C/D class MADS box genes from two monocots, orchid (oncidium gower ramsey) and lily (lilium longiflorum), exhibit different effects on floral transition and formation in arabidopsis thaliana

Plant and Cell Physiology

Volumn 51, Issue 6, 2010, Pages 1029-1045

  Hsu, Hsing Fun ^a   Hsieh, Wen Ping ^a   Chen, Ming Kun ^a   Chang, Yu Yun ^a   Yang, Chang Hsien ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

AGAMOUS; Arabidopsis thaliana; Lilium longiflorum; MADS box genes; Oncidium Gower Ramsey

Indexed keywords

COMPLEMENTARY DNA; MADS DOMAIN PROTEIN; PLANT RNA; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LILY; METABOLISM; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR GENETICS; ORCHIDACEAE; PHYLOGENY; PLANT GENE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LILIUM; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; ORCHIDACEAE; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; RNA, PLANT; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LILIOPSIDA; LILIUM; LILIUM LONGIFLORUM; ONCIDIUM GOWER RAMSEY; ORCHIDACEAE;

EID: 77953583244     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcq052     Document Type: Article

References (63)

1. Altschul, S.F, Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
2. Angenent, G.C. and Colombo, L. (1996) Molecular control of ovule development. Trends Plant Sci. 1: 228-232.
3. Angenent, G.C., Franken, J., Busscher, M., van Dijken, A., van Went, J.L., Dons. H.J., et al. (1995) A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7: 1569-1582.
4. Benedito, V.A., Visser, P.B., van Tuyl, J.M., Angenent, G.C., de Vries, S.C. and Krens, F.A. (2004) Ectopic expression of llag1, an agamous homologue from lily (Lilium longifl orum Thunb.), causes fl oral homeotic modifi cations in Arabidopsis. J. Exp. Bot. 55: 1391-1399.
5. Bradley, D., Carpenter, R., Sommer, H., Hartley, N. and Coen, E. (1993) Complementary fl oral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85-95.
6. Carpenter, R. and Coen, E.S. (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev. 4: 1483-1493.
7. Chang, Y.-Y., Chiu, Y.-F., Wu, J.-W. and Yang, C.-H. (2009) Four orchid (Oncidium Gower Ramsey) ap1/agl9-like MADS box genes show novel expression patterns and cause different effects on fl oral transition and formation in Arabidopsis thaliana. Plant Cell Physiol. 50: 1425-1438.
8. Chang, Y.-Y., Kao, N.-H., Li, J.-Y., Hsu, W.-H., Liang, Y.-L., Wu, J.-W., et al. (2010) Characterization of the possible roles for B functional MADS box genes in regulation of perianth formation in orchid (Oncidium Gower Ramsey). Plant Physiol. In press. doi: 10.1104/pp.109.147116.
9. Chen, M.-K., Lin, I.-C. and Yang, C.-H. (2008) Functional analysis of three lily (Lilium longifl orum) apetala1-like MADS box genes in regulating fl oral transition and formation. Plant Cell Physiol. 49: 704-717.
10. 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.
11. Coen, E.S. and Meyerowitz, E.M. (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
12. Colombo, L., Franken, J., Koetje, E., van Went, J., Dons, H.J., Angenent, G.C., et al. (1995) The Petunia MADS-box gene fbp11 determines ovule identity. Plant Cell 7: 1859-1868.
13. Colombo, L., Franken, J., Van der Krol, A.R., Wittich, P.E., Dons, H.J. and Angenent, G.C. (1997a) Downregulation of ovule-specific MADS box genes from Petunia results in maternally controlled defects in seed development. Plant Cell 9: 703-715.
14. Colombo, L., van Tunen, A.J., Dons, H.J.M. and Angenent, G.C. (1997b) Molecular control of fl ower development in Petunia hybrida. Adv. Bot. Res. 26: 229-250.
15. Egea-Cortines, M., Saedler, H. and Sommer, H. (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of fl oral architecture in Antirrhinum majus. EMBO J. 18: 5370-5379.
16. Flanagan, C.A., Hu, Y. and Ma, H. (1996) Specific expression of the agl1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J. 10: 343-353.
17. Gietz, D., St Jean, A., Woods, R.A. and Schiesti, R.H. (1992) Improved method for high effi ciency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
18. Hsu, H.-F., Huang, C.-H., Chou, L.-T. and Yang, C.-H. (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) agl6-like gene promotes fl owering by activating fl owering time genes in Arabidopsis thaliana. Plant Cell Physiol. 44: 783-794.
19. Hsu, H.-F. and Yang, C.-H. (2002) An orchid (Oncidium Gower Ramsey) ap3-like MADS gene regulates fl oral formation and initiation. Plant Cell Physiol. 43: 1198-1209.
20. Huang, H., Mizukami, Y., Hu, Y. and Ma, H. (1993) Isolation and characterization of the binding sequences for the product of the Arabidopsis fl oral homeotic gene agamous. Nucleic Acids Res. 21: 4769-4776.
21. Kang, H.G., Noh, Y.S., Chung, Y.Y., Costa, M.A., An, K. and An, G. (1995) Phenotypic alterations of petal and sepal by ectopic expression of a rice MADS box gene in tobacco. Plant Mol. Biol. 29: 1-10.
22. Kater, M.M., Colombo, L., Franken, J., Busscher, M., Masiero, S., Van Lookeren Campagne, M.M., et al. (1998) Multiple agamous homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10: 171-182.
23. Kempin, S.A., Mandel, M.A. and Yanofsky, M.F. (1993) Conversion of perianth into reproductive organs by ectopic expression of the tobacco fl oral homeotic gene nag1. Plant Physiol. 103: 1041-1046.
24. Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111-120.
25. Kramer, E.M., Jaramillo, M.A. and Di Stilio, V.S. (2004) Patterns of gene duplication and functional evolution during the diversifi cation of the agamous subfamily of MADS box genes in angiosperms. Genetics 166: 1011-1023.
26. 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.
27. Liljegren, S.J., Ferrandiz, C., Alvarez-Buylla, E.R., Pelaz, S. and Yanofsky, M.F. (1998) Arabidopsis MADS-box genes involved in fruit dehiscence. Flowering Newslett. 25: 9-19.
28. Litt, A. and Kramer, E.M. (2010) The ABC model and the diversification of fl oral organ identity. Semin. Cell. Dev. Biol. 21: 129-137.
29. Lopez-Dee, Z.P., Wittich, P., Enrico Pe, M., Rigola, D., Del Buono, I., Gorla, M.S., et al. (1999) Osmads13, a novel rice MADS-box gene expressed during ovule development. Dev. Genet. 25: 237-244.
30. Ma, H., Yanofsky, M.F. and Meyerowitz, E.M. (1991) Agl1-agl6, an Arabidopsis gene family with similarity to fl oral homeotic and transcription factor genes. Genes Dev. 5: 484-495.
31. Mena, M., Ambrose, B.A., Meeley, R.B., Briggs, S.P., Yanofsky, M.F. and Schmidt, R.J. (1996) Diversification of C-function activity in maize flower development. Science 274: 1537-1540.
32. Mena, M., Mandel, M.A., Lerner, D.R., Yanofsky, M.F. and Schmidt, R.J. (1995) A characterization of the MADS-box gene family in maize. Plant J. 8: 845-854.
33. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor Laboratory Press, Cold Spring
34. Harbor, NY. Miyazaki, S., Sugawara, H., Ikeo, K., Gojobori, T. and Tateno, Y. (2004) DDBJ in the stream of various biological data. Nucleic Acids Res. 32: D31-D34.
35. Mizukami, Y., Huang, H., Tudor, M., Hu, Y. and Ma, H. (1996) Functional domains of the fl oral regulator AGAMOUS: characterization of the DNA binding domain and analysis of dominant negative mutations. Plant Cell 8: 831-845.
36. Mizukami, Y. and Ma, H. (1992) Ectopic expression of the fl oral homeotic gene agamous in transgenic Arabidopsis plants alters fl oral organ identity. Cell 71: 119-131.
37. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant 15: 473-479.
38. Pinyopich, A., Ditta, G.S., Savidge, B., Liljegren, S.J., Baumann, E., Wisman, E., et al. (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424: 85-88. (Pubitemid 36834846)
39. Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F. and Lifschitz, E. (1994) Isolation of the tomato agamous gene tag1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
40. Purugganan, M.D., Rounsley, S.D., Schmidt, R.J. and Yanofsky, M.F. (1995) Molecular evolution of fl ower development: diversifi cation of the plant MADS-box regulatory gene family. Genetics 140: 345-356.
41. Rounsley, S.D., Ditta, G.S. and Yanofsky, M.F. (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7: 1259-1269.
42. Rutledge, R., Regan, S., Nicolas, O., Fobert, P., Cote, C., Bosnich, W., et al. (1998) Characterization of an agamous homologue from the conifer black spruce (Picea mariana) that produces fl oral homeotic conversions when expressed in Arabidopsis. Plant J. 15: 625-634.
43. Savidge, B., Rounsley, S.D. and Yanofsky, M.F. (1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the fl oral organ identity genes. Plant Cell 7: 721-733.
44. Schmidt, R.J., Veit, B., Mandel, M.A., Mena, M., Hake, S. and Yanofsky, M.F. (1993) Identification and molecular characterization of zag1, the maize homolog of the Arabidopsis fl oral homeotic gene agamous. Plant Cell 5: 729-737.
45. Shiraishi, H., Okada, K. and Shimura, Y. (1993) Nucleotide sequences recognized by the agamous MADS domain of Arabidopsis thaliana in vitro. Plant J. 4: 385-398.
46. Song, I.J., Nakamura, T., Fukuda, T., Yokoyama, J., Ito, T., Ichikawa, H., et al. (2006) Spatiotemporal expression of duplicate agamous orthologues during fl oral development in Phalaenopsis. Dev. Genes Evol. 216: 301-313.
47. Theissen, G. (2001) Development of fl oral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4: 75-85.
48. Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Munster, T., et al. (2000) A short history of MADS-box genes in plants. Plant Mol. Biol. 42: 115-149.
49. Theissen, G. and Saedler, H. (1995) MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. Curr. Opin. Genet. Dev. 5: 628-639.
50. Theissen, G. and Saedler, H. (2001) Plant biology. Floral quartets. Nature 409: 469-471.
51. Theissen, G., Strater, T., Fischer, A. and Saedler, H. (1995) Structural characterization, chromosomal localization and phylogenetic evaluation of two pairs of agamous-like MADS-box genes from maize. Gene 156: 155-166.
52. 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-specifi c gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
53. Tilly, J.J., Allen, D.W. and Jack, T. (1998) The CArG boxes inthe promoter of the Arabidopsis fl oral organ identity gene apetala3 mediate diverse regulatory effects. Development 125: 1647-1657.
54. Tsuchimoto, S., van der Krol, A.R. and Chua, N.H. (1993) Ectopic expression of pmads3 in transgenic petunia phenocopies the petunia blind mutant. Plant Cell 5: 843-853.
55. Tzeng, T.-Y., Chen, H.-Y. and Yang, C.-H. (2002) Ectopic expression of carpel-specifi c MADS box genes from lily and lisianthus causes similar homeotic conversion of sepal and petal in Arabidopsis. Plant Physiol. 130: 1827-1836.
56. Tzeng, T.-Y., Hsiao, C.-C., Chi, P.-J. and Yang, C.-H. (2003) Two lily sepallata-like genes cause different effects on fl oral formation and fl oral transition in Arabidopsis. Plant Physiol. 133: 1091-1101.
57. Tzeng, T.-Y., Liu, H.-C. and Yang, C.-H. (2004) The C-terminal sequence of Lmads1 is essential for the formation of homodimers for B function proteins. J. Biol. Chem. 279: 10747-10755.
58. Tzeng, T.-Y. and Yang, C.-H. (2001) A MADS box gene from lily (Lilium longifl orum) is suffi cient to generate dominant negative mutation by interacting with PISTILLATA (PI) in Arabidopsis thaliana. Plant Cell Physiol. 42: 1156-1168.
59. Winter, K.U., Becker, A., Munster, T., Kim, J.T., Saedler, H. and Theissen, G. (1999) MADS-box genes reveal that gnetophytes are more closely related to conifers than to fl owering plants. Proc. Natl Acad. Sci. USA 96: 7342-7347.
60. Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A. and Meyerowitz, E.M. (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346: 35-39.
61. Yu, D., Kotilainen, M., Pollanen, E., Mehto, M., Elomaa, P., Helariutta, Y., et al. (1999) Organ identity genes and modified patterns of fl ower development in Gerbera hybrida (Asteraceae). Plant J. 17: 51-62.
62. Yun, P.-Y., Ito, T., Kim, S.-Y., Kanno, A. and Kameya, T. (2004a) The AVAG1 gene is involved in the development of the reproductive organs in the ornamental asparagus, Asparagus virgatus. Sex. Plant Reprod. 17: 1-8.
63. Yun, P.-Y., Kim, S.-Y., Ochiai, T., Fukuda, T., Ito, T., Kanno, A., et al. (2004b) AVAG2 is a putative D-class gene from an ornamental asparagus. Sex. Plant Reprod. 17: 107-116.