The Arabidopsis floral homeotic proteins APETALA3 and PISTILLATA negatively regulate the BANQUO genes implicated in light signaling

Plant Cell

Volumn 22, Issue 3, 2010, Pages 690-702

  Mara, Chloe D ^a,b   Huang, Tengbo ^a   Irish, Vivian F ^a  

^a YALE UNIVERSITY   (United States)

^b Bldg 142   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 77953220026     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.065946     Document Type: Article

References (84)

1. Alonso, J.M., et al (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Alves-Ferreira, M., Wellmer, F., Banhara, A., Kumar, V., Riechmann, J.L., and Meyerowitz, E.M. (2007). Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol. 145: 747-762.
3. Bailey, P.C., Martin, C., Toledo-Ortiz, G., Quail, P.H., Huq, E., Heim, M.A., Jakoby, M., Werber, M., and Weisshaar, B. (2003). Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana. Plant Cell 15: 2497-2502.
4. Bi, Y.M., Zhang, Y., Signorelli, T., Zhao, R., Zhu, T., and Rothstein, S. (2005). Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. Plant J. 44: 680-692.
5. Bowman, J.L., Smyth, D.R., and Meyerowitz, E.M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1: 37-52.
6. Briggs, W.R. and Olney, M.A. (2001). Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol. 125: 85-88.
7. Castillon, A., Shen, H., and Huq, E. (2007). Phytochrome interacting factors: Central players in phytochrome-mediated light signaling networks. Trends Plant Sci. 12: 514-521.
8. Chae, E., Tan, Q.K., Hill, T.A., and Irish, V.F. (2008). An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135: 1235-1245.
9. Duek, P.D., Elmer, M.V., van Oosten, V.R., and Fankhauser, C. (2004). The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr. Biol. 14: 2296-2301.
10. Duek, P.D. and Fankhauser, C. (2003). HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signalling. Plant J. 34: 827-836.
11. Ellenberger, T., Fass, D., Arnaud, M., and Harrison, S.C. (1994). Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8: 970-980.
12. Fairchild, C.D., Schumaker, M.A., and Quail, P.H. (2000). HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev. 14: 2377-2391.
13. Fairman, R., Beran-Steed, R.K., Anthony-Cahill, S.J., Lear, J.D., Stafford, W.F., III, DeGrado, W.F., Benfield, P.A., and Brenner, S.L. (1993). Multiple oligomeric states regulate the DNA binding of helix-loop-helix peptides. Proc. Natl. Acad. Sci. USA 90: 10429-10433.
14. Franks, R.G., Liu, Z., and Fischer, R.L. (2006). SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals. Planta 224: 801-811.
15. Goto, K. and Meyerowitz, E.M. (1994). Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev. 8: 1548-1560.
16. Guo, Y. and Gan, S. (2006). AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J. 46: 601-612.
17. Hajdukiewicz, P., Svab, Z., and Maliga, P. (1994). The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25: 989-994.
18. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., and Bailey, P.C. (2003). The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol. Biol. Evol. 20: 735-747.
19. Hill, K., Wang, H., and Perry, S.E. (2008). A transcriptional repression motif in the MADS factor AGL15 is involved in recruitment of histone deacetylase complex components. Plant J. 53: 172-185.
20. Hill, T.A., Day, C.D., Zondlo, S.C., Thackeray, A.G., and Irish, V.F. (1998). Discrete spatial and temporal cis-acting elements regulate transcription of the Arabidopsis floral homeotic gene APETALA3. Development 125: 1711-1721.
21. Honma, T. and Goto, K. (2000). The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127: 2021-2030.
22. Honma, T. and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 469-471.
23. Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O., and Fankhauser, C. (2009). Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 28: 3893-3902.
24. Huq, E., Al-Sady, B., Hudson, M., Kim, C., Apel, K., and Quail, P.H. (2004). Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937-1941.
25. Huq, E. and Quail, P.H. (2002). PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21: 2441-2450.
26. Irish, V.F. (2008). The Arabidopsis petal: A model for plant organogenesis. Trends Plant Sci. 13: 430-436.
27. Ito, T., Takahashi, N., Shimura, Y., and Okada, K. (1997). A serine/threonine protein kinase gene isolated by an in vivo binding procedure using the Arabidopsis floral homeotic gene product, AGAMOUS. Plant Cell Physiol. 38: 248-258.
28. 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.
29. Jack, T., Brockman, L.L., and Meyerowitz, E.M. (1992). The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68: 683-697.
30. Jack, T., Fox, G.L., and Meyerowitz, E.M. (1994). Arabidopsis homeotic gene APETALA3 ectopic expression: Transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76: 703-716.
31. Jang, I.C., Yang, J.Y., Seo, H.S., and Chua, N.H. (2005). HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 19: 593-602.
32. Jang, I.C., Yang, S.W., Yang, J.Y., and Chua, N.H. (2007). Independent and interdependent functions of LAF1 and HFR1 in phytochrome A signaling. Genes Dev. 21: 2100-2111.
33. Jenik, P.D. and Irish, V.F. (2001). The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. Development 128: 13-23.
34. Jones, S. (2004). An overview of the basic helix-loop-helix proteins. Genome Biol. 5: 226.
35. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003). Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15: 2399-2407.
36. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19: 408-413.
37. Krizek, B.A. and Meyerowitz, E.M. (1996). The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122: 11-22.
38. Lamb, R.S., Hill, T.A., Tan, Q.K., and Irish, V.F. (2002). Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129: 2079-2086.
39. Laubinger, S., Zeller, G., Henz, S.R., Sachsenberg, T., Widmer, C.K., Naouar, N., Vuylsteke, M., Scholkopf, B., Ratsch, G., and Weigel, D. (2008). At-TAX: A whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol. 9: R112.
40. Lee, S., Lee, S., Yang, K.Y., Kim, Y.M., Park, S.Y., Kim, S.Y., and Soh, M.S. (2006). Overexpression of PRE1 and its homologous genes activates gibberellin-dependent responses in Arabidopsis thaliana. Plant Cell Physiol. 47: 591-600.
41. Li, X., et al (2006). Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol. 141: 1167-1184.
42. Lichtenthaler, H. (1987). Chlorophyll and carotenoids: pigments of the photosynthetic membranes. Methods Enzymol. 148: 350-382.
43. Maddison, W.P. and Maddison, D.R. (2000). MacClade, Analysis of Phylogeny and Character Evolution. (Sunderland, MA: Sinauer Associates).
44. Mara, C.D. and Irish, V.F. (2008). Two GATA transcription factors are downstream effectors of floral homeotic gene action in Arabidopsis. Plant Physiol. 147: 707-718.
45. Massari, M.E. and Murre, C. (2000). Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20: 429-440.
46. McGonigle, B., Bouhidel, K., and Irish, V.F. (1996). Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. Genes Dev. 10: 1812-1821.
47. Ng, M. and Yanofsky, M.F. (2001). Activation of the Arabidopsis B class homeotic genes by APETALA1. Plant Cell 13: 739-753.
48. Norton, J.D. (2000). ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J. Cell Sci. 113: 3897-3905.
49. Oh, E., Kim, J., Park, E., Kim, J.I., Kang, C., and Choi, G. (2004). PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16: 3045-3058.
50. Park, H.J., Ding, L., Dai, M., Lin, R., and Wang, H. (2008). Multisite phosphorylation of Arabidopsis HFR1 by casein kinase II and a plausible role in regulating its degradation rate. J. Biol. Chem. 283: 23264-23273.
51. Peiffer, J.A., Kaushik, S., Sakai, H., Arteaga-Vazquez, M., Sanchez-Leon, N., Ghazal, H., Vielle-Calzada, J.P., and Meyers, B.C. (2008). A spatial dissection of the Arabidopsis floral transcriptome by MPSS. BMC Plant Biol. 8: 43.
52. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and Yanofsky, M.F. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
53. Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E.R., and Yanofsky, M.F. (2001). Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11: 182-184.
54. Pires, N. and Dolan, L. (2010). Origin and diversification of basic-helix-loop-helix proteins in pants. Mol. Biol. Evol. 27: 862-874.
55. Pyke, K.A. and Page, A.M. (1998). Plastid ontogeny during petal development in Arabidopsis. Plant Physiol. 116: 797-803.
56. Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996b). Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA 93: 4793-4798.
57. Riechmann, J.L., Wang, M., and Meyerowitz, E.M. (1996a). DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24: 3134-3141.
58. Sablowski, R.W.M. and Meyerowitz, E.M. (1998). A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92: 93-103.
59. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
60. Schwarz-Sommer, Z., Hue, I., Huijser, P., Flor, P.J., Hansen, R., Tetens, F., Lonnig, W.-E., Saedler, H., and Sommer, H. (1992). Characterization of the Antirrhinum floral homeotic MADS-box gene deficiens: Evidence for DNA binding and autoregulation of its persistent expression throughout flower development. EMBO J. 11: 251-263.
61. Schwechheimer, C. and Willige, B.C. (2009). Shedding light on gibberellic acid signalling. Curr. Opin. Plant Biol. 12: 57-62.
62. Sessa, G., Carabelli, M., Sassi, M., Ciolfi, A., Possenti, M., Mittempergher, F., Becker, J., Morelli, G., and Ruberti, I. (2005). A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 19: 2811-2815.
63. Smith, H. (2000). Phytochromes and light signal perception by plants-An emerging synthesis. Nature 407: 585-591.
64. Soh, M.S., Kim, Y.M., Han, S.J., and Song, P.S. (2000). REP1, a basic helix-loop-helix protein, is required for a branch pathway of phytochrome A signaling in Arabidopsis. Plant Cell 12: 2061-2074.
65. Sridhar, V.V., Surendrarao, A., and Liu, Z. (2006). APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133: 3159-3166.
66. Sundstrom, J.F., Nakayama, N., Glimelius, K., and Irish, V.F. (2006). Direct regulation of the floral homeotic APETALA1 gene by APETALA3 and PISTILLATA in Arabidopsis. Plant J. 46: 593-600.
67. Swofford, D.L. (2000). PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods). (Sunderland, MA: Sinauer Associates).
68. Takahashi, H., Watanabe-Takahashi, A., Smith, F.W., Blake-Kalff, M., Hawkesford, M.J., and Saito, K. (2000). The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23: 171-182.
69. Tepperman, J.M., Hudson, M.E., Khanna, R., Zhu, T., Chang, S.H., Wang, X., and Quail, P.H. (2004). Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J. 38: 725-739.
70. Thomas-Chollier, M., Sand, O., Turatsinze, J.V., Janky, R., Defrance, M., Vervisch, E., Brohee, S., and van Helden, J. (2008). RSAT: Regulatory sequence analysis tools. Nucleic Acids Res. 36: W119-127.
71. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
72. Tilly, J., Allen, D.W., and Jack, T. (1998). The CArG boxes in the promoter of the Arabidopsis floral organ identity gene APETALA3 mediate diverse regulatory effects. Development 125: 1647-1657.
73. Toledo-Ortiz, G., Huq, E., and Quail, P.H. (2003). The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770.
74. Wang, H. and Deng, X.-W. (2004). Phytochrome signaling mechanisms. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD: American Society of Plant Biologists), doi/10.1199/tab.0074.1, http://www.aspb.org/publications/arabidopsis/.
75. Wang, H., Zhu, Y., Fujioka, S., Asami, T., and Li, J. (2009). Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 21: 3781-3791.
76. Wellmer, F., Riechmann, J.L., Alves-Ferreira, M., and Meyerowitz, E.M. (2004). Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16: 1314-1326.
77. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An electronic fluorescent pictograph browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.
78. Yang, J., Lin, R., Hoecker, U., Liu, B., Xu, L., and Wang, H. (2005a). Repression of light signaling by Arabidopsis SPA1 involves post-translational regulation of HFR1 protein accumulation. Plant J. 43: 131-141.
79. Yang, J., Lin, R., Sullivan, J., Hoecker, U., Liu, B., Xu, L., Deng, X.W., and Wang, H. (2005b). Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17: 804-821.
80. Yang, K.Y., Kim, Y.M., Lee, S., Song, P.S., and Soh, M.S. (2003a). Overexpression of a mutant basic helix-loop-helix protein HFR1, HFR1-deltaN105, activates a branch pathway of light signaling in Arabidopsis. Plant Physiol. 133: 1630-1642.
81. Yang, Y., Fanning, L., and Jack, T. (2003b). The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33: 47-59.
82. Zhang, X.N., Wu, Y., Tobias, J.W., Brunk, B.P., Deitzer, G.F., and Liu, D. (2008). HFR1 is crucial for transcriptome regulation in the cryptochrome 1-mediated early response to blue light in Arabidopsis thaliana. PLoS One 3: e3563.
83. Zik, M. and Irish, V.F. (2003). Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15: 207-222.
84. Zondlo, S.C. and Irish, V.F. (1999). CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J. 19: 259-268.