TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis

Plant Cell

Volumn 22, Issue 8, 2010, Pages 2618-2629

  Hirakawa, Yuki ^a   Kondo, Yuki ^a   Fukuda, Hiroo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77957799899     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.076083     Document Type: Article

References (54)

1. Baima, S., Nobili, F., Sessa, G., Lucchetti, S., Ruberti, I., and Morelli, G. (1995). The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171-4182.
2. Björklund, S., Antti, H., Uddestrand, I., Moritz, T., and Sundberg, B. (2007). Cross-talk between gibberellin and auxin in development of Populus wood: Gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J. 52: 499-511.
3. 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.
4. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M., and Laux, T. (2008). Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14: 867-876.
5. Busse, J.S., and Evert, R.F. (1999). Vascular differentiation and transition in the seedling of Arabidopsis thaliana (Brassicaceae). Int. J. Plant Sci. 160: 241-251.
6. Chaffey, N., Cholewa, E., Regan, S., and Sundberg, B. (2002). Secondary xylem development in Arabidopsis: A model for wood formation. Physiol. Plant. 114: 594-600.
7. 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.
8. 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.
9. Cock, J.M., and McCormick, S. (2001). A large family of genes that share homology with CLAVATA3. Plant Physiol. 126: 939-942.
10. De Smet, I., Voss, U., Jürgens, G., and Beeckman, T. (2009). Receptor-like kinases shape the plant. Nat. Cell Biol. 11: 1166-1173.
11. Deveaux, Y., Toffano-Nioche, C., Claisse, G., Thareau, V., Morin, H., Laufs, P., Moreau, H., Kreis, M., and Lecharny, A. (2008). Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol. Biol. 8: 291.
12. Dinneny, J.R., and Benfey, P.N. (2008). Plant stem cell niches: standing the test of time. Cell 132: 553-557.
13. Dolan, L., and Roberts, K. (1995). Secondary thickening in roots of Arabidopsis thaliana: Anatomy and cell surface changes. New Phytol. 131: 121-128.
14. Elo, A., Immanen, J., Nieminen, K., and Helariutta, Y. (2009). Stem cell function during plant vascular development. Semin. Cell Dev. Biol. 20: 1097-1106.
15. rd ed. (Hoboken, NJ: John Wiley & Sons).
16. Fisher, K., and Turner, S. (2007). PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17: 1061-1066.
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. Fukuda, H. (2004). Signals that control plant vascular cell differentiation. Nat. Rev. Mol. Cell Biol. 5: 379-391.
19. Gendreau, E., Traas, J., Desnos, T., Grandjean, O., Caboche, M., and Höfte, H. (1997). Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114: 295-305.
20. Haecker, A., Gross-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H., Herrmann, M., and Laux, T. (2004). Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657-668.
21. Hirakawa, Y., Shinohara, H., Kondo, Y., Inoue, A., Nakanomyo, I., Ogawa, M., Sawa, S., Ohashi-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.
22. 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.
23. Ji, J., Strable, J., Shimizu, R., Koenig, D., Sinha, N., and Scanlon, M.J. (2010). WOX4 promotes procambial development. Plant Physiol. 152: 1346-1356.
24. Jun, J.H., Fiume, E., and Fletcher, J.C. (2008). The CLE family of plant polypeptide signaling molecules. Cell. Mol. Life Sci. 65: 743-755.
25. Love, J., Björklund, S., Vahala, J., Hertzberg, M., Kangasjärvi, J., and Sundberg, B. (2009). Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc. Natl. Acad. Sci. USA 106: 5984-5989.
26. Matsumoto, N., and Okada, K. (2001). A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 15: 3355-3364.
27. Matsumoto-Kitano, M., Kusumoto, T., Tarkowski, P., Kinoshita-Tsujimura, K., Václavíková, K., Miyawaki, K., and Kakimoto, T. (2008). Cytokinins are central regulators of cambial activity. Proc. Natl. Acad. Sci. USA 105: 20027-20031.
28. Mayer, K.F., 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.
29. Müller, R., Borghi, L., Kwiatkowska, D., Laufs, P., and Simon, R. (2006). Dynamic and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signaling. Plant Cell 18: 1188-1198.
30. Nardmann, J., Ji, J., Werr, W., and Scanlon, M.J. (2004). The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131: 2827-2839.
31. Nieminen, K., et al. (2008). Cytokinin signaling regulates cambial development in poplar. Proc. Natl. Acad. Sci. USA 105: 20032-20037.
32. Nilsson, J., Karlberg, A., Antti, H., Lopez-Vernaza, M., Mellerowicz, E., Perrot-Rechenmann, C., Sandberg, G., and Bhalerao, R.P. (2008). Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20: 843-855.
33. Ogawa, M., Shinohara, H., Sakagami, Y., and Matsubayashi, Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.
34. Ohashi-Ito, K., and Fukuda, H. (2003). HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol. 44: 1350-1358.
35. Ohyama, K., Ogawa, M., and Matsubayashi, Y. (2008). Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 55: 152-160.
36. Park, S.O., Zheng, Z., Oppenheimer, D.G., and Hauser, B.A. (2005). The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homeodomain protein that regulates ovule development. Development 132: 841-849.
37. Rebocho, A.B., Bliek, M., Kusters, E., Castel, R., Procissi, A., Roobeek, I., Souer, E., and Koes, R. (2008). Role of EVERGREEN in the development of the cymose petunia inflorescence. Dev. Cell 15: 437-447.
38. Reddy, G.V. (2008). Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr. Opin. Plant Biol. 11: 88-93.
39. Rosso, M.G., Li, Y., Strizhov, N., Reiss, B., Dekker, K., and Weisshaar, B. (2003). An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol. Biol. 53: 247-259.
40. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and Laux, T. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811-814.
41. Scheres, B. (2007). Stem-cell niches: nursery rhymes across kingdoms. Nat. Rev. Mol. Cell Biol. 8: 345-354.
42. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jürgens, G., and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635-644.
43. Schrader, J., Nilsson, J., Mellerowicz, E., Berglund, A., Nilsson, P., Hertzberg, M., and Sandberg, G. (2004). A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16: 2278-2292.
44. Shiu, S.H., and Bleecker, A.B. (2001). Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 98: 10763-10768.
45. Stahl, Y., and Simon, R. (2005). Plant stem cell niches. Int. J. Dev. Biol. 49: 479-489.
46. Stahl, Y., Wink, R.H., Ingram, G.C., and Simon, R. (2009). A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19: 909-914.
47. Till, B.J., et al. (2003). Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res. 13: 524-530.
48. Uggla, C., Moritz, T., Sandberg, G., and Sundberg, B. (1996). Auxin as a positional signal in pattern formation in plants. Proc. Natl. Acad. Sci. USA 93: 9282-9286.
49. Vandenbussche, M., Horstman, A., Zethof, J., Koes, R., Rijpkema, A. S., and Gerats, T. (2009). Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 21: 2269-2283.
50. 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.
51. Wolters, H., and Jürgens, G. (2009). Survival of the flexible: hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10: 305-317.
52. Wu, X., Chory, J., and Weigel, D. (2007). Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev. Biol. 309: 306-316.
53. Wu, X., Dabi, T., and Weigel, D. (2005). Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr. Biol. 15: 436-440.
54. Zhao, Y., Hu, Y., Dai, M., Huang, L., and Zhou, D.X. (2009). The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell 21: 736-748.