Abstract
MADS-box genes in plants are putative transcription factors involved in regulating numerous developmental processes, such as meristem and organ identity in inflorescences and in flowers. Recent reports indicate that they are involved in other processes than flower development such as the establishment of developing embryos, seed coat and ultimately in root and fruit development. We have identified seven tomato MADS-box genes that are highly expressed during the first steps of tomato fruit development. According to comparisons of their deduced amino acid sequences, they were classified into two groups: (1) already identified tomato MADS-box genes previously defined as flower identity genes (TAG1, TDR4 and TDR6) and (2) new tomato MADS-box genes (TAGL1, TAGL2, TAGL11 and TAGL12). With the exception of TAGL12, which is expressed near uniformly in every tissue, the other genes show an induction during the tomato fruit development phase I (anthesis) and phase II, when active cell division occurs. In situ hybridization analyses show a specific expression pattern for each gene within the fruit and embryo sac tissues suggesting an important role in the establishment of tissue identity. Yeast two-hybrid analyses indicate that some of these proteins could potentially form dimers suggesting they could act together to accomplish their proposed role.
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Adachi, J. and Hasegawa, M. 1996. MOLPHY Program for Molecular Phylogenetics Version 2.3. Institute of Mathematical Statistics, Tokyo.
Ampomah-Dwamena, C., Morris, B., Sutherland, P., Veit, B. and Yao, J. 2002. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol. 130: 605-617.
Bowman, J. (Ed.). 1994. Arabidopsis: An Atlas of Morphology and Development. Springer-Verlag, New York.
Cho, S., Jang, S., Chae, S., Chung, K., Moon, Y., An, G. and Jang, S. 1999. Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol. Biol. 40: 419-429.
Coen, E. and Meyerowitz, E. 1991. The war of the whorls: genetic interactions controlling flower development. Nature353: 31-37.
Colombo, L., Franken, J., Koetje, E., van Went J., Dons, H., Angenent, G. and van Tunen A. 1995. The petunia MADS box gene FBP11 determinates ovule identity. Plant Cell 7: 1859-1868.
Colombo, L., Franken, J., van der Krol, A., Witlich, P., Doris, H. and Angenent, G. 1997. Downregulation of ovule-specific MADS box genes from Petunia results in maternally controlled defects in seed development. Plant Cell 9: 703-715.
Davies, B., Egea-Cortines, M., Andrade Silva, E., Saedler, H. and Sommer, H. 1996. Multiple interactions amongst floral homeotic MADS box proteins. EMBO J. 15: 4330-4343.
Egea-Cortines, M. and Davies, B. 2000. Beyond the ABCs: ternary complex formation in the control of floral organ identity. Trends Plant Sci. 5: 471-478.
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.
Ferrándiz, C., Pelaz, S. and Yanofsky, M. 1999. Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem. 68: 321-354.
Ferrándiz, C., Liljegren, S. and Yanofsky, M. 2000. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436-438.
Fields, S. and Sternglanz, R. 1994. The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 10: 286-292.
Flanagan, C., 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.
Franzmann, L., Patton, D. and Meinke, D. 1989. In vitro morphogenesis of arrested embryos form lethal mutations of Arabidopsis thaliana. Theor. Appl. Genet. 77: 609-616.
Gietz, D., St Jean, A., Woods, A. and Schiesti, R. 1992. Improved method for high efficiency transformation of intect yeast cells. Nucl. Acids Res. 20: 1425.
Gill, G., Pascal, E., Tseng, Z. and Tjian, R. 1994. A glutaminerich hydrophobic patch in transcription factor Sp1 contacts the dTAFII110 component of the Drosophila TFIID complex and mediates transcriptional activation. Proc. Natl. Acad. Sci. USA 91: 192-196.
Gillaspy, G., Ben-David, H. and Gruissem, W. 1993. Fruits: a developmental perspective. Plant Cell 5: 1439-1451.
Gu, K., Ferrándiz, C., Yanofsky, M. and Martinsen, R. 1998. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509-1517.
Heck, G., Perry, S., Nichols, K. and Fernandez, D. 1995. AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7: 1271-1282.
Homma, T. and Goto, K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 826-829.
Immink, R., Hannapel, D., Ferrario, S., Busscher, M., Franken, J., Lookeren Campagne, M. and Angenent G. 1999. A petunia MADS box gene involved in the transition from vegetative to reproductive development. Development 126: 5117-5126.
Jack, T. 2001. Relearning our ABCs: new twists on an old model. Trends Plant Sci. 6: 310-316.
Jones, D., Taylor, W., and Thornton, J. 1992. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8: 275-282.
Kang, S. and Hannapel, D. 1995. Nucleotide sequences of novel potato (Solanum tuberosum L.) MADS-box cDNAs and their expression in vegetative organs. Gene 12: 329-330.
Kishino, H. and Hasegawa, M. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29: 170-179.
Kramer, E., Dorit, R. and Irish, V. 1998. Molecular evolution of genes controlling petal and stamen development: duplication and divergence within the APETALA3 and PISTILLATA MADS-box gene lineages. Genetics 149: 765-783.
Lamb, P. and McKnight, S. 1991. Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization. Trends Biochem. Sci. 16: 417-422.
Liljegren, S., Ditta, G., Eshed, Y., Savidge, B., Bowman, J. and Yanofsky, M. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
Lozano, R., Angosto, T., Gómez, P., Payán, C., Capel, J., Huijser, P., Salinas, J. and Martinez-Zapater, M. 1998. Tomato flower abnormalities induced by low temperature are associated with changes of expression of MADS-box genes. Plant Physiol. 117: 91-100.
Mandel, MA. and Yanofsky, M. 1995. The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell 7: 1763-1771.
Mao, L., Begum, D., Chuang, H., Budiman, M., Szymkowiak, E., Irish, E. and Wing, R. 2000. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406: 910-913.
Mazzucato, A., Taddei, A. and Soressi, G. 1998. The parthenocarpic fruit (pat) mutant of tomato (Lycopersicon esculentum Mill.) sets seedless fruits and has aberrant anther and ovule development. Development 125: 107-114.
Meyerowitz, E. 1987. In situ hybridization to RNA in plant tissue. Plant Mol. Biol. Rep. 5: 242-250.
Miller, J. 1992. A Short Course of Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor Laboratory Press, Plainview, NY.
Moon, Y., Jung, J., Kang, H. and An, G. 1999. Identification of a rice APETALA3 homologue by yeast two-hybrid screening. Plant Mol. Biol. 40: 167-177.
Müller, B., Saedler, H. and Zachgo, S. 2001. The MADS-box gene DEFH28 from Antirrhinum is involved in the regulation of floral meristem identity and fruit development. Plant J. 28: 169-179.
Okada, K. and Shimura, Y. 1994. Genetic analyses of signaling in flower development using Arabidopsis. Plant Mol. Biol. 26: 1357-1377.
Pnueli, L., Abu-Abeid, Zamir, D. Necken, W., Schwarz-Sommer, Z. and Lifschitz, E. 1991. The MADS box gene family in tomato: temporal expression during floral development, conserved secondary structure and homology with homeotic genes from Antirrhinum and Arabidopsis. Plant J. 112: 255-266.
Pnueli, L., Hareven, D., Rounsley, S., Yanofsky, M. and Lifschitz, E. 1994a. Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
Pnueli, L. Hareven, D. Broday, L. Hurwitz, C. and Lifschitz, E. 1994b. The TM5MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6: 175-186.
Purugganan, M. 1997. The MADS box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J. Mol. Evol. 45: 392-396.
Rounsley, S., Ditta, G. and Yanofsky, M. 1995. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7: 1259-1269.
Sambrook, J. and Russell, D. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Savidge, B., Rounsley, S., Schmidt, R. and Yanofsky, M. 1995. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7: 721-733.
Sommer, H., Beltran, J., Huijser, P., Papa, H., Lonnig, W., 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.
Theissen, G. and Saedler, H. 1995. MADS-box genes in plant ontogeny and phylogeny: Haeckel's 'biogenetic law' revisited. Curr. Opin. Genet. Dev. 5: 628-638.
Theissen, G. and Saedler, H. 2001. Plant biology: floral quartets. Nature 409: 469-471.
Theissen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J., Münster, T., Winter, K. and Saedler, H. 2000. A short history of MADSbox genes in plants. Plant Mol. Biol. 42: 115-149.
Triezenberg, S. 1995. Structure and function of transcriptional activation domains. Curr. Opin. Genet. Dev. 5: 190-196.
Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., Schuch, W. and Giovannoni, J. 2002. A MADSbox gene necessary for fruit ripening at the tomato ripeninginhibitor (Rin) locus. Science 296: 343-346.
Weigel, D. and Meyerowitz, E. 1994. The ABCs of floral homeotic genes. Cell 78: 203-209.
West, A. and Sharrocks, A. 1999. MADS-box transcription factors adopt alternative mechanisms for bending DNA. J. Mol. Biol. 288: 1311-1323.
Yanofsky, M., Ma, H., Bowman, J., Drews, G., Feldmann, K. and Meyerowitz, E. 1990. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346: 35-39.
Yao, T., Dong., Y. and Morris, B. 1999. Seven MADS-box genes in apple are expressed in different parts of the fruit. J. Am. Soc. Hort. 124: 8-13.
Yao, J., Dong, Y. and Morris, B. 2001. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc. Natl. Acad. Sci. USA 98: 1306-1311.
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Busi, M., Bustamante, C., D'Angelo, C. et al. MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52, 801–815 (2003). https://doi.org/10.1023/A:1025001402838
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DOI: https://doi.org/10.1023/A:1025001402838