Genome-wide binding analysis of the transcription activator IDEAL PLANT ARCHITECTURE1 reveals a complex network regulating rice plant architecture

Plant Cell

Volumn 25, Issue 10, 2013, Pages 3743-3759

  Lu, Zefu ^a   Yu, Hong ^a   Xiong, Guosheng ^a   Wang, Jing ^a,c   Jiao, Yongqing ^a,d   Liu, Guifu ^a   Jing, Yanhui ^a   Meng, Xiangbing ^a   Hu, Xingming ^b   Qian, Qian ^b   Fu, Xiangdong ^a   Wang, Yonghong ^a   Li, Jiayang ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b CHINA NATIONAL RICE RESEARCH INSTITUTE   (China)

^c SICHUAN AGRICULTURAL UNIVERSITY   (China)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ORYZA SATIVA;

TRANSCRIPTION FACTOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

BINDING SITE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT GENE; PROMOTER REGION; PROTEIN DOMAIN; RICE; TRANSCRIPTION INITIATION; TRANSGENIC PLANT;

BINDING SITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; ORYZA SATIVA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME;

EID: 84888411699     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.113639     Document Type: Article

References (76)

1. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H., and Kyozuka, J. (2007). DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51: 1019-1029.
2. Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S., and Kyozuka, J. (2009). d14, a strigolactoneinsensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 50: 1416-1424.
3. Ashburner, M., et al; The Gene Ontology Consortium (2000). Gene ontology: Tool for the unification of biology. Nat. Genet. 25: 25-29.
4. Ashikari, M., Sakakibara, H., Lin, S., Yamamoto, T., Takashi, T., Nishimura, A., Angeles, E.R., Qian, Q., Kitano, H., and Matsuoka, M. (2005). Cytokinin oxidase regulates rice grain production. Science 309: 741-745.
5. Avraham, S., et al. (2008). The Plant Ontology Database: A community resource for plant structure and developmental stages controlled vocabulary and annotations. Nucleic Acids Res. 36 (Database issue): D449-D454.
6. Bailey, T.L. (2011). DREME: Motif discovery in transcription factor ChIP-seq data. Bioinformatics 27: 1653-1659.
7. Bart, R., Chern, M., Park, C.J., Bartley, L., and Ronald, P.C. (2006). A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2: 13.
8. Birkenbihl, R.P., Jach, G., Saedler, H., and Huijser, P. (2005). Functional dissection of the plant-specific SBP-domain: Overlap of the DNA-binding and nuclear localization domains. J. Mol. Biol. 352: 585-596.
9. Bolduc, N., Yilmaz, A., Mejia-Guerra, M.K., Morohashi, K., O'Connor, D., Grotewold, E., and Hake, S. (2012). Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev. 26: 1685-1690.
10. Busch, W., et al. (2010). Transcriptional control of a plant stem cell niche. Dev. Cell 18: 849-861.
11. Donald, C. (1968). The breeding of crop ideotypes. Euphytica 17: 385-403.
12. Dun, E.A., de Saint Germain, A., Rameau, C., and Beveridge, C.A. (2012). Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol. 158: 487-498.
13. Fornara, F., and Coupland, G. (2009). Plant phase transitions make a SPLash. Cell 138: 625-627.
14. Gandikota, M., Birkenbihl, R.P., Höhmann, S., Cardon, G.H., Saedler, H., and Huijser, P. (2007). The miRNA156/157 recognition element in the 39 UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 49: 683-693.
15. Gou, J.Y., Felippes, F.F., Liu, C.J., Weigel, D., and Wang, J.W. (2011). Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23: 1512-1522.
16. Guo, J., Song, J., Wang, F., and Zhang, X.S. (2007). Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol. Biol. 64: 349-360.
17. Guo, S., Xu, Y., Liu, H., Mao, Z., Zhang, C., Ma, Y., Zhang, Q., Meng, Z., and Chong, K. (2013). The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun. 4: 1566.
18. Hu, M., Yu, J., Taylor, J.M., Chinnaiyan, A.M., and Qin, Z.S. (2010). On the detection and refinement of transcription factor binding sites using ChIP-Seq data. Nucleic Acids Res. 38: 2154-2167.
19. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J., and Fu, X. (2009). Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41: 494-497.
20. Ikeda, A., Ueguchi-Tanaka, M., Sonoda, Y., Kitano, H., Koshioka, M., Futsuhara, Y., Matsuoka, M., and Yamaguchi, J. (2001). slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the heightregulating gene GAI/RGA/RHT/D8. Plant Cell 13: 999-1010.
21. Ishikawa, S., Maekawa, M., Arite, T., Onishi, K., Takamure, I., and Kyozuka, J. (2005). Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46: 79-86.
22. Jaiswal, P., Ware, D., Ni, J., Chang, K., Zhao, W., Schmidt, S., Pan, X., Clark, K., Teytelman, L., Cartinhour, S., Stein, L., and McCouch, S. (2002). Gramene: Development and integration of trait and gene ontologies for rice. Comp. Funct. Genomics 3: 132-136.
23. Jansen, R., Yu, H., Greenbaum, D., Kluger, Y., Krogan, N.J., Chung, S., Emili, A., Snyder, M., Greenblatt, J.F., and Gerstein, M. (2003). A Bayesian networks approach for predicting proteinprotein interactions from genomic data. Science 302: 449-453.
24. Jeong, D.H., Park, S., Zhai, J., Gurazada, S.G., De Paoli, E., Meyers, B.C., and Green, P.J. (2011). Massive analysis of rice small RNAs: Mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23: 4185-4207.
25. Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., Qian, Q., and Li, J. (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42: 541-544.
26. Johnson, D.S., et al. (2008). Systematic evaluation of variability in ChIP-chip experiments using predefined DNA targets. Genome Res. 18: 393-403.
27. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., and Tanabe, M. (2012). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40 (Database issue): D109-D114.
28. Khush, G.S. (1995). Breaking the yield frontier of rice. GeoJournal 35: 329-332.
29. 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.
30. Kosugi, S., and Ohashi, Y. (1997). PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9: 1607-1619.
31. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., Sakakibara, H., and Kyozuka, J. (2007). Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652-655.
32. Landt, S.G., et al. (2012). ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 22: 1813-1831.
33. Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Zhao, H., Lee, I., and Deng, X.W. (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731-749.
34. Li, G., Hall, T.C., and Holmes-Davis, R. (2002). Plant chromatin: Development and gene control. Bioessays 24: 234-243.
35. Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., and Wang, J. (2009). SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
36. Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J., and Wang, Y. (2009). DWARF27, an ironcontaining protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512-1525.
37. Martín-Trillo, M., and Cubas, P. (2010). TCP genes: A family snapshot ten years later. Trends Plant Sci. 15: 31-39.
38. Minakuchi, K., Kameoka, H., Yasuno, N., Umehara, M., Luo, L., Kobayashi, K., Hanada, A., Ueno, K., Asami, T., Yamaguchi, S., and Kyozuka, J. (2010). FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol. 51: 1127-1135.
39. Miura, K., Ikeda, M., Matsubara, A., Song, X.J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., and Ashikari, M. (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42: 545-549.
40. Niwa, M., Daimon, Y., Kurotani, K., Higo, A., Pruneda-Paz, J.L., Breton, G., Mitsuda, N., Kay, S.A., Ohme-Takagi, M., Endo, M., and Araki, T. (2013). BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25: 1228-1242.
41. Oh, E., Yamaguchi, S., Hu, J., Yusuke, J., Jung, B., Paik, I., Lee, H.S., Sun, T.P., Kamiya, Y., and Choi, G. (2007). PIL5, a phytochrome-interacting bHLH protein, regulates gibberellin responsiveness by binding directly to the GAI and RGA promoters in Arabidopsis seeds. Plant Cell 19: 1192-1208.
42. Ouyang, S., et al. (2007). The TIGR Rice Genome Annotation Resource: Improvements and new features. Nucleic Acids Res. 35 (Database issue): D883-D887.
43. Pujar, A., et al. (2006). Whole-plant growth stage ontology for angiosperms and its application in plant biology. Plant Physiol. 142: 414-428.
44. Qiao, Y., Piao, R., Shi, J., Lee, S.I., Jiang, W., Kim, B.K., Lee, J., Han, L., Ma, W., and Koh, H.J. (2011). Fine mapping and candidate gene analysis of dense and erect panicle 3, DEP3, which confers high grain yield in rice (Oryza sativa L.). Theor. Appl. Genet. 122: 1439-1449.
45. Rao, N.N., Prasad, K., Kumar, P.R., and Vijayraghavan, U. (2008). Distinct regulatory role for RFL, the rice LFY homolog, in determining flowering time and plant architecture. Proc. Natl. Acad. Sci. USA 105: 3646-3651.
46. Reyes, J.C., Hennig, L., and Gruissem, W. (2002). Chromatinremodeling and memory factors. New regulators of plant development. Plant Physiol. 130: 1090-1101.
47. Rhodes, D.R., Tomlins, S.A., Varambally, S., Mahavisno, V., Barrette, T., Kalyana-Sundaram, S., Ghosh, D., Pandey, A., and Chinnaiyan, A.M. (2005). Probabilistic model of the human proteinprotein interaction network. Nat. Biotechnol. 23: 951-959.
48. 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.
49. Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., Ishiyama, K., Saito, T., Kobayashi, M., Khush, G.S., Kitano, H., and Matsuoka, M. (2002). Green revolution: A mutant gibberellin-synthesis gene in rice. Nature 416: 701-702.
50. Sasaki, A., Itoh, H., Gomi, K., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Jeong, D.H., An, G., Kitano, H., Ashikari, M., and Matsuoka, M. (2003). Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299: 1896-1898.
51. Spitz, F., and Furlong, E.E. (2012). Transcription factors: From enhancer binding to developmental control. Nat. Rev. Genet. 13: 613-626.
52. Sun, Y., et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19: 765-777.
53. Takeda, T., Suwa, Y., Suzuki, M., Kitano, H., Ueguchi-Tanaka, M., Ashikari, M., Matsuoka, M., and Ueguchi, C. (2003). The OsTB1 gene negatively regulates lateral branching in rice. Plant J. 33: 513-520.
54. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
55. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562-578.
56. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511-515.
57. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.Y., Hsing, Y.I., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698.
58. Unte, U.S., Sorensen, A.M., Pesaresi, P., Gandikota, M., Leister, D., Saedler, H., and Huijser, P. (2003). SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15: 1009-1019.
59. Valouev, A., Johnson, D.S., Sundquist, A., Medina, C., Anton, E., Batzoglou, S., Myers, R.M., and Sidow, A. (2008). Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods 5: 829-834.
60. Virk, P., Khush, G., and Peng, S. (2004). Breeding to enhance yield potential of rice at IRRI: The ideotype approach. Int. Rice Res. Notes 29: 5-9.
61. Wang, J.W., Czech, B., and Weigel, D. (2009). MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738-749.
62. Wang, S., Wu, K., Yuan, Q., Liu, X., Liu, Z., Lin, X., Zeng, R., Zhu, H., Dong, G., Qian, Q., Zhang, G., and Fu, X. (2012). Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44: 950-954.
63. Wang, Y., and Li, J. (2008). Molecular basis of plant architecture. Annu. Rev. Plant Biol. 59: 253-279.
64. Winter, C.M., et al. (2011). LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev. Cell 20: 430-443.
65. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., and Poethig, R.S. (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750-759.
66. Wu, G., and Poethig, R.S. (2006). Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539-3547.
67. Yamaguchi, A., Wu, M.F., Yang, L., Wu, G., Poethig, R.S., and Wagner, D. (2009). The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell 17: 268-278.
68. Yamasaki, K., et al. (2004). A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBPfamily transcription factors. J. Mol. Biol. 337: 49-63.
69. Youens-Clark, K., et al. (2011). Gramene database in 2010: Updates and extensions. Nucleic Acids Res. 39 (Database issue): D1085-D1094.
70. Yu, H., Huang, J., Qiao, N., Green, C.D., and Han, J.D. (2010). Evaluating diabetes and hypertension disease causality using mouse phenotypes. BMC Syst. Biol. 4: 97.
71. Yu, N., Cai, W.J., Wang, S., Shan, C.M., Wang, L.J., and Chen, X.Y. (2010). Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22: 2322-2335.
72. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., and Liu, X.S. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9: R137.
73. Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and Quail, P.H. (2013). A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9: e1003244.
74. Zheng, Y., Ren, N., Wang, H., Stromberg, A.J., and Perry, S.E. (2009). Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21: 2563-2577.
75. Zhu, Y., et al. (2006). ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18: 442-456.
76. Zou, J., Chen, Z., Zhang, S., Zhang, W., Jiang, G., Zhao, X., Zhai, W., Pan, X., and Zhu, L. (2005). Characterizations and fine mapping of a mutant gene for high tillering and dwarf in rice (Oryza sativa L.). Planta 222: 604-612.