Advertisement

Petunia pp 225-245 | Cite as

Combinatorial Action of Petunia MADS Box Genes and Their Protein Products

  • Gerco C. Angenent
  • Richard G.H. Immink

Abstract

During the last two decades enormous progress has been made in our understanding of the genes that control the identity of floral organs. These genes appear to be members of a large family of MADS box transcription factors that are well conserved across angiosperms. Research using Petunia as a model plant has contributed substantially to the discovery of novel MADS box gene functions and to our understanding of how these MADS box transcription factors act. The proteins function together in dimeric and possibly larger protein complexes to control the expression of target genes. This combinatorial action forms the basis of the ABC model for floral organ development and underlies many other developmental processes.

Keywords

Floral Organ Floral Meristem Floral Whorl Carpel Primordia Homeotic Conversion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Akam, M. (1983) Decoding the Drosophila complexes. Trends Biochem. Sci. 8, 173–177.CrossRefGoogle Scholar
  2. Alvarez Buylla, E.R., Pelaz, S., Liljegren, S.J., Gold, S.E., Burgeff, C., Ditta, G.S., de Pouplana, L.R., Martinez Castilla, L. and Yanofsky, M.F. (2000) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl. Acad. Sci., USA 97, 5328–5333.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. Angenent, G.C., Franken, J., Busscher, M., Colombo, L. and van Tunen, A.J. (1993) Petal and stamen formation in petunia is regulated by the homeotic gene fbp1. Plant J. 4, 101–112.CrossRefPubMedGoogle Scholar
  5. Angenent, G.C., Franken, J., Busscher, M., Weiss, D. and van Tunen, A.J. (1994) Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J. 5, 33–44.CrossRefPubMedGoogle Scholar
  6. Angenent, G.C., Busscher, M., Franken, J., Dons, H.J.M. and van Tunen, A.J. (1995a) Functional interaction between the homeotic genes fbp1 and pMADS1 during Petunia floral organogenesis. Plant Cell 7, 507–516.Google Scholar
  7. Angenent, G.C., Franken, J., Busscher, M., van Dijken, A., van Went, J.L., Dons, H.J.M. and van Tunen, A.J. (1995b) A novel class of MADS box genes is involved in ovule development in petunia. Plant Cell 7, 1569–1582.Google Scholar
  8. Angenent, G.C. and Colombo, L. (1996) Molecular control of ovule development. Trends Plant Sci. 1, 228–232.Google Scholar
  9. Aronheim, A., Zundi, E., Hennemann, H., Elledge, S.J. and Karin, M. (1997) Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Mol. Cell. Biol. 17, 3094–3102.PubMedGoogle Scholar
  10. Becker, A., Kaufmann, K., Freialdenhoven, A., Vincent, C., Li, M.A., Saedler, H. and Theissen, G. (2002) A novel MADS-box gene subfamily with a sister-group relationship to-class B floral homeotic genes. Molec. Genet. Genom. 266, 942–950.CrossRefGoogle Scholar
  11. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M. and Simon, R. (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617–619.CrossRefPubMedGoogle Scholar
  12. Cartolano, M., Castillo, R., Efremova, N., Kuckenberg, M., Zethof, J., Gerats, T., Schwarz Sommer, Z. and Vandenbussche, M. (2007) A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nature Genetics 39, 901–905.CrossRefPubMedGoogle Scholar
  13. Coen, E.S. and Meyerowitz, E.M. (1991) The war of the whorls: Genetic interactions controlling flower development. Nature 353, 31–37.CrossRefPubMedGoogle Scholar
  14. Colombo, L., Franken, J., Koetje, E., Van-Went, J., Dons, H.J.M., Angenent, G.C. and van Tunen, A.J. (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859–1868.CrossRefPubMedGoogle Scholar
  15. Colombo, L., Franken, J., van der Krol, A.R., Wittich, P.E., Dons, H.J.M. and Angenent, G.C. (1997) Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell 9, 703–715.CrossRefPubMedGoogle Scholar
  16. Cui, H.C., Levesque, M.P., Vernoux, T., Jung, J.W., Paquette, A.J., Gallagher, K.L., Wang, J.Y., Blilou, I., Scheres, B. and Benfey, P.N. (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425.CrossRefPubMedGoogle Scholar
  17. Davies, B., Egea Cortines, M., Silva, E.D., Saedler, H. and Sommer, H. (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 15, 4330–4343.PubMedGoogle Scholar
  18. Davies, B., Motte, P., Keck, E., Saedler, H., Sommer, H. and Schwarz-Sommer, Z. (1999) PLENA and FARINELLI: Redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J. 18, 4023–4034.CrossRefPubMedGoogle Scholar
  19. De Bodt, S., Raes, J., Florquin, K., Rombauts, S., Rouze, P., Theissen, G. and Van de Peer, Y. (2003) Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J. Molec. Evol. 56, 573–586.CrossRefPubMedGoogle Scholar
  20. De Folter, S., Immink, R.G.H., Kieffer, M., Parenicova, L., Henz, S.-R., Weigel, D., Busscher, M., Kooiker, M., Colombo, L., Kater, M.M., Davies, B. and Angenent, G.C. (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17, 1424–1433.CrossRefPubMedGoogle Scholar
  21. De Folter, S. and Angenent, G.C. (2006) Trans meets cis in MADS science. Trends Plant Sci. 11, 224–231CrossRefPubMedGoogle Scholar
  22. De Folter, S., Shchennikova, A.V., Franken, J., Busscher, M., Baskar, R., Grossniklaus, U., Angenent, G.C. and Immink, R.G.H. (2006) A B-sister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. Plant J. l 47, 934–947.CrossRefGoogle Scholar
  23. Ditta, G., Pinyopich, A., Robles, P., Pelaz, S. and Yanofsky, M.F. (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr. Biol. 14, 1935–1940.CrossRefPubMedGoogle Scholar
  24. 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 floral architecture in Antirrhinum majus. EMBO J. 18, 5370–5379.CrossRefPubMedGoogle Scholar
  25. Ferrario, S., Immink, R.G.H., Shchennikova, A., Busscher Lange, J. and Angenent, G.C. (2003) The MADS box gene FBP2 is required for SEPALLATA function in petunia. Plant Cell 15, 914–925.CrossRefPubMedGoogle Scholar
  26. Ferrario, S., Busscher, J., Franken, J., Gerats, T., Vandenbussche, M., Angenent, G.C. and Immink, R.G.H. (2004) 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 16, 1490–1505.CrossRefPubMedGoogle Scholar
  27. Ferrario, S., Shchennikova, A.V., Franken, J., Immink, R.G.H. and Angenent, G.C. (2006) Control of floral meristem determinacy in petunia by MADS-box transcription factors. Plant Physiol. 140, 890–898.CrossRefPubMedGoogle Scholar
  28. Fields, S. and Song, O.-K. (1989) A novel genetic system to detect protein–protein interactions. Nature 340, 245–246.CrossRefPubMedGoogle Scholar
  29. Fornara, F., Marziani, G., Mizzi, L., Kater, M. and Colombo, L. (2003) MADS-box genes controlling flower development in rice. Plant Biol. 5, 16–22.CrossRefGoogle Scholar
  30. Fornara, F., Parenicova, L., Falasca, G., Pelucchi, N., Masiero, S., Ciannamea, S., Lopez Dee, Z., Altamura, M.M., Colombo, L. and Kater, M.M. (2004) Functional characterization of OsMADS18, a member of the AP1/SQUA subfamily of MADS box genes. Plant Physiol. 135, 2207–2219.CrossRefPubMedGoogle Scholar
  31. Gehring, W.J. and Hiromi, Y. (1986) Homeotic genes and the homeobox. Ann. Rev. Genet. 20, 147–173.CrossRefPubMedGoogle Scholar
  32. Gerats, A.G.M., Kaye, C., Collins, C. and Malmberg, R.L. (1988) Polyamine levels in Petunia genotypes with normal and abnormal floral morphologies. Plant Physiol. 86, 390–393.CrossRefPubMedGoogle Scholar
  33. 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.PubMedGoogle Scholar
  34. Immink, R.G.H. (2002) Characterisation of Plant MADS Box Transcription Factor Protein-Protein Interactions. Ph.D. Thesis, Wageningen University, Wageningen.Google Scholar
  35. Immink, R.G.H. and Angenent, G.C. (2002) Transcription factors do it together: The hows and whys of studying protein-protein interactions. Trends Plant Sci. 7, 531–534.CrossRefPubMedGoogle Scholar
  36. Immink, R.G.H., Gadella, T.W.J., 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.CrossRefPubMedGoogle Scholar
  37. 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. Molec. Genet. Genom. 268, 598–606.Google Scholar
  38. Jofuku, K.D., de Boer, B.G.W., van Montagu, M. and Okamuro, J.K. (1994) Control of Arabidopsis flower and seed development by the homeotic gene Apetala2. Plant Cell 6, 1211–1255.CrossRefPubMedGoogle Scholar
  39. Kapoor, M., Tsuda, S., Tanaka, Y., Mayama, T., Okuyama, Y., Tsuchimoto, S. and Takatsuji, H. (2002) Role of petunia pMADS3 in determination of floral organ and meristem identity, as revealed by its loss of function. Plant J. 32, 115–127.CrossRefPubMedGoogle Scholar
  40. Kater, M.M., Colombo, L., Franken, J., Busscher, M., Masiero, S., Campagne, M.M.V. and Angenent, G.C. (1998) Multiple AGAMOUS homologs from cucumber and petunia differ in their ability to induce reproductive organ fate. Plant Cell 10, 171–182.CrossRefPubMedGoogle Scholar
  41. Kotilainen, M., Elomaa, P., Uimari, A., Albert, V.A., Yu, D. and Teeri, T.H. (2000) GRCD1, an AGL2-like MADS box gene, participates in the C function during stamen development in Gerbera hybrida. Plant Cell 12, 1893–1902.CrossRefPubMedGoogle Scholar
  42. Krizek, B.A. and Meyerowitz, E.M. (1996) Mapping the protein regions responsible for the functional specificities of the Arabidopsis MADS domain organ-identity proteins. Proc. Natl. Acad. Sci., USA 93, 4063–4070.CrossRefPubMedGoogle Scholar
  43. Lee, S., Jeon, J.S., An, K., Moon, Y.H., Lee, S., Chung, Y.Y. and An, G. (2003) Alteration of floral organ identity in rice through ectopic expression of OsMADS16. Planta 217, 904–911.CrossRefPubMedGoogle Scholar
  44. Lim, J., Moon, Y.H., An, G. and Jang, S.K. (2000) Two rice MADS domain proteins interact with OsMADS1. Plant Molec. Biol. 44, 513–527.CrossRefGoogle Scholar
  45. Maes, T., van der Steene, N., Zethof, J., Karimi, M., D'Hauw, M., Mares, G., van Montagu, M. and Gerats, T. (2001) Petunia Ap2-like genes and their role in flower and seed development. Plant Cell 13, 229–244.CrossRefPubMedGoogle Scholar
  46. Mandel, M.A., Gustafson-Brown, C., Savidge, B. and Yanofsky, M.F. (1992) Molecular characterizaiton of the Arabidopsis floral homeotic gene Apetala1. Nature 360, 273–277.CrossRefPubMedGoogle Scholar
  47. Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., Jurgens, G. and Laux, T. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805–815.CrossRefPubMedGoogle Scholar
  48. Moon, Y., Jung, J., Kang, H. and An, G. (1999a) Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Molec. Biol. 40, 167–177.Google Scholar
  49. Moon, Y., Kang, H., Jung, J., Jeon, J., Sung, S. and An, G. (1999b) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol. 120, 1193–1203.Google Scholar
  50. Nam, J., Kim, J., Lee, S., An, G., Ma, H. and Nei, M. (2004) Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc. Natl. Acad. Sci., USA 101, 1910–1915.CrossRefPubMedGoogle Scholar
  51. Nesi, N., Debeaujon, I., Jond, C., Stewart, A.-J., Jenkins, G.-I., Caboche, M. and Lepiniec, L. (2002) The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14, 2463–2479.CrossRefPubMedGoogle Scholar
  52. Norman, C., Runswick, M., Pollock, R. and Treisman, R. (1988) Isolation and properties of complementary DNA clones encoding SRF a transcription factor that binds to the C-Fos serum response element. Cell 55, 989–1003.CrossRefPubMedGoogle Scholar
  53. Parenicova, 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.CrossRefPubMedGoogle Scholar
  54. Passmore, S., Maine, G.T., Christ, R.E.C. and Tye, B.K. (1988) Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of Mat-Alpha cells. J. Molec. Biol. 204, 593–606.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. Prasher, D.C., Eckenrode, V.K., Ward, W.W., Prendergast, F.G. and Cormier, M.J. (1992) Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229–233.CrossRefPubMedGoogle Scholar
  57. Riechmann, J.L., Krizek, B.A. and Meyerowitz, E.M. (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Proc. Natl. Acad. Sci., USA 93, 4793–4798.CrossRefPubMedGoogle Scholar
  58. Rijpkema, A.S., Royaert, S., Zethof, J., van der Weerden, G., Gerats, T. and Vandenbussche, M. (2006) Analysis of the Petunia TM6 MADS box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18, 1819–1832.CrossRefPubMedGoogle Scholar
  59. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jurgens, G. and Laux, T. (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644.CrossRefPubMedGoogle Scholar
  60. Shchennikova, A.V., Shulga, O.A., Immink, R., Skryabin, K.G. and Angenent, G.C. (2004) Identification and characterization of four chrysanthemum MADS-box genes, belonging to the APETALA1/FRUITFULL and SEPALLATA3 subfamilies. Plant Physiol. 134, 1632–1641.CrossRefPubMedGoogle Scholar
  61. Sommer, H., Beltran, J.P., Huijser, P., Pape, H., Lonnig, W.E., Saedler, H. and Schwarz Sommer, Z. (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.PubMedGoogle Scholar
  62. Souer, E., van der Krol, A., Kloos, D., Spelt, C., Bliek, M., Mol, J. and Koes, R. (1998) Genetic control of branching pattern and floral identity during Petunia inflorescence development. Devel. 125, 733–742.Google Scholar
  63. Stuurman, J., Jaggi, F. and Kuhlemeier, C. (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Devel. 16, 2213–2218.CrossRefPubMedGoogle Scholar
  64. Theissen, G. and Saedler, H. (2001) Plant biology: Floral quartets. Nature 409, 469–471.CrossRefPubMedGoogle Scholar
  65. Tonaco-Nougalli, I.A.N., Borst, J.W., de Vries, S.C., Angenent, G.C. and Immink, R.G.H. (2006) In vivo imaging of MADS-box transcription factor interactions. J. Exp. Bot. 57, 33–42CrossRefGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. Uimari, A., Kotilainen, M., Elomaa, P., Yu, D., Albert, V.A. and Teeri, T.H. (2004) Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene. Proc. Natl. Acad. Sci., USA 101, 15817–15822.Google Scholar
  68. Vallade, J., Maizonnier, D. and Cornu, A. (1987) Floral morphogenesis in petunia. I. Analysis of a mutant with a staminate corolla. Can. J. Bot. 65, 761–764.CrossRefGoogle Scholar
  69. van Der Krol, A.R., Brunelle, A., Tsuchimoto, S. and Chua, N.H. (1993) Functional analysis of petunia floral homeotic MADS box gene pMADS1. Genes Devel. 7, 1214–1228.CrossRefPubMedGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. Vandenbussche, M., Zethof, J., Royaert, S., Weterings, K. and Gerats, T. (2004) The duplicated B-class heterodimer model: Whorl-specific effects and complex genetic interactions in Petunia hybrida flower development. Plant Cell 16, 741–754.CrossRefPubMedGoogle Scholar
  72. West, A.G., Causier, B.E., Davies, B. and Sharrocks, A.D. (1998) DNA binding and dimerisation determinants of Antirrhinum majus MADS-box transcription factors. Nucl. Acids Res. 26, 5277–5287.CrossRefPubMedGoogle Scholar
  73. Wittich, P.E., de Heer, R.F., Cheng, X.F., Kieft, H., Colombo, L., Angenent, G.C. and van Lammeren, A.A.M. (1999) Immunolocalization of the petunia Foral Binding Proteins 7 and 11 during seed development in wild-type and expression mutants of Petunia hybrida. Protoplasma 208, 224–229.CrossRefGoogle Scholar
  74. Yang, Y.Z., Fanning, L. and Jack, T. (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J. 33, 47–59.CrossRefPubMedGoogle Scholar
  75. Yang, Y.Z. and Jack, T. (2004) Defining subdomains of the K domain important for protein-protein interactions of plant MADS proteins. Plant Molec. Biol. 55, 45–59.CrossRefGoogle Scholar
  76. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Gerco C. Angenent
    • 1
  • Richard G.H. Immink
    • 1
  1. 1.Plant Research InternationalNederland

Personalised recommendations