Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Assessing the redundancy of MADS-box genes during carpel and ovule development

Abstract

Carpels are essential for sexual plant reproduction because they house the ovules and subsequently develop into fruits that protect, nourish and ultimately disperse the seeds. The AGAMOUS (AG) gene is necessary for plant sexual reproduction because stamens and carpels are absent from ag mutant flowers1,2. However, the fact that sepals are converted into carpelloid organs in certain mutant backgrounds even in the absence of AG activity indicates that an AG-independent carpel-development pathway exists2. AG is a member of a monophyletic clade of MADS-box genes that includes SHATTERPROOF1 (SHP1), SHP2 and SEEDSTICK (STK)3, indicating that these four genes might share partly redundant activities. Here we show that the SHP genes are responsible for AG-independent carpel development. We also show that the STK gene is required for normal development of the funiculus, an umbilical-cord-like structure that connects the developing seed to the fruit, and for dispersal of the seeds when the fruit matures. We further show that all four members of the AG clade are required for specifying the identity of ovules, the landmark invention during the course of vascular plant evolution that enabled seed plants to become the most successful group of land plants4.

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

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: AG acts redundantly with SHP genes to specify carpel identity.
Figure 2: Characterization of STK.
Figure 3: All members of the AG clade redundantly specify ovule identity.
Figure 4

Similar content being viewed by others

References

  1. Bowman, J. L., Smyth, D. R. & Meyerowitz, E. M. Genes directing flower development in Arabidopsis. Plant Cell 1, 37–52 (1989)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bowman, J. L., Smyth, D. R. & Meyerowitz, E. M. Genetic interactions among floral homeotic genes of Arabidopsis. Development 112, 1–20 (1991)

    CAS  PubMed  Google Scholar 

  3. Theissen, G. et al. A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115–149 (2000)

    Article  CAS  PubMed  Google Scholar 

  4. Stewart, W. N. & Rothwell, G. W. Paleobotany and the evolution of plants (Cambridge Univ. Press, 1993)

    Google Scholar 

  5. Drews, G. N., Bowman, J. L. & Meyerowitz, E. M. Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991–1002 (1991)

    Article  CAS  PubMed  Google Scholar 

  6. Alvarez, J. & Smyth, D. R. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126, 2377–2386 (1999)

    CAS  PubMed  Google Scholar 

  7. Savidge, B., Rounsley, S. D. & Yanofsky, M. F. Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7, 721–733 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Flanagan, C. A., Hu, Y. & Ma, H. Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J. 10, 343–353 (1996)

    Article  CAS  PubMed  Google Scholar 

  9. Heisler, M. G. B., Atkinson, A., Bylstra, Y. H., Walsh, R. & Smyth, D. R. SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 128, 1089–1098 (2001)

    CAS  PubMed  Google Scholar 

  10. Liljegren, S. J. et al. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404, 766–770 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Mizukami, Y. & Ma, H. Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119–131 (1992)

    Article  CAS  PubMed  Google Scholar 

  12. Rounsley, S. D., Ditta, G. S. & Yanofsky, M. F. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7, 1259–1269 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ma, H., Yanofsky, M. F. & Meyerowitz, E. M. AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev. 5, 484–495 (1991)

    Article  CAS  PubMed  Google Scholar 

  14. Angenent, G. C. et al. A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 7, 1569–1582 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Colombo, L. et al. The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7, 1859–1868 (1995)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Western, T. L. & Haughn, G. W. BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. Plant J. 18, 329–336 (1999)

    Article  CAS  PubMed  Google Scholar 

  17. Blazquez, M. A., Soowal, L. N., Lee, I. & Weigel, D. LEAFY expression and flower initiation in Arabidopsis. Development 124, 3835–3844 (1997)

    CAS  PubMed  Google Scholar 

  18. Sessions, A., Weigel, D. & Yanofsky, M. F. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20, 259–263 (1999)

    Article  CAS  PubMed  Google Scholar 

  19. Wisman, E., Cardon, G. H., Fransz, P. & Saedler, H. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol. Biol. 37, 989–999 (1998)

    Article  CAS  PubMed  Google Scholar 

  20. Kempin, S. A. et al. Targeted disruption in Arabidopsis. Nature 389, 802–803 (1997)

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Kunst, L., Klenz, J. E., Martinezzapater, J. & Haughn, G. W. AP2 gene determines the identity of perianth organs in flowers of Arabidopsis thaliana. Plant Cell 1, 1195–1208 (1989)

    Article  PubMed  PubMed Central  Google Scholar 

  22. Yanofsky, M. F. et al. The protein encoded by the Arabidopsis homeotic gene AGAMOUS resembles transcription factors. Nature 346, 35–39 (1990)

    Article  ADS  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Ray for advice on scanning electron microscopy, D. Weigel for providing the pDW137 vector, members of Yanofsky laboratory for comments, and H. Chang and P. Golshani for technical assistance. A.P. received a scholarship from the Ananda Mahidol Foundation, and this work was supported by a grant from the National Science Foundation (to M.Y.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin F. Yanofsky.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pinyopich, A., Ditta, G., Savidge, B. et al. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424, 85–88 (2003). https://doi.org/10.1038/nature01741

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01741

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing