, N. von Wiren, and H. Takahashi (2014)
PNAS 111, 2029-2034
   Abstract »    Full Text »    PDF »
Message in a bottle: small signalling peptide outputs during growth and development.
N. Czyzewicz, K. Yue, T. Beeckman, and I. D. Smet (2013)
J. Exp. Bot. 64, 5281-5296
   Abstract »    Full Text »    PDF »
Maturing peptides open for communication.
R. B. Aalen (2013)
J. Exp. Bot. 64, 5231-5235
   Full Text »    PDF »
Spatial expression of CLAVATA3 in the shoot apical meristem suggests it is not a stem cell marker in soybean.
C. E. Wong, M. B. Singh, and P. L. Bhalla (2013)
J. Exp. Bot. 64, 5641-5649
   Abstract »    Full Text »    PDF »
The Alteration of Plant Morphology by Small Peptides Released from the Proteolytic Processing of the Bacterial Peptide TENGU.
K. Sugawara, Y. Honma, K. Komatsu, M. Himeno, K. Oshima, and S. Namba (2013)
Plant Physiology 162, 2005-2014
   Abstract »    Full Text »    PDF »
Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3.
S. Depuydt, A. Rodriguez-Villalon, L. Santuari, C. Wyser-Rmili, L. Ragni, and C. S. Hardtke (2013)
PNAS 110, 7074-7079
   Abstract »    Full Text »    PDF »
Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean.
D. E. Reid, D. Li, B. J. Ferguson, and P. M. Gresshoff (2013)
J. Exp. Bot. 64, 1575-1585
   Abstract »    Full Text »    PDF »
ERECTA-Family Receptor Kinases Regulate Stem Cell Homeostasis via Buffering its Cytokinin Responsiveness in the Shoot Apical Meristem.
N. Uchida, M. Shimada, and M. Tasaka (2013)
Plant Cell Physiol. 54, 343-351
   Abstract »    Full Text »    PDF »
Grass Meristems I: Shoot Apical Meristem Maintenance, Axillary Meristem Determinacy and the Floral Transition.
M. Pautler, W. Tanaka, H.-Y. Hirano, and D. Jackson (2013)
Plant Cell Physiol. 54, 302-312
   Abstract »    Full Text »    PDF »
Antagonistic Peptide Technology for Functional Dissection of CLV3/ESR Genes in Arabidopsis.
X.-F. Song, P. Guo, S.-C. Ren, T.-T. Xu, and C.-M. Liu (2013)
Plant Physiology 161, 1076-1085
   Abstract »    Full Text »    PDF »
OrysPSSP: a comparative Platform for Small Secreted Proteins from rice and other plants.
B. Pan, J. Sheng, W. Sun, Y. Zhao, P. Hao, and X. Li (2013)
Nucleic Acids Res. 41, D1192-D1198
   Abstract »    Full Text »    PDF »
WUSCHEL-RELATED HOMEOBOX4 Is Involved in Meristem Maintenance and Is Negatively Regulated by the CLE Gene FCP1 in Rice.
Y. Ohmori, W. Tanaka, M. Kojima, H. Sakakibara, and H.-Y. Hirano (2013)
PLANT CELL 25, 229-241
   Abstract »    Full Text »    PDF »
CLE Signaling Systems During Plant Development and Nematode Infection.
S. Kiyohara and S. Sawa (2012)
Plant Cell Physiol. 53, 1989-1999
   Abstract »    Full Text »    PDF »
Cyclotides Associate with Leaf Vasculature and Are the Products of a Novel Precursor in Petunia (Solanaceae).
A. G. Poth, J. S. Mylne, J. Grassl, R. E. Lyons, A. H. Millar, M. L. Colgrave, and D. J. Craik (2012)
J. Biol. Chem. 287, 27033-27046
   Abstract »    Full Text »    PDF »
Small Signaling Peptides in Arabidopsis Development: How Cells Communicate Over a Short Distance.
E. Murphy, S. Smith, and I. De Smet (2012)
PLANT CELL 24, 3198-3217
   Abstract »    Full Text »    PDF »
The Shoot Apical Meristem Regulatory Peptide CLV3 Does Not Activate Innate Immunity.
C. Segonzac, Z. L. Nimchuk, M. Beck, P. T. Tarr, S. Robatzek, E. M. Meyerowitz, and C. Zipfel (2012)
PLANT CELL 24, 3186-3192
   Abstract »    Full Text »    PDF »
Complexity in Differential Peptide-Receptor Signaling: Response to Segonzac et al. and Mueller et al. Commentaries.
H. Lee, A. Khatri, J. M. Plotnikov, X.-C. Zhang, and J. Sheen (2012)
PLANT CELL 24, 3177-3185
   Full Text »    PDF »
Peptides and receptors controlling root development.
Y. Stahl and R. Simon (2012)
Phil Trans R Soc B 367, 1453-1460
   Abstract »    Full Text »    PDF »
Glycosides of hydroxyproline: Some recent, unusual discoveries.
C. M. Taylor, C. V. Karunaratne, and N. Xie (2012)
Glycobiology 22, 757-767
   Abstract »    Full Text »    PDF »
Chimeric FLS2 Receptors Reveal the Basis for Differential Flagellin Perception in Arabidopsis and Tomato.
K. Mueller, P. Bittel, D. Chinchilla, A. K. Jehle, M. Albert, T. Boller, and G. Felix (2012)
PLANT CELL 24, 2213-2224
   Abstract »    Full Text »    PDF »
Contributions of Individual Amino Acid Residues to the Endogenous CLV3 Function in Shoot Apical Meristem Maintenance in Arabidopsis.
X.-F. Song, D.-L. Yu, T.-T. Xu, S.-C. Ren, P. Guo, and C.-M. Liu (2012)
Mol Plant 5, 515-523
   Abstract »    Full Text »    PDF »
Regulation of Arabidopsis Embryo and Endosperm Development by the Polypeptide Signaling Molecule CLE8.
E. Fiume and J. C. Fletcher (2012)
PLANT CELL 24, 1000-1012
   Abstract »    Full Text »    PDF »
CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis.
L. Meng, B. B. Buchanan, L. J. Feldman, and S. Luan (2012)
PNAS 109, 1760-1765
   Abstract »    Full Text »    PDF »
Stem Cell Signaling in Immunity and Development.
H. Lee, O.- K. Chah, J. Plotnikov, and J. Sheen (2012)
Cold Spring Harb Symp Quant Biol 77, 75-81
   Abstract »    Full Text »    PDF »
WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex.
R. K. Yadav, M. Perales, J. Gruel, T. Girke, H. Jonsson, and G. V. Reddy (2011)
Genes & Dev. 25, 2025-2030
   Abstract »    Full Text »    PDF »
Molecular mechanisms controlling legume autoregulation of nodulation.
D. E. Reid, B. J. Ferguson, S. Hayashi, Y.-H. Lin, and P. M. Gresshoff (2011)
Ann. Bot. 108, 789-795
   Abstract »    Full Text »    PDF »
CLAVATA Signaling Pathway Receptors of Arabidopsis Regulate Cell Proliferation in Fruit Organ Formation as well as in Meristems.
A. R. Durbak and F. E. Tax (2011)
Genetics 189, 177-194
   Abstract »    Full Text »    PDF »
Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean.
M. A. Djordjevic, M. Oakes, C. E. Wong, M. Singh, P. Bhalla, L. Kusumawati, and N. Imin (2011)
J. Exp. Bot. 62, 4649-4659
   Abstract »    Full Text »    PDF »
A Novel Function of TDIF-Related Peptides: Promotion of Axillary Bud Formation.
H. Yaginuma, Y. Hirakawa, Y. Kondo, K. Ohashi-Ito, and H. Fukuda (2011)
Plant Cell Physiol. 52, 1354-1364
   Abstract »    Full Text »    PDF »
Arabidopsis ERECTA-Family Receptor Kinases Mediate Morphological Alterations Stimulated by Activation of NB-LRR-Type UNI Proteins.
N. Uchida, K. Igari, N. L. Bogenschutz, K. U. Torii, and M. Tasaka (2011)
Plant Cell Physiol. 52, 804-814
   Abstract »    Full Text »    PDF »
Diverse Functions of Plant Peptides: Entering a New Phase.
H. Fukuda and T. Higashiyama (2011)
Plant Cell Physiol. 52, 1-4
   Full Text »    PDF »
Post-Translational Modifications in Secreted Peptide Hormones in Plants.
Y. Matsubayashi (2011)
Plant Cell Physiol. 52, 5-13
   Abstract »    Full Text »    PDF »
Analogs of the CLV3 Peptide: Synthesis and Structure-Activity Relationships Focused on Proline Residues.
T. Kondo, K. Yokomine, A. Nakagawa, and Y. Sakagami (2011)
Plant Cell Physiol. 52, 30-36
   Abstract »    Full Text »    PDF »
Mitogen-Activated Protein Kinase Regulated by the CLAVATA Receptors Contributes to Shoot Apical Meristem Homeostasis.
S. Betsuyaku, F. Takahashi, A. Kinoshita, H. Miwa, K. Shinozaki, H. Fukuda, and S. Sawa (2011)
Plant Cell Physiol. 52, 14-29
   Abstract »    Full Text »    PDF »
Comprehensive Analysis of CLE Polypeptide Signaling Gene Expression and Overexpression Activity in Arabidopsis.
J. Jun, E. Fiume, A. H. K. Roeder, L. Meng, V. K. Sharma, K. S. Osmont, C. Baker, C. M. Ha, E. M. Meyerowitz, L. J. Feldman, et al. (2010)
Plant Physiology 154, 1721-1736
   Abstract »    Full Text »    PDF »
RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis.
A. Kinoshita, S. Betsuyaku, Y. Osakabe, S. Mizuno, S. Nagawa, Y. Stahl, R. Simon, K. Yamaguchi-Shinozaki, H. Fukuda, and S. Sawa (2010)
Development 137, 3911-3920
   Abstract »    Full Text »    PDF »
The Roles of Different CLE Domains in Arabidopsis CLE Polypeptide Activity and Functional Specificity.
L. Meng, K. C. Ruth, J. C. Fletcher, and L. Feldman (2010)
Mol Plant 3, 760-772
   Abstract »    Full Text »    PDF »
CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically.
V. Mortier, G. Den Herder, R. Whitford, W. Van de Velde, S. Rombauts, K. D'haeseleer, M. Holsters, and S. Goormachtig (2010)
Plant Physiology 153, 222-237
   Abstract »    Full Text »    PDF »
How a Plant Builds Leaves.
S. A. Braybrook and C. Kuhlemeier (2010)
PLANT CELL 22, 1006-1018
   Abstract »    Full Text »    PDF »
Overproduction of the Membrane-bound Receptor-like Protein Kinase 1, RPK1, Enhances Abiotic Stress Tolerance in Arabidopsis.
Y. Osakabe, S. Mizuno, H. Tanaka, K. Maruyama, K. Osakabe, D. Todaka, Y. Fujita, M. Kobayashi, K. Shinozaki, and K. Yamaguchi-Shinozaki (2010)
J. Biol. Chem. 285, 9190-9201
   Abstract »    Full Text »    PDF »
The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division.
J. P. Etchells and S. R. Turner (2010)
Development 137, 767-774
   Abstract »    Full Text »    PDF »
Two Separate Pathways Including SlCLV1, SlSTM and SlCUC That Control Carpel Development in a Bisexual Mutant of Silene latifolia.
A. Koizumi, K. Yamanaka, K. Nishihara, Y. Kazama, T. Abe, and S. Kawano (2010)
Plant Cell Physiol. 51, 282-293
   Abstract »    Full Text »    PDF »
Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane.
A. Bleckmann, S. Weidtkamp-Peters, C. A.M. Seidel, and R. Simon (2010)
Plant Physiology 152, 166-176
   Abstract »    Full Text »    PDF »
Arabidopsis OPT6 is an Oligopeptide Transporter with Exceptionally Broad Substrate Specificity.
S. Pike, A. Patel, G. Stacey, and W. Gassmann (2009)
Plant Cell Physiol. 50, 1923-1932
   Abstract »    Full Text »    PDF »
Plant Cell Wall Proteomics: Mass Spectrometry Data, a Trove for Research on Protein Structure/Function Relationships.
C. Albenne, H. Canut, G. Boudart, Y. Zhang, H. San Clemente, R. Pont-Lezica, and E. Jamet (2009)
Mol Plant 2, 977-989
   Abstract »    Full Text »    PDF »
A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem.
B. Sun, Y. Xu, K.-H. Ng, and T. Ito (2009)
Genes & Dev. 23, 1791-1804
   Abstract »    Full Text »    PDF »
Epidermal Cell Density is Autoregulated via a Secretory Peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis Leaves.
K. Hara, T. Yokoo, R. Kajita, T. Onishi, S. Yahata, K. M. Peterson, K. U. Torii, and T. Kakimoto (2009)
Plant Cell Physiol. 50, 1019-1031
   Abstract »    Full Text »    PDF »
Involvement of Phytosulfokine in the Attenuation of Stress Response during the Transdifferentiation of Zinnia Mesophyll Cells into Tracheary Elements.
H. Motose, K. Iwamoto, S. Endo, T. Demura, Y. Sakagami, Y. Matsubayashi, K. L. Moore, and H. Fukuda (2009)
Plant Physiology 150, 437-447
   Abstract »    Full Text »    PDF »
Genetic and Epigenetic Regulation of Stem Cell Homeostasis in Plants.
M. Lodha, C.F. Marco, and M.C.P. Timmermans (2009)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Nod Factor/Nitrate-Induced CLE Genes that Drive HAR1-Mediated Systemic Regulation of Nodulation.
S. Okamoto, E. Ohnishi, S. Sato, H. Takahashi, M. Nakazono, S. Tabata, and M. Kawaguchi (2009)
Plant Cell Physiol. 50, 67-77
   Abstract »    Full Text »    PDF »
Intercellular Peptide Signals Regulate Plant Meristematic Cell Fate Decisions.
J. E. Gray, S. Casson, and L. Hunt (2008)
Science Signaling 1, pe53
   Abstract »    Full Text »    PDF »
Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells.
R. Whitford, A. Fernandez, R. De Groodt, E. Ortega, and P. Hilson (2008)
PNAS 105, 18625-18630
   Abstract »    Full Text »    PDF »
The Receptor-Like Kinase SOL2 Mediates CLE Signaling in Arabidopsis.
H. Miwa, S. Betsuyaku, K. Iwamoto, A. Kinoshita, H. Fukuda, and S. Sawa (2008)
Plant Cell Physiol. 49, 1752-1757
   Abstract »    Full Text »    PDF »
BAM Receptors Regulate Stem Cell Specification and Organ Development Through Complex Interactions With CLAVATA Signaling.
B. J. DeYoung and S. E. Clark (2008)
Genetics 180, 895-904
   Abstract »    Full Text »    PDF »
Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system.
Y. Hirakawa, H. Shinohara, Y. Kondo, A. Inoue, I. Nakanomyo, M. Ogawa, S. Sawa, K. Ohashi-Ito, Y. Matsubayashi, and H. Fukuda (2008)
PNAS 105, 15208-15213
   Abstract »    Full Text »    PDF »
Functional Diversification of CLAVATA3-Related CLE Proteins in Meristem Maintenance in Rice.
T. Suzaki, A. Yoshida, and H.-Y. Hirano (2008)
PLANT CELL 20, 2049-2058
   Abstract »    Full Text »    PDF »
The EPIP Peptide of INFLORESCENCE DEFICIENT IN ABSCISSION Is Sufficient to Induce Abscission in Arabidopsis through the Receptor-Like Kinases HAESA and HAESA-LIKE2.
G.-E. Stenvik, N. M. Tandstad, Y. Guo, C.-L. Shi, W. Kristiansen, A. Holmgren, S. E. Clark, R. B. Aalen, and M. A. Butenko (2008)
PLANT CELL 20, 1805-1817
   Abstract »    Full Text »    PDF »
Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense.
R. Shroff, F. Vergara, A. Muck, A. Svatos, and J. Gershenzon (2008)
PNAS 105, 6196-6201
   Abstract »    Full Text »    PDF »
The Receptor Kinase CORYNE of Arabidopsis Transmits the Stem Cell-Limiting Signal CLAVATA3 Independently of CLAVATA1.
R. Muller, A. Bleckmann, and R. Simon (2008)
PLANT CELL 20, 934-946
   Abstract »    Full Text »    PDF »
Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase.
G. Jia, X. Liu, H. A. Owen, and D. Zhao (2008)
PNAS 105, 2220-2225
   Abstract »    Full Text »    PDF »
Arabidopsis CLV3 Peptide Directly Binds CLV1 Ectodomain.
M. Ogawa, H. Shinohara, Y. Sakagami, and Y. Matsubayashi (2008)
Science 319, 294
   Abstract »    Full Text »    PDF »
Requirement of B2-Type Cyclin-Dependent Kinases for Meristem Integrity in Arabidopsis thaliana.
S. U. Andersen, S. Buechel, Z. Zhao, K. Ljung, O. Novak, W. Busch, C. Schuster, and J. U. Lohmann (2008)
PLANT CELL 20, 88-100
   Abstract »    Full Text »    PDF »
Gain-of-Function Phenotypes of Chemically Synthetic CLAVATA3/ESR-Related (CLE) Peptides in Arabidopsis thaliana and Oryza sativa.
A. Kinoshita, Y. Nakamura, E. Sasaki, J. Kyozuka, H. Fukuda, and S. Sawa (2007)
Plant Cell Physiol. 48, 1821-1825
   Abstract »    Full Text »    PDF »
The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole.
E. J. Sohn, M. Rojas-Pierce, S. Pan, C. Carter, A. Serrano-Mislata, F. Madueno, E. Rojo, M. Surpin, and N. V. Raikhel (2007)
PNAS 104, 18801-18806
   Abstract »    Full Text »    PDF »
A sub-proteome of Arabidopsis thaliana mature stems trapped on Concanavalin A is enriched in cell wall glycoside hydrolases.
Z. Minic, E. Jamet, L. Negroni, P Arsene der Garabedian, M. Zivy, and L. Jouanin (2007)
J. Exp. Bot. 58, 2503-2512
   Abstract »    Full Text »    PDF »
Ubiquitin Lysine 63 Chain Forming Ligases Regulate Apical Dominance in Arabidopsis.
X.-J. Yin, S. Volk, K. Ljung, N. Mehlmer, K. Dolezal, F. Ditengou, S. Hanano, S. J. Davis, E. Schmelzer, G. Sandberg, et al. (2007)
PLANT CELL 19, 1898-1911
   Abstract »    Full Text »    PDF »
Conservation and Diversification of Meristem Maintenance Mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 Gene.
T. Suzaki, T. Toriba, M. Fujimoto, N. Tsutsumi, H. Kitano, and H.-Y. Hirano (2006)
Plant Cell Physiol. 47, 1591-1602
   Abstract »    Full Text »    PDF »
The Arabidopsis Unannotated Secreted Peptide Database, a Resource for Plant Peptidomics.
K. A. Lease and J. C. Walker (2006)
Plant Physiology 142, 831-838
   Abstract »    Full Text »    PDF »
BOTANY: Plant Cells CLEave Their Way to Differentiation.
R. Simon and Y. Stahl (2006)
Science 313, 773-774
   Abstract »    Full Text »    PDF »
Dodeca-CLE peptides as suppressors of plant stem cell differentiation..
Y. Ito, I. Nakanomyo, H. Motose, K. Iwamoto, S. Sawa, N. Dohmae, and H. Fukuda (2006)
Science 313, 842-845
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882