Abstract
Stem cells in the shoot apical meristem (SAM) of plants are the self-renewable reservoir for leaf, stem and flower organogenesis1,2. In nature, disease-free plants can be regenerated from SAM despite infections elsewhere, which underlies a horticultural practice for decades3. However, the molecular basis of the SAM immunity remains unclear. Here we show that the CLAVATA3 peptide (CLV3p), expressed and secreted from stem cells and functioning as a key regulator of stem-cell homeostasis in the SAM of Arabidopsis1,2,4, can trigger immune signalling and pathogen resistance via the flagellin receptor kinase FLS2 (refs 5, 6). CLV3p–FLS2 signalling acts independently from the stem-cell signalling pathway mediated through CLV1 and CLV2 receptors1,2,4, and is uncoupled from FLS2-mediated growth suppression5,6. Endogenous CLV3p perception in the SAM by a pattern recognition receptor for bacterial flagellin, FLS2, breaks the previously defined self and non-self discrimination in innate immunity6,7. The dual perception of CLV3p illustrates co-evolution of plant peptide and receptor kinase signalling for both development and immunity. The enhanced immunity in SAM or germ lines may represent a common strategy towards immortal fate in plants and animals1,2,8.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bäurle, I. & Laux, T. Apical meristems: the plant’s fountain of youth. Bioessays 25, 961–970 (2003)
Scheres, B. Stem cells: a plant biology perspective. Cell 122, 499–504 (2005)
Hollings, M. Disease control through virus-free stock. Annu. Rev. Phytopathol. 3, 367–396 (1965)
Jun, J. H., Fiume, E. & Fletcher, J. C. The CLE family of plant polypeptide signaling molecules. Cell. Mol. Life Sci. 65, 743–755 (2008)
Gomez-Gomez, L. & Boller, T. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis . Mol. Cell 5, 1003–1011 (2000)
Boller, T. & Felix, G. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406 (2009)
Ishii, K. J., Koyama, S., Nakagawa, A., Coban, C. & Akira, S. Host innate immune receptors and beyond: Making sense of microbial infections. Cell Host Microbe 3, 352–363 (2008)
Curran, S. P., Wu, X., Riedel, C. G. & Ruvkun, G. A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459, 1079–1084 (2009)
Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983 (2002)
Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767 (2004)
Yamamizo, C. et al. Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol. 140, 681–692 (2006)
Yadav, R. K., Girke, T., Pasala, S., Xie, M. & Reddy, G. V. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl Acad. Sci. USA 106, 4941–4946 (2009)
Kondo, T. et al. A plant peptide encoded by CLV3 identified by in situ MALDI-TPF MS analysis. Science 313, 845–848 (2006)
Shan, L. et al. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17–27 (2008)
Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007)
Heese, A. et al. The receptor-like kinase SEERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007)
Butenko, M. A., Vie, A. K., Brembu, T., Aalen, R. B. & Bones, A. M. Plant peptides in signaling: looking for new partners. Trends Plant Sci. 14, 255–263 (2009)
Miwa, H. et al. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis . Plant Cell Physiol. 49, 1752–1757 (2008)
Müller, R., Bleckmann, A. & Simon, R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934–946 (2008)
Zipfel, C. et al. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760 (2006)
Fiers, M. et al. The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141, 1284–1292 (2006)
Felix, G., Duran, J. D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276 (1999)
Bäurle, I. & Laux, T. Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17, 2271–2280 (2005)
Chinchilla, D., Bauer, Z., Regenass, M., Boller, T. & Felix, G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18, 465–476 (2006)
Gómez-Gómez, L., Bauer, Z. & Boller, T. Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signaling in Arabidopsis . Plant Cell 13, 1155–1163 (2001)
Dunning, F. M., Sun, W., Jansen, K. L., Helft, L. & Bent, A. F. Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell 19, 3297–3313 (2007)
Bauer, Z., Gomez-Gomez, L., Boller, T. & Felix, G. Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J. Biol. Chem. 276, 45669–45676 (2001)
Guo, Y., Han, L., Hymes, M., Denver, R. & Clark, S. E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889–900 (2010)
Goldsby, R. A., Kindt, T. J. & Osborne, B. A. Kuby Immunology (W. H. Freeman, New York, 2006)
Clark, R. M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana . Science 317, 338–342 (2007)
Koornneef, M. et al. Linkage map of Arabidopsis thaliana . J. Hered. 74, 265–272 (1983)
Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057–2067 (1995)
Diévart, A. et al. CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15, 1198–1211 (2003)
Jeong, S., Trotochaud, A. E. & Clark, S. E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11, 1925–1933 (1999)
Fletcher, J. C., Brand, U., Running, M. P., Simon, R. & Meyerowitz, E. M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911–1914 (1999)
Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565–1572 (2007)
Schreiber, K., Ckurshumova, W., Peek, J. & Desveaux, D. A high-throughput chemical screen for resistance to Pseudomonas syringae in Arabidopsis . Plant J. 54, 522–531 (2008)
Boudsocq, M. et al. Differential innate immune signaling via Ca2+ sensor protein kinases. Nature 464, 418–422 (2010)
Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294 (2008)
Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M. & Matsubayashi, Y. A glycopeptide regulating stem cell fate in Arabidopsis thaliana . Nature Chem. Biol. 5, 578–580 (2009)
Acknowledgements
We thank T. Laux for the pWUS::GUS line, Y. Matsubayashi for the purified Ara-CLV3 peptide and advice, A. Collmer for the GFP-labelled P. syringae pv. tomato DC3000, L. Shan and P. He for constructs, G. Tena, F. Ausubel, J. Bush, J. Plotnikova and ABRC for mutant seeds and bacterial strains, and Y. Xiong, M. McCormack, Y. Niu, M. Ramon and J. Li for critically reading of the manuscript. Funding was provided by the NSF, NIH and the MGH CCIB fund to J.S.
Author information
Authors and Affiliations
Contributions
H.L. and J.S. initiated the project and designed the experiments; H.L. carried out the experiments and prepared the data with assistance from O.-K.C.; H.L and J.S. wrote the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-15 with legends, Supplementary Tables 1-2 and additional references. (PDF 1045 kb)
Rights and permissions
About this article
Cite this article
Lee, H., Chah, OK. & Sheen, J. Stem-cell-triggered immunity through CLV3p–FLS2 signalling. Nature 473, 376–379 (2011). https://doi.org/10.1038/nature09958
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature09958
This article is cited by
-
Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem
Plant Cell Reports (2019)
-
Holaphyllamine, a steroid, is able to induce defense responses in Arabidopsis thaliana and increases resistance against bacterial infection
Planta (2017)
-
Q&A: How does peptide signaling direct plant development?
BMC Biology (2016)
-
Molecular signaling networks in the shoot apical meristem
Journal of Plant Biology (2014)
-
A wound-induced small polypeptide gene family is upregulated in soybean nodules
Chinese Science Bulletin (2013)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.