Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner

Plant Cell

Volumn 16, Issue 6, 2004, Pages 1490-1505

  Ferrario, Silvia ^a   Busscher, Jacqueline ^a   Franken, John ^a   Gerats, Tom ^a,b   Vandenbussche, Michiel ^a,c   Angenent, Gerco C ^a   Immink, Richard G H ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; GENETIC ENGINEERING; PROTEINS;

FLORAL ORGANS; FLORAL TRANSITIONS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA; INSERTION SEQUENCES; PETUNIA; PETUNIA HYBRIDA; PETUNIA X HYBRIDA; TRANSPOSONS;

EID: 2942666360     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.019679     Document Type: Article

References (72)

1. Abu-Shaar, M., Ryoo, H.D., and Mann, R.S. (1999). Control of the nuclear localization of Extradenticle by competing nuclear import and export signals. Genes Dev. 13, 935-945.
2. Angenent, G.C., Busscher, M., Franken, J., Mol, J.N.M., and Van Tunen, A.J. (1992). Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant Cell 4, 983-993.
3. Angenent, G.C., Franken, J., Busscher, M., Van Dijken, A., Van Went, J., Dons, H.J.M., and Van Tunen, A.J. (1995). A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7, 1569-1582.
4. Belaguli, N.S., Schildmeyer, L.A., and Schwartz, R.J. (1997). Organization and myogenic restricted expression of the murine serum response factor gene. J. Biol. Chem. 272, 18222-18231.
5. Belaguli, N.S., Zhou, W., Trinh, T.H.T., Majesky, M.W., and Schwartz, R.J. (1999). Dominant negative murine serum response factor: Alternative splicing within the activation domain inhibits transactivation of serum response factor binding targets. Mol. Cell. Biol. 19, 4582-4591.
6. Bevan, M.W. (1984). Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 12, 8711-8721.
7. Bonhomme, F., Kurz, B., Melzer, S., Bernier, G., and Jacqmard, A. (2000). Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J. 24, 103-111.
8. Borner, R., Kampmann, G., Chandler, J., Gleißner, R., Wisman, E., Apel, K., and Melzer, S. (2000). A MADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24, 591-599.
9. Bowman, J.L., Alvarez, J., Weigel, D., Meyerowitz, E.M., and Smyth, D.R. (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119, 721-743.
10. Burn, J.B., Smyth, D.R., Peacock, W.J., and Dennis, E.S. (1993). Genes conferring late flowering in Arabidopsis thaliana. Genetica 90, 147-155.
11. Cañas, L.A., Busscher, M., Angenent, G.C., Beltran, J.P., and Van Tunen, A.J. (1994). Nuclear localization of the petunia MADS box protein FBP1. Plant J. 6, 597-604.
12. Carmona, M.J., Ortega, N., and Garcìa-Maroto, F. (1998). Isolation and characterization of a new vegetative MADS-box gene from Solanum tuberosum L. Planta 207, 181-188.
13. Clarke, J.H., and Dean, C. (1994). Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol. Gen. Genet. 242, 81-89.
14. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
15. Colombo, L., Franken, J., Koetje, E., Van Went, J., Dons, H.J.M., Angenent, G., and Van Tunen, A.J. (1995). The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859-1868.
16. Croissant, J.D., Kim, J., Eichele, G., Goering, L., Lough, J., Prywes, R., and Schwartz, R.J. (1996). Avian serum response factor expression restricted primarily to muscle cell lineages is required for α-actin gene transcription. Dev. Biol. 177, 250-264.
17. Denecke, J., Gosselé, V., Botterman, J., and Cornelissen, M. (1989). Quantitative analysis of transiently expressed genes in plant cells. Methods Mol. Cell. Biol. 1, 19-27.
18. Feinberg, A.P., and Vogelstein, B. (1984). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137, 266-267.
19. Garcìa-Maroto, F., Ortega, N., Lozano, R., and Carmona, M.J. (2000). Characterization of the potato MADS-box gene STMADS16 and expression analysis in tobacco transgenic plants. Plant Mol. Biol. 42, 499-513.
20. Gerats, A.G.M., Huits, H., Vrijlandt, E., Maraña, C., Souer, E., and Beld, M. (1990). Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. Plant Cell 2, 1121-1128.
21. Gu, Q., Ferrándiz, C., Yanofsky, M.F., and Martienssen, R. (1998). The FRUITFUL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509-1517.
22. Hartmann, U., Höhmann, S., Nettesheim, K., Wisman, E., Saedler, H., and Huijser, P. (2000). Molecular cloning of SVP: A negative regulator of the floral transition in Arabidopsis. Plant J. 21, 351-360.
23. Hepworth, S.R., Valverde, F., Ravenscroft, D., Mouradov, A., and Coupland, G. (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327-4337.
24. Immink, R.G.H., Ferrario, S., Busscher-Lange, J., Kooiker, M., Busscher, M., and Angenent, G.C. (2003). Analysis of the petunia MADS-box transcription factor family. Mol. Genet. Genomics 268, 598-606.
25. Immink, R.G.H., Gadella, T.W., Jr., Ferrario, S., Busscher, M., and Angenent, G.C. (2002). Analysis of MADS box protein-protein interactions in living plant cells. Proc. Natl. Acad. Sci. USA 99, 2416-2421.
26. Immink, R.G.H., Hannapel, D.J., Ferrario, S., Busscher, M., Franken, J., Campagne, M.M.L., and Angenent, G.C. (1999). A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126, 5117-5126.
27. Irish, V.F., and Sussex, I.M. (1990). Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 2, 741-753.
28. Jeon, J., Jang, S., Lee, S., Nam, J., Kim, C., Lee, S., Chung, Y., Kim, S., Lee, Y.H., Cho, Y., and An, G. (2000). leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development. Plant Cell 12, 871-884.
29. Johansen, F.-E., and Prywes, R. (1993). Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol. Cell. Biol. 13, 4640-4647.
30. Kim, K.W., Shin, J.H., Moon, J., Kim, M., Lee, J., Park, M.C., and Lee, I. (2003). The function of the flowering time gene AGL20 is conserved in Crucifers. Mol. Cells 16, 136-141.
31. Koes, R., et al. (1995). Targeted gene inactivation in petunia by PCR-based selection of transposon insertion mutants. Proc. Natl. Acad. Sci. USA 92, 8149-8153.
32. Lee, H., Suh, S.-S., Park, E., Cho, E., Ahn, J.H., Kim, S.-G., Lee, J.S., Kwon, Y.M., and Lee, I. (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev. 14, 2366-2376.
33. Lee, I., Bleecker, A., and Amasino, R.M. (1993). Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol. Gen. Genet. 237, 171-176.
34. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., and Yanofsky, M.F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766-770.
35. Ma, H., Yanofsky, M.F., and Meyerowitz, E.M. (1991). AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484-495.
36. Mandel, T., Lutziger, I., and Kuhlemeier, C. (1994). A ubiquitously expressed MADS-box gene from Nicotiana tabacum. Plant Mol. Biol. 25, 319-321.
37. 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.
38. Menzel, G., Apel, K., and Melzer, S. (1996). Identification of two MADS box genes that are expressed in the apical meristem of the long-day plant Sinapis alba in transition to flowering. Plant J. 9, 399-408.
39. Michaels, S.D., and Amasino, R.M. (1999). FLOWERING LOCUS C encodes a novel MADS-domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956.
40. Michaels, S.D., and Amasino, R.M. (2001). Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13, 935-941.
41. Michaels, S.D., Ditta, G., Gustafson-Brown, C., Pelaz, S., Yanofsky, M., and Amasino, R.M. (2003). AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J. 33, 867-874.
42. Mizukami, Y., Huang, H., Tudor, M., Hu, Y., and Ma, H. (1996). Functional domains of the floral regulator AGAMOUS: Characterization of the DNA binding domain and analysis of dominant negative mutations. Plant Cell 8, 831-845.
43. Moon, J., Suh, S.-S., Lee, H., Choi, K.-R., Hong, C.B., Paek, N.-C., Kim, S.-G., and Lee, I. (2003). The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J. 35, 613-623.
44. Mouradov, A., Cremer, F., and Coupland, G. (2002). Control of flowering time: Interacting pathways as a basis for diversity. Plant Cell 14 (suppl.), S111-S130.
45. Ng, M., and Yanofsky, M.F. (2001). Function and evolution of the plant MADS-box gene family. Nat. Rev. Genet. 2, 186-195.
46. Okamoto, S., Krainc, D., Sherman, K., and Lipton, S.A. (2000). Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. Proc. Natl. Acad. Sci. USA 97, 7561-7566.
47. Ornatsky, O.I., Andreucci, J.J., and McDermott, J.C. (1997). A dominant-negative form of transcription factor MEF2 inhibits myogenesis. J. Biol. Chem. 272, 33271-33278.
48. Pařenicová, L., De Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Busscher, J., Cook, H.E., Ingram, R.M., Kater, M.M., Davies, B., Angenent, G.C., and Colombo, L. (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: New openings to the MADS world. Plant Cell 15, 1538-1551.
49. Pasion, S.G., and Forsburg, S. (1999). Nuclear localization of Schizosaccaromyces pombe Mcm2/Cdc19p requires MCM complex assembly. Mol. Biol. Cell 10, 4043-4057.
50. Pnueli, L., Abu-Abeid, M., Zamir, D., Nacken, W., Schwarz-Sommer, Z., and Lifschitz, E. (1991). The MADS box gene family in tomato: Temporal expression during floral development, conserved secondary structures and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J. 1, 255-266.
51. Ratcliffe, O.J., Nadzan, G.C., Reuber, T.L., and Riechmann, J.L. (2001). Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol. 126, 122-132.
52. Ratcliffe, O.J., Kumimoto, R.W., Wong, B.J., and Riechmann, J.L. (2003). Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15, 1159-1169.
53. Ratcliffe, O.J., and Riechmann, J.L. (2002). Arabidopsis transcription factors and the regulation of flowering time: A genomic perspective. Curr. Issues Mol. Biol. 4, 77-91.
54. Riechmann, J.L., and Meyerowitz, E.M. (1997). MADS domain proteins in plant development. Biol. Chem. 378, 1079-1101.
55. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F., and Coupland, G. (2000). Distinct roles of COSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616.
56. Scortecci, K.C., Michaels, S.D., and Amasino, R.M. (2001). Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J. 26, 229-236.
57. Sheldon, C.C., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and Dennis, E.S. (1999). The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445-458.
58. Sheldon, C.C., Conn, A.B., Dennis, E.S., and Peacock, W.J. (2002). Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14, 2527-2537.
59. Sheldon, C.C., Rouse, D.T., Finnegan, E.J., Peacock, W.J., and Dennis, E.S. (2000). The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). Proc. Natl. Acad. Sci. USA 97, 3753-3758.
60. Shore, P., and Sharrocks, A.D. (1995). The MADS-box family of transcription factors. Eur. J. Biochem. 229, 1-13.
61. Simon, R., Igeño, M.I., and Coupland, G. (1996). Activation of floral meristem identity genes in Arabidopsis. Nature 384, 59-62.
62. Simpson, G.G., and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time? Science 296, 285-289.
63. Sink, K.C., ed (1984). Monographs on Theoretical and Applied Genetics 9: Petunia. (Berlin: Springer-Verlag), pp. 211-215.
64. Sommer, H., Beltran, J.P., Huijser, P., Pape, H., and Lonnig, W.-E. (1990). DEFICIENS, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: The protein shows homology to transcription factors. EMBO J. 9, 605-613.
65. Tadege, M., Sheldon, C.C., Gelliwell, C.A., Upadhyaya, N.M., Dennis, E.S., and Peacock, W.J. (2003). Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotech. J. 1, 361-369.
66. 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.
67. Tzeng, T.-Y., and Yang, C.-H. (2001). A MADS box gene from lily (Lilium longiflorum) is sufficient to generate dominant negative mutation by interacting with PISTILLATA (PI) in Arabidopsis thaliana. Plant Cell Physiol. 42, 1156-1168.
68. Vandenbussche, M., Zethof, J., Souer, E., Koes, R., Tornielli, G.B., Pezzotti, M., Ferrario, S., Angenent, G.C., and Gerats, T. (2003). Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant Cell 15, 2680-2693.
69. Verwoerd, T.C., Dekker, B.M.M., and Hoekema, A. (1989). A smallscale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 17, 2362.
70. Yanofsky, M.F., Ma, H., Bowman, I.L., Drews, G., Feldmann, K., and Meyerowitz, E.M. (1990). The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35-39.
71. Yu, H., Xu, Y., Tan, E.L., and Kumar, P.P. (2002). AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc. Natl. Acad. Sci. USA 99, 16336-16341.
72. Zhang, H., and Forde, B.G. (1998). An Arabidopsis MADS box gene that controls nutrient induced changes in root architecture. Science 279, 407-409.