Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: Dissection of the CLV3 signaling pathway from a direct ligand-binding point of view

Plant Journal

Volumn 82, Issue 2, 2015, Pages 328-336

  Shinohara, Hidefumi ^a   Matsubayashi, Yoshikatsu ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Arabidopsis thaliana; arabinosylation; BAM1; CLAVATA; CLV1; CLV3; ligand receptor interaction; peptide hormone; receptor kinase; shoot apical meristem

Indexed keywords

CELL PROLIFERATION; CELL SIGNALING; COMPLEX NETWORKS; CYTOLOGY; ENZYMES; LIGANDS; PEPTIDES; STEM CELLS; TRANSCRIPTION;

ARABIDOPSIS THALIANA; ARABINOSYLATION; BAM1; CLAVATA; CLV1; CLV3; LIGAND-RECEPTOR INTERACTIONS; PEPTIDE HORMONES; RECEPTOR KINASE; SHOOT APICAL MERISTEMS;

PLANTS (BOTANY);

ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; PROTEIN BINDING;

ARABIDOPSIS; GENE EXPRESSION REGULATION; MERISTEM; METABOLISM; SHOOT; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MERISTEM; PLANT SHOOTS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84926453566     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12817     Document Type: Article

References (30)

1. Brand, U., Fletcher, J., Hobe, M., Meyerowitz, E., and, Simon, R., (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science, 289, 617-619.
2. Clark, S., Running, M., and, Meyerowitz, E., (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development, 119, 397-418.
3. Clough, S., and, Bent, A., (1999) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
4. Depuydt, S., Rodriguez-Villalon, A., Santuari, L., Wyser-Rmili, C., Ragni, L., and, Hardtke, C. S., (2013) Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc. Natl Acad. Sci. USA, 110, 7074-7079.
5. Deyoung, B., and, Clark, S., (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics, 180, 895-904.
6. DeYoung, B., Bickle, K., Schrage, K., Muskett, P., Patel, K., and, Clark, S., (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16.
7. Diévart, A., Dalal, M., Tax, F., Lacey, A., Huttly, A., Li, J., and, Clark, S., (2003) CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell, 15, 1198-1211.
8. Durbak, A., and, Tax, F., (2012) CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics, 189, 177-194.
9. Fletcher, J., Brand, U., Running, M., Simon, R., and, Meyerowitz, E., (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science, 283, 1911-1914.
10. Guo, Y., Han, L., Hymes, M., Denver, R., and, Clark, S., (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889-900.
11. Hord, C., Chen, C., Deyoung, B., Clark, S., and, Ma, H., (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell, 18, 1667-1680.
12. Kayes, J., and, Clark, S., (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development, 125, 3843-3851.
13. Kinoshita, A., Betsuyaku, S., Osakabe, Y., Mizuno, S., Nagawa, S., Stahl, Y., Simon, R., Yamaguchi-Shinozaki, K., Fukuda, H., and, Sawa, S., (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development, 137, 3911-3920.
14. Kondo, T., Sawa, S., Kinoshita, A., Mizuno, S., Kakimoto, T., Fukuda, H., and, Sakagami, Y., (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science, 313, 845-848.
15. Kosugi, S., Arai, Y., Nakajima, K., and, Ohashi, Y., (1990) An improved assay for ß-glucuronidase (GUS) in transformed cells: methanol almost suppresses a putative endogenous GUS activity. Plant Sci. 70, 133-140.
16. Lenhard, M., Jurgens, G., and, Laux, T., (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development, 129, 3195-3206.
17. Lisso, J., Steinhauser, D., Altmann, T., Kopka, J., and, Mussig, C., (2005) Identification of brassinosteroid-related genes by means of transcript co-response analyses. Nucleic Acids Res. 33, 2685-2696.
18. Mayer, K., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G., and, Laux, T., (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell, 95, 805-815.
19. Müller, R., Bleckmann, A., and, Simon, R., (2008) The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell, 20, 934-946.
20. Nimchuk, Z., Tarr, P., and, Meyerowitz, E., (2011) An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell, 23, 851-854.
21. Ogawa, M., Shinohara, H., Sakagami, Y., and, Matsubayashi, Y., (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science, 319, 294.
22. Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M., and, Matsubayashi, Y., (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5, 578-580.
23. Okamoto, S., Shinohara, H., Mori, T., Matsubayashi, Y., and, Kawaguchi, M., (2013) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4, 2191.
24. Schoof, H., Lenhard, M., Haecker, A., Mayer, K., Jürgens, G., and, Laux, T., (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell, 100, 635-644.
25. Shinohara, H., and, Matsubayashi, Y., (2013) Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant Cell Physiol. 54, 369-374.
26. Shinohara, H., Moriyama, Y., Ohyama, K., and, Matsubayashi, Y., (2012) Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J. 70, 845-854.
27. Song, X., Yu, D., Xu, T., Ren, S., Guo, P., and, Liu, C., (2012) Contributions of individual amino acid residues to the endogenous CLV3 function in shoot apical meristem maintenance in Arabidopsis. Mol. Plant. 5, 515-523.
28. Yadav, R. K., Girke, T., Pasala, S., Xie, M., and, Reddy, G. V., (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl Acad. Sci. USA, 106, 4941-4946.
29. Yadav, R. K., Tavakkoli, M., Xie, M., Girke, T., and, Reddy, G. V., (2014) A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche. Development, 141, 2735-2744.
30. Zhu, Y., Wang, Y., Li, R., Song, X., Wang, Q., Huang, S., Jin, J., Liu, C., and, Lin, J., (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J. 61, 223-233.