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Model for perianth formation in orchids

Abstract

Orchidaceae, the orchid family under the order Asparagales, contains more than 20,000 accepted species in approximately 880 genera13. In contrast to most flowers of actinomorphic symmetry, orchid flowers typically have zygomorphic symmetry with a striking well-differentiated labellum (lip) that acts as the main pollinator attractant by employing visual, fragrance and tactile cues47. Genetics models controlling patterning formation of actinomorphic flowers, such as Arabidopsis, are well known. However, the mechanisms of sepal/petal/lip determination remain obscure. Here, we demonstrate a conserved principle, called the Perianth (P) code, which involves competition between two protein complexes containing different AP3/AGL6 homologues to determine the formation of the complex perianth patterns in orchids. In the P code, the higher-order heterotetrameric SP (sepal/petal) complex (OAP3-1/OAGL6-1/OAGL6-1/OPI) specifies sepal/petal formation, whereas the L (lip) complex (OAP3-2/OAGL6-2/OAGL6-2/OPI) is exclusively required for lip formation. This model is validated by the conversion of lips into sepal/petal structures in Oncidium and Phalaenopsis orchids through the suppression of the proposed L complex activity in lips using the virus-induced gene silencing (VIGS) strategy. A comprehensive examination of four different subfamilies of Orchidaceae further validates the P code and significantly extends the current knowledge regarding the mechanism and pathways of perianth formation in orchids.

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Figure 1: OMADS box gene expression profiles in Oncidium reveal the P-code model.
Figure 2: Detection of interaction among OMADS proteins.
Figure 3: Conversion of lips into sepal/petal-like structures in Oncidium and Phalaenopsis orchids by suppressing OAGL6-2 orthologue expression through the VIGS strategy.
Figure 4: Possible evolutionary relationships between the SP and L complexes of the P-code model involved in regulating sepal/petal/lip formation in orchids.

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References

  1. Cameron, K. M. et al. A phylogenetic analysis of the Orchidaceae: evidence from rbcL nucleotide. Am. J. Bot. 86, 208–224 (1999).

    Article  Google Scholar 

  2. Chase, M. W., Cameron, K. M., Barrett, R. L. & Freudenstein, J. V. in Orchid Conservation (eds Dixon, K. M., Kell, S. P., Barrett, R. L. & Cribb, P. J. ) 69–89 (Natural History Publications, 2003).

    Google Scholar 

  3. Gorniak, M., Paun, O. & Chase, M. W. Phylogenetic relationships within Orchidaceae based on a low-copy nuclear coding gene, Xdh: congruence with organellar and nuclear ribosomal DNA results. Mol. Phylogenet. Evol. 56, 784–795 (2010).

    Article  CAS  Google Scholar 

  4. Dressler, R. L. Phylogeny and classification of the Orchid family [electronic resource] (Dioscorides Press, 1993).

    Google Scholar 

  5. Rudall, P. J. & Bateman, R. M. Roles of synorganisation, zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots. Biol. Rev. Camb. Philos. Soc. 77, 403–441 (2002).

    Article  Google Scholar 

  6. Kocyan, A., Conti, E., Qiu, Y-L. & Endress, P. K. A phylogenetic analysis of Apostasioideae (Orchidaceae) based on ITS, trn L-F and mat K sequences. Plant Syst. Evol. 247, 203–213 (2004).

    Article  CAS  Google Scholar 

  7. Cozzolino, S. & Widmer, A. Orchid diversity: an evolutionary consequence of deception? Trends Ecol. Evol. 20, 487–494 (2005).

    Article  Google Scholar 

  8. Krizek, B. A. & Meyerowitz, E. M. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11–22 (1996).

    CAS  PubMed  Google Scholar 

  9. Kramer, E. M., Dorit, R. L. & Irish, V. F. 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 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Hernandez-Hernandez, T., Martinez-Castilla, L. P. & Alvarez-Buylla, E. R. Functional diversification of B MADS-box homeotic regulators of flower development: adaptive evolution in protein-protein interaction domains after major gene duplication events. Mol. Biol. Evol. 24, 465–481 (2007).

    Article  CAS  Google Scholar 

  11. Irish, V. F. Evolution of petal identity. J. Exp. Bot. 60, 2517–2527 (2009).

    Article  CAS  Google Scholar 

  12. Hsu, H. F. & Yang, C. H. An orchid (Oncidium Gower Ramsey) AP3-like MADS gene regulates floral formation and initiation. Plant Cell Physiol. 43, 1198–1209 (2002).

    Article  CAS  Google Scholar 

  13. Tsai, W. C., Kuoh, C. S., Chuang, M. H., Chen, W. H. & Chen, H. H. Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell. Physiol. 45, 831–844 (2004).

    Article  CAS  Google Scholar 

  14. Xu, Y., Teo, L. L., Zhou, J., Kumar, P. P. & Yu, H. Floral organ identity genes in the orchid Dendrobium crumenatum. Plant J. 46, 54–68 (2006).

    Article  CAS  Google Scholar 

  15. Mondragon-Palomino, M. & Theissen, G. MADS about the evolution of orchid flowers. Trends Plant Sci. 13, 51–59 (2008).

    Article  CAS  Google Scholar 

  16. Chang, Y. Y. et al. Characterization of the possible roles for B class MADS box genes in regulation of perianth formation in orchid. Plant Physiol. 152, 837–853 (2010).

    Article  CAS  Google Scholar 

  17. Mondragon-Palomino, M. & Theissen, G. Conserved differential expression of paralogous DEFICIENS- and GLOBOSA-like MADS-box genes in the flowers of Orchidaceae: refining the ‘orchid code’. Plant J. 66, 1008–1019 (2011).

    Article  CAS  Google Scholar 

  18. Pan, Z. J. et al. The duplicated B-class MADS-box genes display dualistic characters in orchid floral organ identity and growth. Plant Cell Physiol. 52, 1515–1531 (2011).

    Article  CAS  Google Scholar 

  19. Su, C. L. et al. A modified ABCDE model of flowering in orchids based on gene expression profiling studies of the moth orchid Phalaenopsis aphrodite. PLoS ONE 8, http://dx.doi.org/10.1371/journal.pone.0080462 (2013).

  20. Acri-Nunes-Miranda, R. & Mondragon-Palomino, M. Expression of paralogous SEP-, FUL-, AG- and STK-like MADS-box genes in wild-type and peloric Phalaenopsis flowers. Front. Plant Sci. 5, http://dx.doi.org/doi:10.3389/fpls.2014.00076 (2014).

  21. Pan, Z. J. et al. Flower development of Phalaenopsis orchid involves functionally divergent SEPALLATA-like genes. New Phytol. 202, 1024–1042 (2014).

    Article  CAS  Google Scholar 

  22. Chang, Y. Y., Chiu, Y. F., Wu, J. W. & Yang, C. H. Four orchid (Oncidium Gower Ramsey) AP1/AGL9-like MADS box genes show novel expression patterns and cause different effects on floral transition and formation in Arabidopsis thaliana. Plant Cell. Physiol. 50, 1425–1438 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Theissen, G. & Saedler, H. Plant biology. Floral quartets. Nature 409, 469–471 (2001).

    Article  CAS  Google Scholar 

  25. Melzer, R. & Theissen, G. Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res. 37, 2723–2736 (2009).

    Article  CAS  Google Scholar 

  26. Smaczniak, C. et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc. Natl Acad. Sci. USA 109, 1560–1565 (2012).

    Article  CAS  Google Scholar 

  27. Hsu, W. H. et al. AGAMOUS-LIKE13, a putative ancestor for the E functional genes, specifies male and female gametophyte morphogenesis. Plant J. 77, 1–15 (2014).

    Article  CAS  Google Scholar 

  28. Hsieh, M. H. et al. Virus-induced gene silencing unravels multiple transcription factors involved in floral growth and development in Phalaenopsis orchids. J. Exp. Bot. 64, 3869–3884 (2013).

    Article  CAS  Google Scholar 

  29. Hsieh, M. H. et al. Optimizing virus-induced gene silencing efficiency with Cymbidium mosaic virus in Phalaenopsis flower. Plant Sci. 201–202, 25–41 (2013).

    Article  Google Scholar 

  30. Lu, H. C. et al. A high-throughput virus-induced gene-silencing vector for screening transcription factors in virus-induced plant defense response in orchid. Mol. Plant Microbe Interact. 25, 738–746 (2012).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants to C-H.Y. from the National Science Council, Taiwan, ROC, grant number: NSC96-2752-B-005-007-PAE and NSC 100-2313-B-005-004-MY3. This work was also supported in part by the Ministry of Education, Taiwan, ROC under the ATU plan. We thank Drs Elena M. Kramer (Department of Organismic and Evolutionary Biology, Harvard University) and Kerstin Kaufmann (Institute of Biochemistry and Biology, University of Potsdam) for their helpful discussion of the results.

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Contributions

C-H.Y. and H-F.H. developed the overall strategy, designed experiments and coordinated the project. H-F.H. and W-T.M. performed gene expression analyses. W-H.H., H-F.H. and J-Y.L. performed FRET analyses. Y-I.L., H-F.H. and C-H.Y. collected the orchid samples. Y-I.L. and H-F.H. performed the cryoscanning electron microscopy. H-F.H., W-T.M. and J-Y.Y. performed VIGS experiments. C-H.Y. and H-F.H. prepared and revised the manuscript.

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Correspondence to Chang-Hsien Yang.

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The authors declare no competing financial interests.

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Hsu, HF., Hsu, WH., Lee, YI. et al. Model for perianth formation in orchids. Nature Plants 1, 15046 (2015). https://doi.org/10.1038/nplants.2015.46

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