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:

Growth dynamics underlying petal shape and asymmetry

Abstract

Development commonly involves the generation of complex shapes from simpler ones. One way of following this process is to use landmarks to track the fate of particular points in a developing organ1,2,3,4,5,6,7, but this is limited by the time over which it can be monitored. Here we use an alternative method, clonal analysis8, whereby dividing cells are genetically marked and their descendants identified visually, to observe the development of Antirrhinum (snapdragon) petals. Clonal analysis has previously been used to estimate growth parameters of leaves9,10,11 and Drosophila wings12,13,14 but these results were not integrated within a dynamic growth model. Here we develop such a model and use it to show that a key aspect of shape—petal asymmetry—in the petal lobe of Antirrhinum depends on the direction of growth rather than regional differences in growth rate. The direction of growth is maintained parallel to the proximodistal axis of the flower, irrespective of changes in shape, implying that long-range signals orient growth along the petal as a whole. Such signals may provide a general mechanism for orienting growth in other growing structures.

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: Determining growth parameters.
Figure 2: Results and validation of growth analysis.
Figure 3: Petal lobe shapes at P46 resulting from growth simulations run forwards in developmental time from P32.
Figure 4: Growth of petal lobe in relation to the whole flower.

Similar content being viewed by others

References

  1. Avery, G. S. Structure and development of the tobacco leaf. Am. J. Bot. 20, 565–592 (1933)

    Article  Google Scholar 

  2. Richards, O. W. & Kavanagh, A. J. The analysis of the relative growth gradients and changing form of growing organisms: Illustrated by the tobacco leaf. Am. Nat. 77, 385–399 (1943)

    Article  Google Scholar 

  3. Erickson, R. O. Modeling of plant growth. Annu. Rev. Plant Physiol. 27, 407–434 (1976)

    Article  Google Scholar 

  4. Erickson, R. O. Relative elemental rates and anisotropy of growth in area: a computer programme. J. Exp. Bot. 17, 390–403 (1966)

    Article  Google Scholar 

  5. Wolf, S. D., Silk, W. K. & Plant, R. E. Quantitative patterns of leaf expansion—Comparison of normal and malformed leaf growth in Vitis-Vinifera Cv Ruby Red. Am. J. Bot. 73, 832–846 (June 1986)

    Article  Google Scholar 

  6. Dumais, J. & Kwiatkowska, D. Analysis of surface growth in shoot apices. Plant J. 31, 229–241 (2002)

    Article  Google Scholar 

  7. Hernandez, F., Havelange, A., Bernier, G. & Green, P. B. Growth behavior of single epidermal cells during flower formation: Sequential scanning electron micrographs provide kinematic patterns for Anagallis. Planta 185, 139–147 (1991)

    Article  CAS  Google Scholar 

  8. Subtelny, S. & Sussex, I. M. (eds) The Clonal Basis of Development (Academic, New York, 1978)

  9. Poethig, R. S. & Sussex, I. M. The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165, 170–184 (1985)

    Article  CAS  Google Scholar 

  10. Poethig, R. S. & Szymkowiak, R. J. Clonal analysis of leaf development in maize. Maydica 40, 67–76 (1995)

    Google Scholar 

  11. Dolan, L. & Poethig, R. S. Clonal analysis of leaf development in cotton. Am. J. Bot. 85, 315–321 (1998)

    Article  CAS  Google Scholar 

  12. Garcia-Bellido, A. & Merriam, J. R. Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev. Biol. 24, 61–87 (1971)

    Article  CAS  Google Scholar 

  13. Gonzalez-Gaitan, M., Capdevila, M. P. & Garcia-Bellido, A. Cell proliferation patterns in the wing imaginal disc of Drosophila. Mech. Dev. 40, 183–200 (1994)

    Article  Google Scholar 

  14. Resino, J., Salama-Cohen, P. & Garcia-Bellido, A. Determining the role of patterned cell proliferation in the shape and size of the Drosophila wing. Proc Natl Acad. Sci. USA 99, 7502–7507 (2002)

    Article  ADS  CAS  Google Scholar 

  15. Poethig, R. S. Clonal analysis of cell lineage patterns in plant development. Am. J. Bot. 74, 581–594 (1987)

    Article  Google Scholar 

  16. Almeida, J., Rocheta, M. & Galego, L. Genetic control of flower shape in Antirrhinum majus. Development 124, 1387–1392 (1997)

    CAS  PubMed  Google Scholar 

  17. Luo, D. et al. Control of organ asymmetry in flowers of Antirrhinum. Cell 99, 367–376 (1999)

    Article  CAS  Google Scholar 

  18. Luo, D., Carpenter, R., Vincent, C., Copsey, L. & Coen, E. Origin of floral asymmetry in Antirrhinum. Nature 383, 794–799 (1995)

    Article  ADS  Google Scholar 

  19. Cubas, P., Lauter, N., Doebley, J. & Coen, E. The TCP domain: a motif found in proteins regulating plant growth and development. Plant J. 18, 215–222 (1999)

    Article  CAS  Google Scholar 

  20. Vincent, C. A., Carpenter, C. & Coen, E. S. Plant J. 33, 1–10 (2003)

    Article  Google Scholar 

  21. Perbal, M. C., Haughn, G., Saedler, H. & Schwarz-Sommer, Z. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122, 3433–3441 (1996)

    CAS  PubMed  Google Scholar 

  22. Efremova, N. et al. Epidermal control of floral organ identity by class B homeotic genes in Antirrhinum and Arabidopsis. Development 14, 2661–2671 (2001)

    Google Scholar 

  23. Tilney-Basset, R. A. E. Plant Chimeras (Edward Arnolds, London, 1986)

    Google Scholar 

  24. Maksymowych, R. Analysis of Leaf Development Developmental and cell biology series 1 (Cambridge Univ. Press, London, 1973)

    Google Scholar 

  25. Lloyd, C. W. & Traas, J. A. The role of F-actin in determining the division plane of carrot suspension cells—drug studies. Development 102, 211–221 (1988)

    CAS  Google Scholar 

  26. Thompson, D. A. W. On Growth and Form, 2nd edn Vol. 2 (Cambridge Univ. Press, Cambridge, UK, 1942)

    MATH  Google Scholar 

  27. Sachs, T. in Pattern Formation in Plant Tissues (eds Barlow, P. W., Bray, D., Green, P. B. & Slack, J. M. W.) (Cambridge Univ. Press, Cambridge, UK, 1991)

    Book  Google Scholar 

  28. Teleman, A., Strigini, M. & Cohen, S. M. Shaping morphogen gradients. Cell 105, 559–562 (2001)

    Article  CAS  Google Scholar 

  29. Vincent, C. A., Carpenter, R. & Coen, E. S. Cell lineage patterns and homeotic gene activity during Antirrhinum flower development. Curr. Biol. 5, 1449–1457 (1995)

    Article  CAS  Google Scholar 

  30. Harrison, B. J. & Fincham, J. R. S. Instability at the Pal locus in Antirrhinum Majus. I. Effects of environment on frequencies of somatic and germinal mutation. Heredity 19, 237–258 (1964)

    Article  Google Scholar 

Download references

Acknowledgements

We thank R. Carpenter for providing plant stocks, C. Vincent and K. Lee for the scanning electron microscopy, J. Dumais for help with SEM 3D reconstructions, N. Orme for drawings in Fig. 1, S. J. Impey for gathering the image database and for early work on the project, supported by a BBSRC grant. A.-G. R.-L. was supported by a Norwich Research Park studentship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Enrico Coen.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rolland-Lagan, AG., Bangham, J. & Coen, E. Growth dynamics underlying petal shape and asymmetry. Nature 422, 161–163 (2003). https://doi.org/10.1038/nature01443

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01443

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