Skip to main content

MADS-box genes expressed during tomato seed and fruit development

Plant Molecular Biology volume 52, pages 801–815 (2003)Cite this article

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Adachi, J. and Hasegawa, M. 1996. MOLPHY Program for Molecular Phylogenetics Version 2.3. Institute of Mathematical Statistics, Tokyo.

    Google Scholar 

  • 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.

    Google Scholar 

  • Bowman, J. (Ed.). 1994. Arabidopsis: An Atlas of Morphology and Development. Springer-Verlag, New York.

    Google Scholar 

  • 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.

    Google Scholar 

  • Coen, E. and Meyerowitz, E. 1991. The war of the whorls: genetic interactions controlling flower development. Nature353: 31-37.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Ferrándiz, C., Pelaz, S. and Yanofsky, M. 1999. Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem. 68: 321-354.

    Google Scholar 

  • Ferrándiz, C., Liljegren, S. and Yanofsky, M. 2000. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436-438.

    Google Scholar 

  • Fields, S. and Sternglanz, R. 1994. The two-hybrid system: an assay for protein-protein interactions. Trends Genet. 10: 286-292.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Gillaspy, G., Ben-David, H. and Gruissem, W. 1993. Fruits: a developmental perspective. Plant Cell 5: 1439-1451.

    Google Scholar 

  • 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.

    Google Scholar 

  • Heck, G., Perry, S., Nichols, K. and Fernandez, D. 1995. AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7: 1271-1282.

    Google Scholar 

  • Homma, T. and Goto, K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 826-829.

    Google Scholar 

  • 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.

    Google Scholar 

  • Jack, T. 2001. Relearning our ABCs: new twists on an old model. Trends Plant Sci. 6: 310-316.

    Google Scholar 

  • Jones, D., Taylor, W., and Thornton, J. 1992. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8: 275-282.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lamb, P. and McKnight, S. 1991. Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization. Trends Biochem. Sci. 16: 417-422.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Meyerowitz, E. 1987. In situ hybridization to RNA in plant tissue. Plant Mol. Biol. Rep. 5: 242-250.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Okada, K. and Shimura, Y. 1994. Genetic analyses of signaling in flower development using Arabidopsis. Plant Mol. Biol. 26: 1357-1377.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Rounsley, S., Ditta, G. and Yanofsky, M. 1995. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7: 1259-1269.

    Google Scholar 

  • Sambrook, J. and Russell, D. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Theissen, G. and Saedler, H. 2001. Plant biology: floral quartets. Nature 409: 469-471.

    Google Scholar 

  • 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.

    Google Scholar 

  • Triezenberg, S. 1995. Structure and function of transcriptional activation domains. Curr. Opin. Genet. Dev. 5: 190-196.

    Google Scholar 

  • 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.

    Google Scholar 

  • Weigel, D. and Meyerowitz, E. 1994. The ABCs of floral homeotic genes. Cell 78: 203-209.

    Google Scholar 

  • West, A. and Sharrocks, A. 1999. MADS-box transcription factors adopt alternative mechanisms for bending DNA. J. Mol. Biol. 288: 1311-1323.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

Download references

Author information

Affiliations

  1. Instituto de Investigaciones Biotecnológicas, IIB/INTECH (CONICET/UNSAM) c.c. 164, 7130, Chascomús, Argentina

    María Victoria Busi, Claudia Bustamante, Cecilia D'Angelo, Mauricio Hidalgo-Cuevas & Eduardo Zabaleta

  2. Instituto de Biología Molecular y Celular de Rosario, IBR, Facultad Cs. Bioquímicas y Farmacéuticas, UNR, Suipacha 531, 2000, Rosario, Argentina

    Silvana B. Boggio & Estela M. Valle

Authors
  1. María Victoria Busi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Bustamante
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia D'Angelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mauricio Hidalgo-Cuevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Silvana B. Boggio
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Estela M. Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eduardo Zabaleta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eduardo Zabaleta.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025001402838

  • fruit development
  • Lycopersicon esculentum
  • MADS-box genes
  • seed development