AGAMOUS terminates floral stem cell maintenance in arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins

Plant Cell

Volumn 23, Issue 10, 2011, Pages 3654-3670

  Liu, Xigang ^a   Kim, Yun Ju ^a   Müller, Ralf ^b   Yumul, Rae Eden ^a   Liu, Chunyan ^c   Pan, Yanyun ^d   Cao, Xiaofeng ^c   Goodrich, Justin ^b   Chen, Xuemei ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d AGRICULTURAL UNIVERSITY OF HEBEI   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 82755174071     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.091538     Document Type: Article

References (67)

1. Alvarez, J., and Smyth, D.R. (1999). CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126: 2377-2386.
2. Bäurle, I., and Laux, T. (2005). Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17: 2271-2280.
3. Bowman, J.L., Sakai, H., Jack, T., Weigel, D., Mayer, U., and Meyerowitz, E.M. (1992). SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114: 599-615.
4. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
5. Boyer, L.A., et al. (2006). Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
6. Cai, S., and Lashbrook, C.C. (2006). Laser capture microdissection of plant cells from tape-transferred paraffin sections promotes recovery of structurally intact RNA for global gene profiling. Plant J. 48: 628-637.
7. Carles, C.C., Choffnes-Inada, D., Reville, K., Lertpiriyapong, K., and Fletcher, J.C. (2005). ULTRAPETALA1 encodes a SAND domain putative transcriptional regulator that controls shoot and floral meristem activity in Arabidopsis. Development 132: 897-911.
8. Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y.H., Sung, Z.R., and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263-5276.
9. Chen, X., Liu, J., Cheng, Y., and Jia, D. (2002). HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129: 1085-1094.
10. Chuck, G., Lincoln, C., and Hake, S. (1996). KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8: 1277-1289.
11. Clark, S.E., Jacobsen, S.E., Levin, J.Z., and Meyerowitz, E.M. (1996). The CLAVATA and SHOOT MERISTEMLESS loci competitively egulate meristem activity in Arabidopsis. Development 122: 1567-1575.
12. Das, P., Ito, T., Wellmer, F., Vernoux, T., Dedieu, A., Traas, J., and Meyerowitz, E.M. (2009). Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development 136: 1605-1611.
13. Drews, G.N., Bowman, J.L., and Meyerowitz, E.M. (1991). Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65: 991-1002.
14. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
15. Gómez-Mena, C., de Folter, S., Costa, M.M., Angenent, G.C., and Sablowski, R. (2005). Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132: 429-438.
16. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M., and Coupland, G. (1997). A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44-51.
17. Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A., and Gagliano, W.B. (1998). Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280: 446-450.
18. Hennig, L., and Derkacheva, M. (2009). Diversity of Polycomb group complexes in plants: Same rules, different players? Trends Genet. 25: 414-423.
19. Heo, J.B., and Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79.
20. Hsieh, T.F., Shin, J., Uzawa, R., Silva, P., Cohen, S., Bauer, M.J., Hashimoto, M., Kirkbride, R.C., Harada, J.J., Zilberman, D., and Fischer, R.L. (2011). Regulation of imprinted gene expression in Arabidopsis endosperm. Proc. Natl. Acad. Sci. USA 108: 1755-1762.
21. Huang, H., Mizukami, Y., Hu, Y., and Ma, H. (1993). Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucleic Acids Res. 21: 4769-4776.
22. Ito, T., Wellmer, F., Yu, H., Das, P., Ito, N., Alves-Ferreira, M., Riechmann, J.L., and Meyerowitz, E.M. (2004). The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430: 356-360.
23. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
24. Ji, L., et al. (2011). ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet. 7: e1001358.
25. Jürgens, G. (1985). A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316: 153-155.
26. Kanhere, A., et al. (2010). Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol. Cell 38: 675-688.
27. Khalil, A.M., et al. (2009). Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 106: 11667-11672.
28. Köhler, C., and Villar, C.B. (2008). Programming of gene expression by Polycomb group proteins. Trends Cell Biol. 18: 236-243.
29. Kotake, T., Takada, S., Nakahigashi, K., Ohto, M., and Goto, K. (2003). Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44: 555-564.
30. Larsson, A.S., Landberg, K., and Meeks-Wagner, D.R. (1998). The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana. Genetics 149: 597-605.
31. Laux, T., Mayer, K.F., Berger, J., and Jürgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87-96.
32. Lenhard, M., Bohnert, A., Jürgens, G., and Laux, T. (2001). Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805-814.
33. Lewis, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
34. Liu, C., Xi, W., Shen, L., Tan, C., and Yu, H. (2009). Regulation of floral patterning by flowering time genes. Dev. Cell 16: 711-722.
35. Lohmann, J.U., Hong, R.L., Hobe, M., Busch, M.A., Parcy, F., Simon, R., and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105: 793-803.
36. Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66-69.
37. Maier, A.T., Stehling-Sun, S., Wollmann, H., Demar, M., Hong, R.L., Haubeiss, S., Weigel, D., and Lohmann, J.U. (2009). Dual roles of the bZIP transcription factor PERIANTHIA in the control of floral architecture and homeotic gene expression. Development 136: 1613-1620.
38. Masui, S., Nakatake, Y., Toyooka, Y., Shimosato, D., Yagi, R., Takahashi, K., Okochi, H., Okuda, A., Matoba, R., Sharov, A.A., Ko, M.S., and Niwa, H. (2007). Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat. Cell Biol. 9: 625-635.
39. 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.
40. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. (2003). The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642.
41. Müller, J., and Verrijzer, P. (2009). Biochemical mechanisms of gene regulation by polycomb group protein complexes. Curr. Opin. Genet. Dev. 19: 150-158.
42. Mylne, J.S., Barrett, L., Tessadori, F., Mesnage, S., Johnson, L., Bernatavichute, Y.V., Jacobsen, S.E., Fransz, P., and Dean, C. (2006). LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA 103: 5012-5017.
43. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H., and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct 4. Cell 95: 379-391.
44. Pasini, D., Bracken, A.P., Hansen, J.B., Capillo, M., and Helin, K. (2007). The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27: 3769-3779.
45. Payne, T., Johnson, S.D., and Koltunow, A.M. (2004). KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development 131: 3737-3749.
46. Pien, S., and Grossniklaus, U. (2007). Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta 1769: 375-382.
47. Prunet, N., Morel, P., Thierry, A.M., Eshed, Y., Bowman, J.L., Negrutiu, I., and Trehin, C. (2008). REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell 20: 901-919.
48. Riechmann, J.L., Wang, M., and Meyerowitz, E.M. (1996). DNAbinding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24: 3134-3141.
49. Rinn, J.L., Kertesz, M., Wang, J.K., Squazzo, S.L., Xu, X., Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E., and Chang, H.Y. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
50. Rodrigues-Pousada, R.A., De Rycke, R., Dedonder, A., Van Caeneghem, W., Engler, G., Van Montagu, M., and Van Der Straeten, D. (1993). The Arabidopsis 1-Aminocyclopropane-1-Carboxylate Synthase Gene 1 is expressed during early development. Plant Cell 5: 897-911.
51. Schatlowski, N., Creasey, K., Goodrich, J., and Schubert, D. (2008). Keeping plants in shape: Polycomb-group genes and histone methylation. Semin. Cell Dev. Biol. 19: 547-553.
52. Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T., and Goodrich, J. (2006). Silencing by plant Polycombgroup genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 25: 4638-4649.
53. Schultz, E.A., Pickett, F.B., and Haughn, G.W. (1991). The FLO10 gene product regulates the expression domain of homeotic genes AP3 and PI in Arabidopsis flowers. Plant Cell 3: 1221-1237.
54. Shen, X., Liu, Y., Hsu, Y.J., Fujiwara, Y., Kim, J., Mao, X., Yuan, G.C., and Orkin, S.H. (2008). EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32: 491-502.
55. Shiraishi, H., Okada, K., and Shimura, Y. (1993). Nucleotide sequences recognized by the AGAMOUS MADS domain of Arabidopsis thaliana in vitro. Plant J. 4: 385-398.
56. Smyth, D.R., Bowman, J.L., and Meyerowitz, E.M. (1990). Early flower development in Arabidopsis. Plant Cell 2: 755-767.
57. Sun, B., Xu, Y., Ng, K.H., and Ito, T. (2009). A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev. 23: 1791-1804.
58. Sung, S., He, Y., Eshoo, T.W., Tamada, Y., Johnson, L., Nakahigashi, K., Goto, K., Jacobsen, S.E., and Amasino, R.M. (2006). Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38: 706-710.
59. Tsai, M.C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J.K., Lan, F., Shi, Y., Segal, E., and Chang, H.Y. (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689-693.
60. Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M.L., Guillaume, E., Buisine, N., Gagnot, S., Martienssen, R.A., Coupland, G., and Colot, V. (2007). Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3: e86.
61. Xu, L., and Shen, W.H. (2008). Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr. Biol. 18: 1966-1971.
62. Yap, K.L., Li, S., Muñoz-Cabello, A.M., Raguz, S., Zeng, L., Mujtaba, S., Gil, J., Walsh, M.J., and Zhou, M.M. (2010). Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38: 662-674.
63. Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y.V., Pellegrini, M., Goodrich, J., and Jacobsen, S.E. (2007b). Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5: e129.
64. Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V., and Jacobsen, S.E. (2007a). The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14: 869-871.
65. Zhao, J., Sun, B.K., Erwin, J.A., Song, J.J., and Lee, J.T. (2008). Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756.
66. Zheng, B., and Chen, X. (2011). Dynamics of histone H3 lysine 27 trimethylation in plant development. Curr. Opin. Plant Biol. 14: 123-129.
67. Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J.Y., and Chen, X. (2009). Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 23: 2850-2860.