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Model for Perianth Formation in Orchids See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/276162457 Model for perianth formation in orchids Article in Nature Plants · April 2015 DOI: 10.1038/nplants.2015.46 CITATIONS READS 82 1,993 7 authors, including: Yung-I Lee Wan-Ting Mao National Museum of Natural Science National Chung Hsing University 81 PUBLICATIONS 1,297 CITATIONS 4 PUBLICATIONS 94 CITATIONS SEE PROFILE SEE PROFILE Jun-Yi Yang National Chung Hsing University 60 PUBLICATIONS 1,905 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: I am working on orchid embryology, cytogenetics, mycorrhizal association, usingCypripedium, Paphiopedilum and Phalaenopsis as the experimental materials. View project All content following this page was uploaded by Yung-I Lee on 07 January 2016. The user has requested enhancement of the downloaded file. LETTERS PUBLISHED: 27 APRIL 2015 | ARTICLE NUMBER: 15046 | DOI: 10.1038/NPLANTS.2015.46 Model for perianth formation in orchids Hsing-Fun Hsu1, Wei-Han Hsu1,Yung-ILee2,3, Wan-Ting Mao1, Jun-Yi Yang4, Jen-Ying Li1 and Chang-Hsien Yang1,5* Orchidaceae, the orchid family under the order Asparagales, protein complexes involved in perianth formation and patterning. contains more than 20,000 accepted species in approximately We comprehensively examined the expression of all identified A 880 genera1–3. In contrast to most flowers of actinomorphic (AP1-like), B (AP3-like and PI-like) and E (AGL6-like and SEP1/ symmetry, orchid flowers typically have zygomorphic sym- 3-like) OMADS box genes in mature flowers of O. Gower Ramsey metry with a striking well-differentiated labellum (lip) that (Fig. 1a-1, left), its parent species O. flexuosum (Supplementary acts as the main pollinator attractant by employing visual, Fig. 2a-1) and the closely related horticultural cultivars O. Sweet fragrance and tactile cues4–7. Genetics models controlling pat- Sugar (Supplementary Fig. 2a-2) and O. Lemon Heart terning formation of actinomorphic flowers, such as (Supplementary Fig. 3a-1, left). As shown in Fig. 1b-1 and Arabidopsis, are well known. However, the mechanisms of Supplementary Figs 2b-1, b-2 and 3b-1, OMADS8 (OPI) was sepal/petal/lip determination remain obscure. Here, we found to be universally expressed in all perianth organs. demonstrate a conserved principle, called the Perianth (P) OMADS5 (OAP3-1) and OMADS7 (OAGL6-1) were highly code, which involves competition between two protein com- expressed in petals/sepals but undetectable in lips. OMADS9 plexes containing different AP3/AGL6 homologues to deter- (OAP3-2) was detected at high levels in lips and petals, and mine the formation of the complex perianth patterns in OMADS1 (OAGL6-2) was only expressed in lips, but its expression orchids. In the P code, the higher-order heterotetrameric SP was relatively low in lateral sepals. Further analysis indicated that (sepal/petal) complex (OAP3-1/OAGL6-1/OAGL6-1/OPI) the expression patterns of OPI, OAP3-1, OAGL6-1, OAP3-2 and specifies sepal/petal formation, whereas the L (lip) complex OAGL6-2 were very similar and highly conserved in the perianths (OAP3-2/OAGL6-2/OAGL6-2/OPI) is exclusively required of both young flower buds (2, 3, 5 and 8 mm) and mature flowers for lip formation. This model is validated by the conversion of of O. Gower Ramsey (Supplementary Fig. 4a–c). Other B, A and E lips into sepal/petal structures in Oncidium and Phalaenopsis genes, such as OMADS3 (OAP3-3), OMADS6/11 (E, OSEP3/1) and orchids through the suppression of the proposed L complex OMADS10 (A, OAP1)22, were expressed in all perianths, without a activity in lips using the virus-induced gene silencing (VIGS) notable pattern in the sepal/petal/lips (Supplementary Figs 2b-1, strategy. A comprehensive examination of four different subfa- b-2 and 3e-1). This result suggested that these A and E OMADS milies of Orchidaceae further validates the P code and signifi- box genes should involve in the general formation of perianth cantly extends the current knowledge regarding the organs. However, they do not participate further in the specification mechanism and pathways of perianth formation in orchids. of the lips and sepal/petal in orchid. In contrast, OMADS12 (OAP3-4) According to the ABCDE model, which predicts the formation of was only weakly expressed in the stamen but was expressed in any flower organ through the interaction of five classes of homeotic the carpel, although its expression was completely absent in the genes in plants, the B class genes APETALA3 (AP3) and sepal/petal/lips (Supplementary Fig. 4d). The highly conserved PISTILLATA (PI) are of particular importance in petal for- expression pattern for the A, B and E OMADS homologues was mation8–11. The AP3 orthologues identified in lower eudicots, mag- also observed in the perianth organs of four Oncidium botanical nolid dicots and monocots make up the paleoAP3 lineage, whereas species: O. gutfreundianum, O. tipuloides, O. cheirophorum and the euAP3 lineage is composed of the AP3 orthologues identified in O.cebolleta (Supplementary Fig. 2a-3 to a-6, b-3 to b-6). dicots9. More than two duplicated AP3-like genes have been ident- On the basis of the gene expression patterns among these ified in many orchid species12–17 (Supplementary Fig. 1b). However, Oncidium species, we have proposed a Perianth code (P code) hypoth- as most studies have mainly focused on the expression and function esis for the regulation of identity of perianth organs in Oncidium, of individual B or E class genes18–21, it is difficult to reach a solid which involves the interaction of OPI with two different AP3/AGL6 conclusion on perianth determination in orchids. We have pre- homologues to form two protein complexes, named SP (sepal/petal viously found that expression variation in clade 1 (OMADS5, complex) and L (lip complex) (Fig. 1c). In this P-code model, OPI renamed as OAP3-1 in this study) and clade 3 (OMADS9, is expressed ubiquitously in perianths. OAP3-1 and OAGL6-1 form renamed as OAP3-2) AP3-like genes potentially affects labellum the determinant unit of the SP complex, promoting sepal/petal devel- determination in Oncidium Gower Ramsey16 (Supplementary opment, whereas OAP3-2 and OAGL6-2 function as the determinant Fig. 1b). Additionally, an AGL6 homologue of Oncidium, unit of the L complex to promote lip development (Fig. 1c).Inthis OMADS1 (renamed as OAGL6-2) (Supplementary Fig. 1a), shows model, the SP and L complexes oppositely regulate perianth develop- a synchronized increase in gene expression accompanying perianth ment (Fig. 1c).LossofeitherOAP3-1 or OAGL6-1 in the SP complex transition towards lip-like structures16, suggesting that perianth andhighexpressionoftheintactLunit(OAP3-2/OAGL6-2)will organ identity may be determined by a complicated complex. contribute to lip development (Fig. 1d-1). Conversely, loss of either We first used Oncidium orchids (subtribe Oncidiinae, tribe OAP3-2 or OAGL6-2 from the L complex and high expression Cymbidieae in subfamily Epidendroideae) to further identify levels of the intact SP unit (OAP3-1/OAGL6-1)willcontributeto 1Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan 40227 ROC. 2Biology Department, National Museum of Natural Science, Taichung, Taiwan 40227 ROC. 3Department of Life Sciences, National Chung Hsing University, Taichung, Taiwan 40227 ROC. 4Institute of Biochemistry, National Chung Hsing University, Taichung, Taiwan 40227 ROC. 5Agricultural Biotechnology Center, National Chung Hsing University, Taichung, Taiwan 40227 ROC. *e-mail: [email protected] NATURE PLANTS | VOL 1 | MAY 2015 | www.nature.com/natureplants 1 LETTERS NATURE PLANTS DOI: 10.1038/NPLANTS.2015.46 a 1 DS P 2 3 P 4 DS 5 DS 6 DS P P P P P P P P LS LS Lip Lip Lip Lip LS Lip Lip GR GRtrip GRpl Amp Macro Pp Oc Op b 123456 4.0 PI OPI 1.4 OPI 1.6 OPI 5.0 OPI 1.6 OPI OPI 1.2 4.0 3.0 1.4 4.0 1.4 1.0 1.2 1.2 3.0 2.0 0.8 1.0 3.0 1.0 0.6 0.8 0.8 2.0 0.6 2.0 0.6 1.0 0.4 0.4 0.4 1.0 1.0 0.2 0.2 0.2 0.0 0.0 0.0 0.0 0.0 0.0 1.2 OAP3-1 OAP3-1 OAP3-1 OAP3-1 OAP3-1 OAP3-1 1.2 2.5 2.5 1.2 1.0 * 4.0 1.0 2.0 2.0 1.0 0.8 0.8 * 3.0 1.5 0.8 0.6 1.5 0.6 * 0.6 2.0 1.0 1.0 0.4 0.4 0.4 * * 1.0 0.2 0.2 0.5 0.5 0.2 0.0 0.0 0.0 0.0 0.0 0.0 SP 1.8 1.6 OL6-1 OL6-1 OL6-1 OL6-1 OL6-1 OL6-1 2.5 1.6 1.8 2.5 5.0 1.4 1.6 1.4 2.0 1.2 1.4 2.0 1.2 4.0 1.0 1.2 1.0 * 1.5 1.5 3.0 0.8 1.0 0.8 0.6 0.8 1.0 1.0 0.6 0.6 * 2.0 0.4 * * 0.4 0.4 * 0.5 0.5 * 1.0 0.2 0.2 0.2 0.0 0.0 0.0 0.0 0.0 0.0 2.0 OAP3-2 OAP3-2 OAP3-2 OAP3-2 OAP3-2 OAP3-2 1.8 2.0 * * 1.4 1.2 1.2 1.6 * 1.8 * 1.2 3.5 * 1.0 1.0 * 1.6 * 1.4 * 3.0 1.2 1.0 1.4 * 0.8 0.8 1.2 2.5 1.0 0.8 * 0.6 0.6 1.0 2.0 0.8 0.6 0.8 1.5 0.6 0.4 0.4 0.4 0.6 0.4 0.4 1.0 0.2 0.2 0.2 0.2 0.2 0.5 0.0 0.0 0.0 0.0 0.0 0.0 L 1.2 OL6-2 OL6-2 OL6-2 OL6-2 OL6-2 OL6-2 * 1.0 1.4 1.2 1.4 1.8 3.5 1.2 1.0 * 1.2 1.6 * * 0.8 * * * 1.4 3.0 1.0 1.0 0.8 1.2 2.5 0.6 0.8 0.8 * 0.6 1.0 2.0 0.4 0.6 0.6 0.8 1.5 0.4 0.6 0.4 0.4 1.0 0.2 * 0.2 * 0.4 0.2 0.2 0.2 0.5 0.0 0.0 0.0 0.0 0.0 0.0 Lip P DS LS Lip P DS LS Lip P DS LS Lip P DS LS Lip P DS LS Lip P DS LS Lip P DS LS Lip P DS LS GR GRtrip GRpl Amp Macro Pp Oc Op c d L AP3 SP Sepal/petal L6 Lip -2 -1 L6 AP3 -2 -1 1 OPI 2 OPI Lip Sepal/petal AP3-2/L6-2 AP3-1/L6-1 L SP L AP3 L6 AP3 L6 SP -2 -2 -15 -17 OPI PI 3 OPI 4 OPI Intermediate Figure 1 | OMADS box gene expression profiles in Oncidium reveal the P-code model.
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