Interactions of OsMADS1 with floral homeotic genes in rice flower development

Molecular Plant

Volumn 8, Issue 9, 2015, Pages 1366-1384

  Hu, Yun ^a   Liang, Wanqi ^a   Yin, Changsong ^a   Yang, Xuelian ^a   Ping, Baozhe ^a   Li, Anxue ^b   Jia, Ru ^a   Chen, Mingjiao ^a   Luo, Zhijing ^a   Cai, Qiang ^a   Zhao, Xiangxiang ^c   Zhang, Dabing ^a,d   Yuan, Zheng ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SHANGHAI OCEAN UNIVERSITY   (China)

^c HUAIYIN NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

floral homeotic genes; floral meristem; floral organ identity; OsMADS1; regulatory network

Indexed keywords

MADS DOMAIN PROTEIN; VEGETABLE PROTEIN;

DNA MICROARRAY; EPISTASIS; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOBOX; MERISTEM; METABOLISM; ORYZA; PHENOTYPE; PLANT GENE;

EPISTASIS, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, HOMEOBOX; GENES, PLANT; MADS DOMAIN PROTEINS; MERISTEM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORYZA; PHENOTYPE; PLANT PROTEINS;

EID: 84941168046     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.04.009     Document Type: Article

References (101)

1. G.K. Agrawal, K. Abe, M. Yamazaki, A. Miyao, and H. Hirochika 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 2005 125 135
2. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate: A practical and powerful approach to multiple testing J. Roy. Stat. Soc. B 57 1995 289 300
3. M.A. Blazquez, L.N. Soowal, I. Lee, and D. Weigel LEAFY expression and flower initiation in Arabidopsis Development 124 1997 3835 3844
4. C. Bowler, G. Benvenuto, P. Laflamme, D. Molino, A.V. Probst, M. Tariq, and J. Paszkowski Chromatin techniques for plant cells Plant J. 39 2004 776 789
5. J.L. Bowman, J. Alvarez, D. Weigel, E.M. Meyerowitz, and D.R. Smyth Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes Development 119 1993 721 743
6. M.A. Busch, K. Bomblies, and D. Weigel Activation of a floral homeotic gene in Arabidopsis Science 285 1999 585 587
7. J. Cacharrón, H. Saedler, and G. Theißen Expression of MADS box genes ZMM8 and ZMM14 during inflorescence development of Zea mays discriminates between the upper and the lower floret of each spikelet Dev. Genes Evol. 209 1999 411 420
8. Q. Cai, Z. Yuan, M. Chen, C. Yin, Z. Luo, X. Zhao, W. Liang, J. Hu, and D. Zhang Jasmonic acid regulates spikelet development in rice Nat. Commun. 5 2014 3476
9. C. Castillejo, M. Romera-Branchat, and S. Pelaz A new role of the Arabidopsis SEPALLATA3 gene revealed by its constitutive expression Plant J. 43 2005 586 596
10. B. Causier, Z. Schwarz-Sommer, and B. Davies Floral organ identity: 20 years of ABCs Semin. Cell Dev. Biol. 21 2010 73 79
11. Z.X. Chen, J.G. Wu, W.N. Ding, H.M. Chen, P. Wu, and C.H. Shi Morphogenesis and molecular basis on naked seed rice, a novel homeotic mutation of OsMADS1 regulating transcript level of AP3 homologue in rice Planta 223 2006 882 890
12. A.R. Christensen, and S.T. Malcomber Duplication and diversification of the LEAFY HULL STERILE1 and Oryza sativa MADS5 SEPALLATA lineages in graminoid Poales Evodevo 3 2012 4
13. G. Chuck, R. Meeley, and S. Hake Floral meristem initiation and meristem cell fate are regulated by the maize AP2 genes ids1 and sid1 Development 135 2008 3013 3019
14. M. Ciaffi, A.R. Paolacci, O.A. Tanzarella, and E. Porceddu Molecular aspects of flower development in grasses Sex. Plant Reprod. 24 2011 247 282
15. E.S. Coen, and E.M. Meyerowitz The war of the whorls: genetic interactions controlling flower development Nature 353 1991 31 37
16. L. Colombo, J. Franken, E. Koetje, J. van Went, H.J. Dons, G.C. Angenent, and A.J. van Tunen The petunia MADS box gene FBP11 determines ovule identity Plant Cell 7 1995 1859 1868
17. R. Cui, J. Han, S. Zhao, K. Su, F. Wu, X. Du, Q. Xu, K. Chong, G. Theißen, and Z. Meng Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa) Plant J. 61 2010 767 781
18. P. Derbyshire, and M.E. Byrne MORE SPIKELETS1 is required for spikelet fate in the inflorescence of Brachypodium Plant Physiol. 161 2013 1291 1302
19. G. Ditta, A. Pinyopich, P. Robles, S. Pelaz, and M.F. Yanofsky The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity Curr. Biol. 14 2004 1935 1940
20. L. Dreni, and M.M. Kater MADS reloaded: evolution of the AGAMOUS subfamily genes New Phytol. 201 2014 717 732
21. L. Dreni, S. Jacchia, F. Fornara, M. Fornari, P.B. Ouwerkerk, G. An, L. Colombo, and M.M. Kater The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice Plant J. 52 2007 690 699
22. L. Dreni, A. Pilatone, D. Yun, S. Erreni, A. Pajoro, E. Caporali, D. Zhang, and M.M. Kater Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy Plant Cell 23 2011 2850 2863
23. L. Dreni, M. Osnato, and M.M. Kater The ins and outs of the rice AGAMOUS subfamily Mol. Plant 6 2013 650 664
24. R. Favaro, A. Pinyopich, R. Battaglia, M. Kooiker, L. Borghi, G. Ditta, M.F. Yanofsky, M.M. Kater, and L. Colombo MADS-box protein complexes control carpel and ovule development in Arabidopsis Plant Cell 15 2003 2603 2611
25. C. Ferrandiz, Q. Gu, R. Martienssen, and M.F. Yanofsky Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER Development 127 2000 725 734
26. X. Gao, W. Liang, C. Yin, S. Ji, H. Wang, X. Su, C. Guo, H. Kong, H. Xue, and D. Zhang The SEPALLATA-like gene OsMADS34 is required for rice inflorescence and spikelet development Plant Physiol. 153 2010 728 740
27. T. Honma, and K. Goto Complexes of MADS-box proteins are sufficient to convert leaves into floral organs Nature 409 2001 525 529
28. L. Hu, W. Liang, C. Yin, X. Cui, J. Zong, X. Wang, J. Hu, and D. Zhang Rice MADS3 regulates ROS homeostasis during late anther development Plant Cell 23 2011 515 533
29. Y. Huang, W. Liang, A. Pan, Z. Zhou, C. Huang, J. Chen, and D. Zhang Production of FaeG, the major subunit of K88 fimbriae, in transgenic tobacco plants and its immunogenicity in mice Infect. Immun. 71 2003 5436 5439
30. K. Ikeda-Kawakatsu, M. Maekawa, T. Izawa, J. Itoh, and Y. Nagato ABERRANT PANICLE ORGANIZATION 2/RFL, the rice ortholog of Arabidopsis LEAFY, suppresses the transition from inflorescence meristem to floral meristem through interaction with APO1 Plant J. 69 2012 168 180
31. R.G. Immink, I.A. Tonaco, S. de Folter, A. Shchennikova, A.D. van Dijk, J. Busscher-Lange, J.W. Borst, and G.C. Angenent SEPALLATA3: the "glue" for MADS box transcription factor complex formation Genome Biol. 10 2009 R24
32. V.F. Irish, and I.M. Sussex Function of the apetala-1 gene during Arabidopsis floral development Plant Cell 2 1990 741 753
33. R.A. Irizarry, B. Hobbs, F. Collin, Y.D. Beazer-Barclay, K.J. Antonellis, U. Scherf, and T.P. Speed Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 4 2003 249 264
34. J.S. Jeon, S. Jang, S. Lee, J. Nam, C. Kim, S.H. Lee, Y.Y. Chung, S.R. Kim, Y.H. Lee, Y.G. Cho, and et al. leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development Plant Cell 12 2000 871 884
35. M.M. Kater, L. Dreni, and L. Colombo Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis J. Exp. Bot. 57 2006 3433 3444
36. K. Kaufmann, J.M. Muino, R. Jauregui, C.A. Airoldi, C. Smaczniak, P. Krajewski, and G.C. Angenent Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower PLoS Biol. 7 2009 e1000090
37. E.A. Kellogg Evolutionary history of the grasses Plant Physiol. 125 2001 1198 1205
38. I. Khanday, S.R. Yadav, and U. Vijayraghavan Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways Plant Physiol. 161 2013 1970 1983
39. K. Kobayashi, M. Maekawa, A. Miyao, H. Hirochika, and J. Kyozuka PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice Plant Cell Physiol. 51 2010 47 57
40. K. Kobayashi, N. Yasuno, Y. Sato, M. Yoda, R. Yamazaki, M. Kimizu, H. Yoshida, Y. Nagamura, and J. Kyozuka 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 2012 1848 1859
41. H. Kouchi, and S. Hata Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development Mol. Gen. Genet. 238 1993 106 119
42. J. Kyozuka, and K. Shimamoto Ectopic expression of OsMADS3, a rice ortholog of AGAMOUS, caused a homeotic transformation of lodicules to stamens in transgenic rice plants Plant Cell Physiol. 43 2002 130 135
43. J. Kyozuka, T. Kobayashi, M. Morita, and K. Shimamoto Spatially and temporally regulated expression of rice MADS box genes with similarity to Arabidopsis class A, B and C genes Plant Cell Physiol. 41 2000 710 718
44. D.Y. Lee, and G. An Two AP2 family genes, SUPERNUMERARY BRACT (SNB) and OsINDETERMINATE SPIKELET 1 (OsIDS1), synergistically control inflorescence architecture and floral meristem establishment in rice Plant J. 69 2012 445 461
45. S. Lee, J.S. Jeon, K. An, Y.H. Moon, Y.Y. Chung, and G. An Alteration of floral organ identity in rice through ectopic expression of OsMADS16 Planta 217 2003 904 911
46. D.Y. Lee, J. Lee, S. Moon, S.Y. Park, and G. An The rice heterochronic gene SUPERNUMERARY BRACT regulates the transition from spikelet meristem to floral meristem Plant J. 49 2007 64 78
47. M. Lenhard, A. Bohnert, G. Jurgens, and T. Laux Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS Cell 105 2001 805 814
48. N. Li, D.S. Zhang, H.S. Liu, C.S. Yin, X.X. Li, W.Q. Liang, Z. Yuan, B. Xu, H.W. Chu, J. Wang, and et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development Plant Cell 18 2006 2999 3014
49. H. Li, W. Liang, R. Jia, C. Yin, J. Zong, H. Kong, and D. Zhang The AGL6-like gene OsMADS6 regulates floral organ and meristem identities in rice Cell Res. 20 2010 299 313
50. H. Li, W. Liang, Y. Hu, L. Zhu, C. Yin, J. Xu, L. Dreni, M.M. Kater, and D. Zhang Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate Plant Cell 23 2011 2536 2552
51. H. Li, W. Liang, C. Yin, L. Zhu, and D. Zhang Genetic interaction of OsMADS3, DROOPING LEAF, and OsMADS13 in specifying rice floral organ identities and meristem determinacy Plant Physiol. 156 2011 263 274
52. J. Lim, Y.H. Moon, G. An, and S.K. Jang Two rice MADS domain proteins interact with OsMADS1 Plant Mol. Biol. 44 2000 513 527
53. A. Litt, and E.M. Kramer The ABC model and the diversification of floral organ identity Semin. Cell Dev. Biol. 21 2010 129 137
54. C. Liu, W. Xi, L. Shen, C. Tan, and H. Yu Regulation of floral patterning by flowering time genes Dev. Cell 16 2009 711 722
55. J.U. Lohmann, R.L. Hong, M. Hobe, M.A. Busch, F. Parcy, R. Simon, and D. Weigel A molecular link between stem cell regulation and floral patterning in Arabidopsis Cell 105 2001 793 803
56. Z.P. Lopez-Dee, P. Wittich, M. Enrico Pe, D. Rigola, I. Del Buono, M.S. Gorla, M.M. Kater, and L. Colombo OsMADS13, a novel rice MADS-box gene expressed during ovule development Dev. Genet. 25 1999 237 244
57. S.T. Malcomber, and E.A. Kellogg Heterogeneous expression patterns and separate roles of the SEPALLATA gene LEAFY HULL STERILE1 in grasses Plant Cell 16 2004 1692 1706
58. S.T. Malcomber, and E.A. Kellogg SEPALLATA gene diversification: brave new whorls Trends Plant Sci. 10 2005 427 435
59. M.A. Mandel, C. Gustafson-Brown, B. Savidge, and M.F. Yanofsky Molecular characterization of the Arabidopsis floral homeotic gene APETALA1 Nature 360 1992 273 277
60. Y.H. Moon, H.G. Kang, J.Y. Jung, J.S. Jeon, S.K. Sung, and G. An Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system Plant Physiol. 120 1999 1193 1204
61. N. Nagasawa, M. Miyoshi, Y. Sano, H. Satoh, H. Hirano, H. Sakai, and Y. Nagato SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice Development 130 2003 705 718
62. O. Nilsson, I. Lee, M.A. Blazquez, and D. Weigel Flowering-time genes modulate the response to LEAFY activity Genetics 150 1998 403 410
63. S. Ohmori, M. Kimizu, M. Sugita, A. Miyao, H. Hirochika, E. Uchida, Y. Nagato, and H. Yoshida MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice Plant Cell 21 2009 3008 3025
64. S. Pelaz, G.S. Ditta, E. Baumann, E. Wisman, and M.F. Yanofsky B and C floral organ identity functions require SEPALLATA MADS-box genes Nature 405 2000 200 203
65. S. Pelaz, C. Gustafson-Brown, S.E. Kohalmi, W.L. Crosby, and M.F. Yanofsky APETALA1 and SEPALLATA3 interact to promote flower development Plant J. 26 2001 385 394
66. S. Pelaz, R. Tapia-Lopez, E.R. Alvarez-Buylla, and M.F. Yanofsky Conversion of leaves into petals in Arabidopsis Curr. Biol. 11 2001 182 184
67. A. Pinyopich, G.S. Ditta, B. Savidge, S.J. Liljegren, E. Baumann, E. Wisman, and M.F. Yanofsky Assessing the redundancy of MADS-box genes during carpel and ovule development Nature 424 2003 85 88
68. K. Prasad, and U. Vijayraghavan Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncovers its second-whorl-specific function in floral organ patterning Genetics 165 2003 2301 2305
69. K. Prasad, P. Sriram, C.S. Kumar, K. Kushalappa, and U. Vijayraghavan Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals Dev. Genes Evol. 211 2001 281 290
70. K. Prasad, S. Parameswaran, and U. Vijayraghavan 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 2005 915 928
71. J.C. Preston, and E.A. Kellogg Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae) Genetics 174 2006 421 437
72. P. Prusinkiewicz, Y. Erasmus, B. Lane, L.D. Harder, and E. Coen Evolution and development of inflorescence architectures Science 316 2007 1452 1456
73. R. Reinheimer, and E.A. Kellogg Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new Plant Cell 21 2009 2591 2605
74. D. Ren, Y. Li, F. Zhao, X. Sang, J. Shi, N. Wang, S. Guo, Y. Ling, C. Zhang, Z. Yang, and et al. MULTI-FLORET SPIKELET1, which encodes an AP2/ERF protein, determines spikelet meristem fate and sterile lemma identity in rice Plant Physiol. 162 2013 872 884
75. A.S. Rijpkema, M. Vandenbussche, R. Koes, K. Heijmans, and T. Gerats Variations on a theme: changes in the floral ABCs in angiosperms Semin. Cell Dev. Biol. 21 2010 100 107
76. Y. Sato, S.K. Hong, A. Tagiri, H. Kitano, N. Yamamoto, Y. Nagato, and M. Matsuoka A rice homeobox gene, OSH1, is expressed before organ differentiation in a specific region during early embryogenesis Proc. Natl. Acad. Sci. USA 93 1996 8117 8122
77. G.K. Smyth Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat. Appl. Genet. Mol. Biol. 3 2004 Article3
78. D.E. Soltis, A.S. Chanderbali, S. Kim, M. Buzgo, and P.S. Soltis The ABC model and its applicability to basal angiosperms Ann. Bot. 100 2007 155 163
79. B. Sun, Y. Xu, K.H. Ng, and T. Ito A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem Genes Dev. 23 2009 1791 1804
80. B. Sun, L.S. Looi, S. Guo, Z. He, E.S. Gan, J. Huang, Y. Xu, W.Y. Wee, and T. Ito Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells Science 343 2014 1248559
81. G. Theissen, and H. Saedler Plant biology. Floral quartets Nature 409 2001 469 471
82. G. Theissen, and R. Melzer Molecular mechanisms underlying origin and diversification of the angiosperm flower Ann. Bot. 100 2007 603 619
83. K. Wang, D. Tang, L. Hong, W. Xu, J. Huang, M. Li, M. Gu, Y. Xue, and Z. Cheng DEP and AFO regulate reproductive habit in rice PLoS Genet. 6 2010 e1000818
84. D. Weigel, J. Alvarez, D.R. Smyth, M.F. Yanofsky, and E.M. Meyerowitz LEAFY controls floral meristem identity in Arabidopsis Cell 69 1992 843 859
85. H. Xiao, Y. Wang, D. Liu, W. Wang, X. Li, X. Zhao, J. Xu, W. Zhai, and L. Zhu Functional analysis of the rice AP3 homologue OsMADS16 by RNA interference Plant Mol. Biol. 52 2003 957 966
86. J. Xu, C. Yang, Z. Yuan, D. Zhang, M.Y. Gondwe, Z. Ding, W. Liang, and Z.A. Wilson The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana Plant Cell 22 2010 91 107
87. S.R. Yadav, K. Prasad, and U. Vijayraghavan Divergent regulatory OsMADS2 functions control size, shape and differentiation of the highly derived rice floret second-whorl organ Genetics 176 2007 283 294
88. T. Yamaguchi, N. Nagasawa, S. Kawasaki, M. Matsuoka, Y. Nagato, and H.Y. Hirano The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa Plant Cell 16 2004 500 509
89. T. Yamaguchi, D.Y. Lee, A. Miyao, H. Hirochika, G. An, and H.Y. Hirano Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa Plant Cell 18 2006 15 28
90. S.G. Yao, S. Ohmori, M. Kimizu, and H. Yoshida Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development Plant Cell Physiol. 49 2008 853 857
91. R. Yockteng, A.M. Almeida, K. Morioka, E.R. Alvarez-Buylla, and C.D. Specht Molecular evolution and patterns of duplication in the SEP/AGL6-like lineage of the zingiberales: a proposed mechanism for floral diversification Mol. Biol. Evol. 30 2013 2401 2422
92. H. Yoshida Is the lodicule a petal: molecular evidence? Plant Sci. 184 2012 121 128
93. H. Yoshida, and Y. Nagato Flower development in rice J. Exp. Bot. 62 2011 4719 4730
94. Z. Yuan, S. Gao, D.W. Xue, D. Luo, L.T. Li, S.Y. Ding, X. Yao, Z.A. Wilson, Q. Qian, and D.B. Zhang RETARDED PALEA1 controls palea development and floral zygomorphy in rice Plant Physiol. 149 2009 235 244
95. L.M. Zahn, H. Kong, J.H. Leebens-Mack, S. Kim, P.S. Soltis, L.L. Landherr, D.E. Soltis, C.W. Depamphilis, and H. Ma The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history Genetics 169 2005 2209 2223
96. X. Zhang Plant science. Delayed gratification-waiting to terminate stem cell identity Science 343 2014 498 499
97. D. Zhang, and Z. Wilson Stamen specification and anther development in rice Chin. Sci. Bull. 54 2009 2342 2353
98. D. Zhang, and Z. Yuan Molecular control of grass inflorescence development Annu. Rev. Plant Biol. 65 2014 553 578
99. D. Zhang, W. Liang, C. Yin, J. Zong, and F. Gu OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice Plant Physiol. 154 2010 149 162
100. D. Zhang, Z. Yuan, G. An, L. Dreni, J. Hu, and M. Kater Panicle development Q. Zhang, R. Wing, Genetics and Genomics of Rice 2013 Springer New York 279 295
101. Y. Zhang, W. Liang, J. Shi, J. Xu, and D. Zhang MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana J. Integr. Plant Biol. 55 2013 1166 1178