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.

  • Article
  • Published:

Flexibility in the structure of spiral flowers and its underlying mechanisms

Nature Plants volume 2, Article number: 15188 (2016) Cite this article

Subjects

Abstract

Spiral flowers usually bear a variable number of organs, suggestive of the flexibility in structure. The mechanisms underlying the flexibility, however, remain unclear. Here we show that in Nigella damascena, a species with spiral flowers, different types of floral organs show different ranges of variation in number. We also show that the total number of organs per flower is largely dependent on the initial size of the floral meristem, whereas the respective numbers of different types of floral organs are determined by the functional domains of corresponding genetic programmes. By conducting extensive expression and functional studies, we further elucidate the genetic programmes that specify the identities of different types of floral organs. Notably, the AGL6-lineage member NdAGL6, rather than the AP1-lineage members NdFL1/2, is an A-function gene, whereas petaloidy of sepals is not controlled by AP3- or PI-lineage members. Moreover, owing to the formation of a regulatory network, some floral organ identity genes also regulate the boundaries between different types of floral organs. On the basis of these results, we propose that the floral organ identity determination programme is highly dynamic and shows considerable flexibility. Transitions from spiral to whorled flowers, therefore, may be explained by evolution of the mechanisms that reduce the flexibility.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Whorled versus spiral flowers.
Figure 2: Dynamic expression of floral organ identity genes in Nigella damascena.
Figure 3: Phenotypes of VIGS-treated Nigella damascena flowers.
Figure 4: Floral organ identity determination in wild-type, ‘Double Sepals’ and VIGS-treated Nigella damascena flowers.

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  Google Scholar 

  2. Schwarz-Sommer, Z., Huijser, P., Nacken, W., Saedler, H. & Sommer, H. Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250, 931–936 (1990).

    Article  CAS  Google Scholar 

  3. Coen, E. S. & Meyerowitz, E. M. The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37 (1991).

    Article  CAS  Google Scholar 

  4. Pelaz, S., Ditta, G. S., Baumann, E., Wisman, E. & Yanofsky, M. F. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405, 200–203 (2000).

    Article  CAS  Google Scholar 

  5. Honma, T. & Goto, K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409, 525–529 (2001).

    Article  CAS  Google Scholar 

  6. Theissen, G. Development of floral organ identity: stories from the MADS house. Curr. Opin. Plant Biol. 4, 75–85 (2001).

    Article  CAS  Google Scholar 

  7. Ferrario, S., Immink, R. G. & Angenent, G. C. Conservation and diversity in flower land. Curr. Opin. Plant Biol. 7, 84–91 (2004).

    Article  Google Scholar 

  8. Litt, A. & Kramer, E. M. The ABC model and the diversification of floral organ identity. Semin. Cell Dev. Biol. 21, 129–137 (2010).

    Article  CAS  Google Scholar 

  9. Causier, B., Schwarz-Sommer, Z. & Davies, B. Floral organ identity: 20 years of ABCs. Semin. Cell Dev. Biol. 21, 73–79 (2010).

    Article  CAS  Google Scholar 

  10. Mandel, M. A., Gustafson-Brown, C., Savidge, B. & Yanofsky, M. F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360, 273–277 (1992).

    Article  CAS  Google Scholar 

  11. Kim, S. et al. Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators. Plant J. 43, 724–744 (2005).

    Article  CAS  Google Scholar 

  12. Soltis, D. E., Chanderbali, A. S., Kim, S., Buzgo, M. & Soltis, P. S. The ABC model and its applicability to basal angiosperms. Ann. Bot. 100, 155–163 (2007).

    Article  CAS  Google Scholar 

  13. Endress, P. K. & Doyle, J. A. Floral phyllotaxis in basal angiosperms: development and evolution. Curr. Opin. Plant Biol. 10, 52–57 (2007).

    Article  Google Scholar 

  14. Endress, P. K. The early evolution of the angiosperm flower. Trends Ecol. Evol. 2, 300–304 (1987).

    Article  CAS  Google Scholar 

  15. Soltis, P. S. et al. Floral variation and floral genetics in basal angiosperms. Am. J. Bot. 96, 110–128 (2009).

    Article  Google Scholar 

  16. Ronse De Craene, L. P., Soltis, P. S. & Soltis, D. E. Evolution of floral structures in basal angiosperms. Int. J. Plant Sci. 164, S329–S363 (2003).

    Article  Google Scholar 

  17. Zhang, R. et al. Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae). Proc. Natl Acad. Sci. USA 110, 5074–5079 (2013).

    Article  CAS  Google Scholar 

  18. Goncalves, B. et al. An APETALA3 homolog controls both petal identity and floral meristem patterning in Nigella damascena L. (Ranunculaceae). Plant J. 76, 223–235 (2013).

    CAS  PubMed  Google Scholar 

  19. Running, M. P. & Hake, S. The role of floral meristems in patterning. Curr. Opin. Plant Biol. 4, 69–74 (2001).

    Article  CAS  Google Scholar 

  20. Hill, J. P. & Lord, E. M. Floral development in Arabidopsis thaliana – a comparison of the wild-type and the homeotic pistillata mutant. Can. J. Bot. 67, 2922–2936 (1989).

    Article  Google Scholar 

  21. Jack, T., Brockman, L. L. & Meyerowitz, E. M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68, 683–697 (1992).

    Article  CAS  Google Scholar 

  22. Riechmann, J. L., Krizek, B. A. & Meyerowitz, E. M. Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl Acad. Sci. USA 93, 4793–4798 (1996).

    Article  CAS  Google Scholar 

  23. Kramer, E. M. et al. Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. Plant Cell 19, 750–766 (2007).

    Article  CAS  Google Scholar 

  24. Kramer, E. M. New model systems for the study of developmental evolution in plants. Curr. Top. Dev. Biol. 86, 67–105 (2009).

    Article  CAS  Google Scholar 

  25. Chanderbali, A. S. et al. Genetic footprints of stamen ancestors guide perianth evolution in Persea (Lauraceae). Int. J. Plant Sci. 167, 1075–1089 (2006).

    Article  CAS  Google Scholar 

  26. Baum, D. A. The evolution of plant development. Curr. Opin. Plant Biol. 1, 79–86 (1998).

    Article  CAS  Google Scholar 

  27. Douglas, A. W. The developmental basis of morphological diversification and synorganization in flowers of Conospermeae (Stirlingia and Conosperminae: Proteaceae). Int. J. Plant Sci. 158, S13–S48 (1997).

    Article  Google Scholar 

  28. Smith, R. S., Kuhlemeier, C. & Prusinkiewicz, P. Inhibition fields for phyllotactic pattern formation: a simulation study. Can. J. Bot. 84, 1635–1649 (2006).

    Article  Google Scholar 

  29. Jabbour, F., De Craene, L. P. R., Nadot, S. & Damerval, C. Establishment of zygomorphy on an ontogenic spiral and evolution of perianth in the tribe Delphinieae (Ranunculaceae). Ann. Bot. 104, 809–822 (2009).

    Article  Google Scholar 

  30. Corley, S. B., Carpenter, R., Copsey, L. & Coen, E. Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc. Natl Acad. Sci. USA 102, 5068–5073 (2005).

    Article  CAS  Google Scholar 

  31. LaRue, N. C., Sullivan, A. M. & Di Stilio, V. S. Functional recapitulation of transitions in sexual systems by homeosis during the evolution of dioecy in Thalictrum. Front. Plant Sci. 4, 487 (2013).

    PubMed  PubMed Central  Google Scholar 

  32. Zachgo, S. et al. Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development 121, 2861–2875 (1995).

    CAS  PubMed  Google Scholar 

  33. Ito, T., Ng, K. H., Lim, T. S., Yu, H. & Meyerowitz, E. M. The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19, 3516–3529 (2007).

    Article  CAS  Google Scholar 

  34. Wuest, S. E. et al. Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc. Natl Acad. Sci. USA 109, 13452–13457 (2012).

    Article  CAS  Google Scholar 

  35. Zahn, L. M. et al. Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol. Dev. 8, 30–45 (2006).

    Article  CAS  Google Scholar 

  36. Yellina, A. L. et al. Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica). Evodevo 1, 13 (2010).

    Article  CAS  Google Scholar 

  37. Di Stilio, V. S., Kramer, E. M. & Baum, D. A. Floral MADS box genes and homeotic gender dimorphism in Thalictrum dioicum (Ranunculaceae) – a new model for the study of dioecy. Plant J. 41, 755–766 (2005).

    Article  CAS  Google Scholar 

  38. Galimba, K. D. & Di Stilio, V. S. Sub-functionalization to ovule development following duplication of a floral organ identity gene. Dev. Biol. 405, 158–172 (2015).

    Article  CAS  Google Scholar 

  39. Wardlaw, C. W. The floral meristem as a reaction system. Proc. R. Soc. Edinb. B. 66, 394–408 (1957).

    Google Scholar 

  40. Hicks, G. S. & Sussex, I. M. Organ regeneration in sterile culture after median bisection of the flower primordia of Nicotiana tabacum. Bot. Gaz. 132, 350–363 (1971).

    Article  Google Scholar 

  41. Coen, E. S. The role of homeotic genes in flower development and evolution. Annu. Rev. Plant Physiol. Mol. Biol. 42, 241–279 (1991).

    Article  Google Scholar 

  42. Day, C. D., Galgoci, B. F. C. & Irish, V. F. Genetic ablation of petal and stamen primordia to elucidate cell-interactions during floral development. Development 121, 2887–2895 (1995).

    CAS  PubMed  Google Scholar 

  43. Chanderbali, A. S. et al. Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Proc. Natl Acad. Sci. USA 107, 22570–22575 (2010).

    Article  CAS  Google Scholar 

  44. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    Article  CAS  Google Scholar 

  45. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

  46. Kramer, E. M. Methods for studying the evolution of plant reproductive structures: comparative gene expression techniques. Methods Enzymol. 395, 617–636 (2005).

    Article  CAS  Google Scholar 

  47. Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol. 29, 644–652 (2011).

    Article  CAS  Google Scholar 

  48. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628 (2008).

    Article  CAS  Google Scholar 

  49. Gould, B. & Kramer, E. M. Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae). Plant Methods 3, 6 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

We thank members of the Kong laboratory for helpful discussion, and E. M. Kramer, S.-H. Shiu and three anonymous reviewers for valuable comments. This work was supported by National Natural Science Foundation of China Grants 31125005 and 31330007 and CAS Interdisciplinary Innovation Team.

Author information

Author notes

  1. Peipei Wang, Hong Liao and Wengen Zhang: These authors contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Peipei Wang, Hong Liao, Wengen Zhang, Xianxian Yu, Rui Zhang, Hongyan Shan, Xiaoshan Duan, Xu Yao & Hongzhi Kong

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Peipei Wang, Hong Liao, Wengen Zhang, Xianxian Yu, Xiaoshan Duan & Xu Yao

Authors
  1. Peipei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wengen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianxian Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hongyan Shan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaoshan Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xu Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hongzhi Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.W. and H.K. designed the research. P.W., H.L. and W.Z. performed the qRT–PCR, in situ hybridization and VIGS experiments, with the help of R.Z. and H.S. for analyzing the data. R.Z. and X. Yu provided the RNA-seq and yeast two-hybrid results, respectively, and P.W., X.D. and X. Yao conducted the morphological analyses. P.W., H.S. and H.K. wrote the manuscript.

Corresponding author

Correspondence to Hongzhi Kong.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, P., Liao, H., Zhang, W. et al. Flexibility in the structure of spiral flowers and its underlying mechanisms. Nature Plants 2, 15188 (2016). https://doi.org/10.1038/nplants.2015.188

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.188

This article is cited by

Search

Advanced 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