The roles of different CLE domains in arabidopsis CLE polypeptide activity and functional specificity

Molecular Plant

Volumn 3, Issue 4, 2010, Pages 760-772

  Meng, Ling ^a   Ruth, Kenneth C ^a   Fletcher, Jennifer C ^b   Feldman, Lewis ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PLANT GENE EXPRESSION CENTER   (United States)

Author keywords

Arabidopsis; cell signaling; CLE; meristem; polypeptide; protein domain

Indexed keywords

ARABIDOPSIS;

EID: 77955168108     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssq021     Document Type: Article

References (54)

1. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M., and Simon, R. (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 289, 617-619.
2. Carlsson, F., Stalhammar-Carlemalm, M., Flardh, K., Sandin, C., Carlemalm, E., and Lindahl, G. (2006). Signal sequence directs localized secretion of bacterial surface proteins. Nature. 442, 943-946.
3. Casamitjana-Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R., and Scheres, B. (2003). Root-specific CLE19 overex- pression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 3, 1435-1441.
4. Clark, S.E., Running, M.P., and Meyerowitz, E.M. (1993). CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development. 119, 397-418.
5. Clark, S.E., Running, M.P., and Meyerowitz, E.M. (1995). CLAVA- TA3is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development. 121, 2057-2067.
6. Clark, S.E., Williams, R.W., and Meyerowitz, E.M. (1997). The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell. 89, 575-585.
7. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. Clowes, F.A.L. (1956). Nucleic acids in root apical meristems of Zea. New Phytol. 55, 29-34.
9. Cock, J.M., and McCormick, S. (2001). A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939-942.
10. Denecke, J., Botterman, J., and Deblaere, R. (1990). Protein secretion in plant cells can occur via a default pathway. Plant Cell. 2, 51-59.
11. Diévart, A., Dalal, M., Tax, F.E., Lacey, A.D., Huttly, A., Li, J., and Diévart, A. (2003). CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell. 15, 1198-1211.
12. Eichler, R., Lenz, O., Strecker, T., Eickmann, M., Klenk, H.D., and Garten, M. (2003). Identification of Lassa virus glycoprotein signal peptide as a trans-acting maturation factor, EMBO Rep. 4, 1084-1088. (Pubitemid 37527428)
13. Fiers, M., Golemiec, E., Xu, J., van der Geest, L., Heidstra, R., Stiekema, W., and Liu, C.M. (2005). The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell. 17, 2542-2553.
14. Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R., van der Geest, L., van Lookeren Campagne, M., and Liu, C.M. (2004). Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene. 327, 37-49.
15. Fiers, M., Golemiec, E., van der Schors, R., van der Geest, L., Li, K.W., Stiekema, W.J., and Liu, C.M. (2006). The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141, 1284-1292.
16. Fletcher, J.C. (2002). Shoot and floral meristem maintenance in Arabidopsis. Annu. Rev. Plant Biol. 53, 45-66.
17. Fletcher, J.C., Brand, U., Running, M.P., Simon, R., and Meyerowitz, E.M. (1999). Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 283, 1911-1914.
18. Gleave, A.P. (1992). A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203-1207.
19. Hegde, R.S., and Bernstein, H.D. (2006). The surprising complexity of signal sequences. Trends Biochem. Sci. 31, 563-571.
20. Hobe, M., Müller, R., Grünewald, M., Brand, U., and Simon, R. (2003). Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213, 371-381.
21. Höfgen, R., and Willmitzer, L. (1988). Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res. 16, 9877.
22. Ito, K., Matsubayashi, Y., and Fukuda, H. (2008). Non-cell- autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl Acad. Sci. USA. 105, 15208-15213.
23. Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N., and Fukuda, H. (2006). Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science. 313, 842-845.
24. Jefferson, R.A., Kilian, A., and Keese, P.K. (1998). Microbial genes for secreted beta-glucuronidases, gene products and uses thereof. Patent: PCT (PCT/US98/19217) CAMBIA. Molecular Technologies, Canberra, Australia.
25. Jeong, S., Trotochaud, A.E., and Clark, S.E. (1999). The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required forthe stability of the CLAVATA1 receptor-like kinase. Plant Cell. 11, 1925-1934.
26. Kaiser, C.A., Preuss, D., Grisafi, P., and Botstein, D. (1987). Many random sequences functionally replace the secretion signal sequence of yeast invertase. Science. 235, 312-317.
27. Kang, S.W., Rane, N.S., Kim, S.J., Garrison, J.L., Taunton, J., and Hegde, R.S. (2006). Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell. 127, 999-1013.
28. Kayes, J.M., and Clark, S.E. (1998). CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development. 125, 3843-3851.
29. 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.
30. Laux, T., Mayer, K.F., Berger, J., and Jurgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 122, 87-96.
31. Lei, M., and Wu, R. (1991). A novel glycine-rich cell wall protein gene in rice. Plant Mol. Biol. 16, 187-198.
32. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25, 402-408.
33. Mayer, K.F., Schoof, H., Haecker, A., Lenhard, M., Jurgens, G., and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 95, 805-815.
34. Miwa, H., Betsuyaku, S., Iwamoto, K., Kinoshita, A., Fukuda, H., and Sawa, S. (2008). The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49, 1752-1757.
35. 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.
36. Ni, J., and Clark, S.E. (2006). Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 140, 726-733.
37. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites,. Protein Engineering. 10, 1-6.
38. Nielsen, H., and Krogh, A. (1998). Prediction of signal peptides and signal anchors by a hidden Markov model. Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (ISMB 6), AAAI Press, Menlo Park, California, 122130.
39. Oelkers, K., Goffard, N., Weiller, G.F., Gresshoff, P.M., Mathesius, U., and Frickey, T. (2008). Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8, 1.
40. Ogawa, M., Shinohara, H., Sakagami, Y., and Matsubayashi, Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodo- main. Science. 319, 294.
41. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., and Fletcher, J.C. (2002). CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell. 14, 969-977.
42. Ruzin, S.E. (1999). Plant Microtechnique and Microscopy (New York: Oxford University Press), pp. 161-171.
43. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jurgens, 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.
44. Sharma, V.K., Ramirez, J., and Fletcher, J.C. (2003). The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Mol Biol. 51, 415-425.
45. Sharman, B.C. (1943). Tannic acid and iron alum with safranin and orange G in studies of the shoot apex. Stain. Technol. 18, 105-111.
46. Strabala, T.J., O'Donnell, P.J., Smit, A.M., Ampomah-Dwamena, C., Martin, E.J., Netzler, N., Nieuwenhuizen, N.J., Quinn, B.D., Foote, H.C., and Hudson, K.R. (2006). Gain-of-function pheno-types of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol. 140, 1331-1344.
47. Talmadge, K., Stahl, S., and Gilbert, W. (1980). Eukaryotic signal sequence transports insulin antigen in Escherichia coli. Proc. Natl Acad. Sci. USA. 77, 3369-3373.
48. Trotochaud, A., Hao, T., Wu, G., Yang, Z., and Clark, S.E. (1999). The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho- related protein. Plant Cell. 11, 393-406.
49. van den Berg, C., Willemsen, V., Hage, W., Weisbeek, P., and Scheres, B. (1995). Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature. 378, 62-65.
50. van den Berg, C., Willemsen, V., Hendricks, G., Weisbeek, P., and Scheres, B. (1997). Short-range control of cell differentiation in the Arabidopsis root meristem. Nature. 390, 287-289.
51. von Heijne, G. (1985). Signal sequences: the limits of variation. J. Mol. Biol. 184, 99-105.
52. Walter, P., Gilmore, R., and Blobel, G. (1984). Protein translocation across the endoplasmic reticulum. Cell. 38, 5-8.
53. Wang, X., Mitchum, M.G., Gao, B., Li, C., Diab, H., Baum, T.J., Hussey, R.S., and Davis, E.L. (2005). A parasitism gene from a plant-parasitic nematode with function similar to CLAV- ATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 6, 187-191.
54. Whitford, R., Fernandez, A., De Groodt, R., Ortega, E., and Hilson, P. (2008). Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl Acad. Sci. USA. 105, 18625-18630.