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Model for perianth formation in orchids

Nature Plants volume 1, Article number: 15046 (2015) Cite this article

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Abstract

Orchidaceae, the orchid family under the order Asparagales, contains more than 20,000 accepted species in approximately 880 genera1–3. 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 cues4–7. 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.

According to the ABCDE model, which predicts the formation of any flower organ through the interaction of five classes of homeotic genes in plants, the B class genes APETALA3 (AP3) and PISTILLATA (PI) are of particular importance in petal formation8–11. The AP3 orthologues identified in lower eudicots, magnolid dicots and monocots make up the paleoAP3 lineage, whereas the euAP3 lineage is composed of the AP3 orthologues identified in dicots9. More than two duplicated AP3-like genes have been identified in many orchid species12–17 (Supplementary Fig. 1b). However, as most studies have mainly focused on the expression and function of individual B or E class genes18–21, it is difficult to reach a solid conclusion on perianth determination in orchids. We have previously found that expression variation in clade 1 (OMADS5, renamed as OAP3-1 in this study) and clade 3 (OMADS9, renamed as OAP3-2) AP3-like genes potentially affects labellum determination in Oncidium Gower Ramsey16 (Supplementary Fig. 1b). Additionally, an AGL6 homologue of Oncidium, OMADS1 (renamed as OAGL6-2) (Supplementary Fig. 1a), shows a synchronized increase in gene expression accompanying perianth transition towards lip-like structures16, suggesting that perianth organ identity may be determined by a complicated complex.

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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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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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Authors and Affiliations

  1. Institute of Biotechnology, National Chung Hsing University, Taichung, 40227, Taiwan, ROC

    Hsing-Fun Hsu, Wei-Han Hsu, Wan-Ting Mao, Jen-Ying Li & Chang-Hsien Yang

  2. Biology Department, National Museum of Natural Science, Taichung, 40227, Taiwan, ROC

    Yung-I Lee

  3. Department of Life Sciences, National Chung Hsing University, Taichung, 40227, Taiwan, ROC

    Yung-I Lee

  4. Institute of Biochemistry, National Chung Hsing University, Taichung, 40227, Taiwan, ROC

    Jun-Yi Yang

  5. Agricultural Biotechnology Center, National Chung Hsing University, Taichung, 40227, Taiwan, ROC

    Chang-Hsien Yang

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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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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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