The polycomb group gene EMF2B is essential for maintenance of floral meristem determinacy in rice

Plant Journal

Volumn 80, Issue 5, 2014, Pages 883-894

  Conrad, Liza J ^a,e   Khanday, Imtiyaz ^b   Johnson, Cameron ^a   Guiderdoni, Emmanuel ^c   An, Gynheung ^d   Vijayraghavan, Usha ^b   Sundaresan, Venkatesan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c UMR AGAP   (France)

^d Kyung Hee University   (South Korea)

^e ECKERD COLLEGE   (United States)

Author keywords

EMF2B; floral meristem; MADS box; Oryza sativa; polycomb

Indexed keywords

AMINO ACIDS; GENES;

EMF2B; FLORAL MERISTEMS; MADS-BOX; ORYZA SATIVA; POLYCOMB;

GENES; GENE EXPRESSION;

ARABIDOPSIS; ORYZA SATIVA;

HISTONE; MADS DOMAIN PROTEIN; POLYCOMB GROUP PROTEIN; VEGETABLE PROTEIN;

CHROMATIN IMMUNOPRECIPITATION; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; METHYLATION; MUTATION; ORYZA; PHYSIOLOGY;

CHROMATIN IMMUNOPRECIPITATION; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HISTONES; MADS DOMAIN PROTEINS; MERISTEM; METHYLATION; MUTATION; ORYZA; PLANT PROTEINS; POLYCOMB-GROUP PROTEINS;

EID: 84922258300     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12688     Document Type: Article

References (65)

1. Agrawal, G.K., Abe, K., Yamazaki, M., Miyao, A., and, Hirochika, H., (2005) Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol. Biol. 59, 125-135.
2. Bemer, M., and, Grossniklaus, U., (2012) Dynamic regulation of Polycomb group activity during plant development. Curr. Opin. Plant Biol. 15, 523-529.
3. Bouyer, D., Roudier, F., Heese, M., et al. (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet. 7, e1002014.
4. Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., and, Paszkowski, J., (2004) Chromatin techniques for plant cells. Plant J. 39, 776-789.
5. Bowman, J.L., Drews, G.N., and, Meyerowitz, E.M., (1991) Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell, 3, 749-758.
6. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S., and, Zhang, Y., (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science, 298, 1039-1043.
7. 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.
8. Chen, Z.X., Wu, J.G., Ding, W.N., Chen, H.M., Wu, P., and, Shi, C.H., (2006) Morphogenesis and molecular basis on naked seed rice, a novel homeotic mutation of OsMADS1 regulating transcript level of AP3 homologue in rice. Planta, 223, 882-890.
9. Chen, L.J., Diao, Z.Y., Specht, C., and, Sung, Z.R., (2009) Molecular evolution of VEF-domain-containing PcG genes in plants. Mol. Plant, 2, 738-754.
10. Cui, R., Han, J., Zhao, S., Su, K., Wu, F., Du, X., Xu, Q., Chong, K., Theissen, G., and, Meng, Z., (2010) Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant J. 61, 767-781.
11. Czermin, B., Melfi, R., McCabe, D., Seitz, V., Imhof, A., and, Pirrotta, V., (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell, 111, 185-196.
12. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S., and, Yanofsky, M.F., (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14, 1935-1940.
13. Dreni, L., Pilatone, A., Yun, D., Erreni, S., Pajoro, A., Caporali, E., Zhang, D., and, Kater, M.M., (2011) Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy. Plant Cell, 23, 2850-2863.
14. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and, Su, Z., (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70.
15. Duncan, I.M., (1982) Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene compleses of Drosophila melanogaster. Genetics, 102, 49-70.
16. Francis, N.J., and, Kingston, R.E., (2001) Mechanisms of transcriptional memory. Nat. Rev. Mol. Cell Biol. 2, 409-421.
17. Gao, X., Liang, W., Yin, C., Ji, S., Wang, H., Su, X., Guo, C., Kong, H., Xue, H., and, Zhang, D., (2010) The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development. Plant Physiol. 153, 728-740.
18. 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.
19. Guitton, A.E., and, Berger, F., (2005) Control of reproduction by Polycomb Group complexes in animals and plants. Int. J. Dev. Biol. 49, 707-716.
20. He, G., Zhu, X., Elling, A.A., et al. (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 22, 17-33.
21. Irish, V.F., (2010) The flowering of Arabidopsis flower development. Plant J. 61, 1014-1028.
22. Itoh, J., Nonomura, K., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H., and, Nagato, Y., (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46, 23-47.
23. Jeon, J.S., Jang, S., Lee, S., et al,. (2000) leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell, 12, 871-884.
24. Jeong, D.H., An, S., Kang, H.G., Moon, S., Han, J.J., Park, S., Lee, H.S., An, K., and, An, G., (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol. 130, 1636-1644.
25. Jurgens, G., (1985) A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 316, 153-155.
26. Kater, M.M., Dreni, L., and, Colombo, L., (2006) Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis. J. Exp. Bot. 57, 3433-3444.
27. Ketel, C.S., Andersen, E.F., Vargas, M.L., Suh, J., Strome, S., and, Simon, J.A., (2005) Subunit contributions to histone methyltransferase activities of fly and worm polycomb group complexes. Mol. Cell. Biol. 25, 6857-6868.
28. Khanday, I., Yadav, S.R., and, Vijayraghavan, U., (2013) Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol. 161, 1970-1983.
29. Kinoshita, T., Harada, J.J., Goldberg, R.B., and, Fischer, R.L., (2001) Polycomb repression of flowering during early plant development. Proc. Natl Acad. Sci. USA, 98, 14156-14161.
30. Kobayashi, K., Maekawa, M., Miyao, A., Hirochika, H., and, Kyozuka, J., (2010) PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant Cell Physiol. 51, 47-57.
31. Kobayashi, K., Yasuno, N., Sato, Y., Yoda, M., Yamazaki, R., Kimizu, M., Yoshida, H., Nagamura, Y., and, Kyozuka, J., (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell, 24, 1848-1859.
32. Kuzmichev, A., Nishioka, K., Erdjument-Bromage, H., Tempst, P., and, Reinberg, D., (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16, 2893-2905.
33. Lee, S., Choi, S.C., and, An, G., (2008) Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. Plant J. 54, 93-105.
34. Lewis, E.B., (1978) A gene complex controlling segmentation in Drosophila. Nature, 276, 565-570.
35. Li, H., Liang, W., Jia, R., Yin, C., Zong, J., Kong, H., and, Zhang, D., (2010) The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice. Cell Res. 20, 299-313.
36. Liu, X., Kim, Y.J., Muller, R., Yumul, R.E., Liu, C., Pan, Y., Cao, X., Goodrich, J., and, Chen, X., (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell, 23, 3654-3670.
37. Lopez-Vernaza, M., Yang, S., Muller, R., Thorpe, F., de Leau, E., and, Goodrich, J., (2012) Antagonistic roles of SEPALLATA3, FT and FLC genes as targets of the polycomb group gene CURLY LEAF. PLoS ONE, 7, e30715.
38. Luo, H., Li, Y., Yang, Z., Zhong, B., Xie, R., Ren, M., Luo, D., and, He, G., (2006) Fine mapping of a pistilloid-stamen (PS) gene on the short arm of chromosome 1 in rice. Genome, 49, 1016-1022.
39. Luo, M., Platten, D., Chaudhury, A., Peacock, W.J., and, Dennis, E.S., (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol. Plant, 2, 711-723.
40. Makarevitch, I., Eichten, S.R., Briskine, R., Waters, A.J., Danilevskaya, O.N., Meeley, R.B., Myers, C.L., Vaughn, M.W., and, Springer, N.M., (2013) Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell, 25, 780-793.
41. Margueron, R., and, Reinberg, D., (2011) The Polycomb complex PRC2 and its mark in life. Nature, 469, 343-349.
42. Moon, Y.H., Kang, H.G., Jung, J.Y., Jeon, J.S., Sung, S.K., and, An, G., (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol. 120, 1193-1204.
43. Moon, Y.H., Chen, L., Pan, R.L., Chang, H.S., Zhu, T., Maffeo, D.M., and, Sung, Z.R., (2003) EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell, 15, 681-693.
44. Muller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E., and, Simon, J.A., (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell, 111, 197-208.
45. Nallamilli, B.R., Zhang, J., Mujahid, H., Malone, B.M., Bridges, S.M., and, Peng, Z., (2013) Polycomb group gene OsFIE2 regulates rice (Oryza sativa) seed development and grain filling via a mechanism distinct from Arabidopsis. PLoS Genet. 9, e1003322.
46. Nekrasov, M., Wild, B., and, Muller, J., (2005) Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep. 6, 348-353.
47. Ohmori, S., Kimizu, M., Sugita, M., Miyao, A., Hirochika, H., Uchida, E., Nagato, Y., and, Yoshida, H., (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell, 21, 3008-3025.
48. 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.
49. Pien, S., and, Grossniklaus, U., (2007) Polycomb group and trithorax group proteins in Arabidopsis. Biochim. Biophys. Acta, 1769, 375-382.
50. Prasad, K., Parameswaran, S., and, Vijayraghavan, U., (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J. 43, 915-928.
51. Saleh, A., Alvarez-Venegas, R., and, Avramova, Z., (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat. Protoc. 3, 1018-1025.
52. Schuettengruber, B., and, Cavalli, G., (2009) Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development, 136, 3531-3542.
53. Sentoku, N., Kato, H., Kitano, H., and, Imai, R., (2005) OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in non-vegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Mol. Genet. Genomics, 273, 1-9.
54. 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.
55. Thompson, B.E., Bartling, L., Whipple, C., Hall, D.H., Sakai, H., Schmidt, R., and, Hake, S., (2009) bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell, 21, 2578-2590.
56. Weinhofer, I., Hehenberger, E., Roszak, P., Hennig, L., and, Kohler, C., (2010) H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet. 6, e1001152.
57. Xiao, H., Tang, J., Li, Y., et al. (2009) STAMENLESS 1, encoding a single C2H2 zinc finger protein, regulates floral organ identity in rice. Plant J. 59, 789-801.
58. Xu, X., Kawasaki, S., Fujimura, T., and, Wang, C., (2005) A protocol for high-throughput extraction of DNA from rice leaves. Plant Mol. Biol. Rep. 23, 291-295.
59. Yamaki, S., Nagato, Y., Kurata, N., and, Nonomura, K., (2011) Ovule is a lateral organ finally differentiated from the terminating floral meristem in rice. Dev. Biol. 351, 208-216.
60. Yang, C.H., Chen, L.J., and, Sung, Z.R., (1995) Genetic regulation of shoot development in Arabidopsis: role of the EMF genes. Dev. Biol. 169, 421-435.
61. Yang, J., Lee, S., Hang, R., Kim, S.R., Lee, Y.S., Cao, X., Amasino, R., and, An, G., (2012) OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J. 73, 566-578.
62. Yoshida, H., and, Nagato, Y., (2011) Flower development in rice. J. Exp. Bot. 62, 4719-4730.
63. Yoshida, N., Yanai, Y., Chen, L., Kato, Y., Hiratsuka, J., Miwa, T., Sung, Z.R., and, Takahashi, S., (2001) EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell, 13, 2471-2481.
64. Zhang, J., Nallamilli, B.R., Mujahid, H., and, Peng, Z., (2010) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J. 64, 604-617.
65. Zhang, L., Cheng, Z., Qin, R., et al. (2012) Identification and Characterization of an Epi-Allele of FIE1 Reveals a Regulatory Linkage between Two Epigenetic Marks in Rice. Plant Cell, 24, 4407-4421.