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Lhmyb12, Regulating Tepal Anthocyanin Pigmentation in Asiatic Hybrid Lilies, Is Derived from Lilium Dauricum and L. Bulbiferum

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Lhmyb12, Regulating Tepal Anthocyanin Pigmentation in Asiatic Hybrid Lilies, Is Derived from Lilium Dauricum and L. Bulbiferum This article is an Advance Online Publication of the authors’ corrected proof. Note that minor changes may be made before final version publication. The Horticulture Journal Preview e Japanese Society for doi: 10.2503/hortj.OKD-057 JSHS Horticultural Science http://www.jshs.jp/ LhMYB12, Regulating Tepal Anthocyanin Pigmentation in Asiatic Hybrid Lilies, is Derived from Lilium dauricum and L. bulbiferum Masumi Yamagishi1* and Takashi Nakatsuka2 1Research Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan 2Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan Genes encoding a MYB12 transcription factor, which regulates anthocyanin biosynthesis, are the key genes causing variations in the anthocyanin colors in lily flowers. However, the origin of the MYB12 in Asiatic hybrid lilies (Lilium spp.) is not completely known. In this study, we analyzed anthocyanin pigments in tepals of L. maculatum, L. lancifolium, L. callosum, L. leichtlinii, L. davidii, L. bulbiferum, and L. dauricum, and clarified that L. dauricum and L. bulbiferum accumulated a single anthocyanin, cyanidin 3-O-rutinoside, in entire tepals, although these wild species had orange-colored tepals. The sequencing of MYB12 genes revealed seven allelic sequences among ten L. dauricum plants and two allelic sequences in one L. bulbiferum plant. These MYB12 sequences were the same as or similar to the sequences isolated from pink Asiatic hybrid lily cultivars, indicating that L. dauricum and L. bulbiferum have contributed to the anthocyanin coloration of these cultivars. Key Words: cyanidin 3-O-rutinoside, flower color, R2R3-MYB, section Daurolirion, section Sinomartagon. bear flowers with novel hues, intensities, and patterns Introduction of color. A typical feature of Asiatic hybrid lilies is the Lilies (Lilium spp.) are among the commercially huge variation in hues including yellows (because of most important and widely cultivated floriculture crops. carotenoids), oranges (because of carotenoids), pinks Cut flower production of lilies has ranked second only (because of anthocyanins), reds (because of the com- to chrysanthemums in Japan in recent years (Ministry bined presence of anthocyanins and carotenoids), and of Agriculture, Forestry and Fisheries, 2014, http:// white (Yamagishi, 2013; Yamagishi et al., 2010a, b). In www.maff.go.jp/j/tokei/kikaku/nenji/index.html, De- addition to the hues, Asiatic hybrid lily cultivars often cember 10, 2016). Interspecific hybridization is the develop raised red spots on the interior surfaces of their principal method for lily breeding. Asiatic hybrid lilies tepals (Abe et al., 2002), and sometimes develop are derived from crosses among L. dauricum, splatter-type spots, which are morphologically and ge- L. bulbiferum, L. maculatum, L. lancifolium, netically distinct from the raised spots (Yamagishi and L. callosum, L. leichtlinii, L. davidii, L. cernuum, and Akagi, 2013; Yamagishi et al., 2014b). Cyanidin 3- others, whereas Oriental hybrid lilies are derived from rutinoside is a major anthocyanin that accumulates in crosses among L. auratum, L. speciosum, L. rubellum, the lily tepals and tepal spots (Nørbæk and Kondo, L. japonicum, L. nobilissimum, and others (belonging to 1999). the section Archerilion, Leslie, 1982). The activity of anthocyanin biosynthesis enzymes is Flower color is a crucial characteristic that deter- primarily regulated by complexes that consist of R2R3- mines the commercial value of floriculture crops. Much MYB transcription factors, basic helix-loop-helix interest has been expressed in developing cultivars that (bHLH) transcription factors, and WD40 proteins (Koes et al., 2005; Lai et al., 2013; Xu et al., 2015). In lilies, LhMYB12 (R2R3-MYB) determines tepal-specific Received; October 17, 2016. Accepted; January 24, 2017. anthocyanin biosynthesis together with LhbHLH2 First Published Online in J-STAGE on February 28, 2017. (Nakatsuka et al., 2009) and LhWD40A (Suzuki et al., This work was supported by a Grant-In-Aid for Scientific Research 2016). LhMYB12 often gives rise to full-pink-colored (No. 15H04447) from the Japan Society for the Promotion of Science. tepals in Asiatic and Oriental hybrid lilies (Lai et al., * Corresponding author (E-mail: [email protected]). 2012; Yamagishi, 2011; Yamagishi et al., 2010b). An © 2017 The Japanese Society for Horticultural Science (JSHS), All rights reserved. 2 M. Yamagishi and T. Nakatsuka LhMYB12 allele, MYB12-Lat, causes splatter-type spots China, were derived from the collections at Yurigahara on tepals (Yamagishi et al., 2014b). In addition, the ex- Park and grown at the experimental farm of Hokkaido pression levels of LhMYB12 strongly affect the color in- University. The flowers of other L. dauricum plants tensities in tepals (Yamagishi et al., 2012). These results were directly collected from their natural habitats in indicate that LhMYB12 is a key factor that determines Hokkaido. One Asiatic hybrid lily ‘Sugar Love’, the hue, intensities, and patterns of anthocyanin colors MYB12 sequence of which was additionally deter- in lily flowers. Thus, understanding of the natural varia- mined, was purchased from a local market. tion in MYB12 among the wild species is important in Anthocyanin pigments in tepal backgrounds were an- lily breeding and for the introduction of novel genes or alyzed. First, pigments were extracted in 5% formic alleles of MYB12 that bring unnatural color phenotypes acid overnight from the tepals of the seven wild species. into new lily cultivars. For progress in such research, it Second, the pigments in the tepals of L. dauricum and is necessary to determine the wild species that donated L. bulbiferum were extracted with a mixture of metha- MYB12 to the lily cultivars. nol, acetic acid, and water (4:1:5, v/v/v) to analyze In an earlier study, we determined the MYB12 se- anthocyanins qualitatively. After filtration through quences in wild lily species that have been used to de- ZORBAX Eclipse Plus C18 (Agilent Technologies, velop Asiatic and Oriental hybrid lilies and compared Tokyo, Japan), the extract was analyzed by high- them to the MYB12 sequences in Asiatic and Oriental performance liquid chromatography (HPLC), using an hybrid lily cultivars (Yamagishi et al., 2014a). The Agilent 1290 infinity system (Agilent Technologies), pink- and red-colored Oriental hybrid lily cultivars had with a YMC-Triart C18 column (2.0 × 50 mm, 1.9 μm, the same or similar MYB12 sequences as L. rubellum YMC Co., Ltd, Kyoto, Japan). A linear gradient of 10– and L. speciosum, indicating that LhMYB12 in Oriental 60% solvent B (1.5% H3PO4, 20% acetic acid, and 25% hybrid lilies is mainly derived from these two species. acetonitrile) in solvent A (1.5% H3PO4) was passed Among the pink-colored Asiatic hybrid lily cultivars, over a 9-min period. The anthocyanins were identified ‘Vermeer’ had the same MYB12 sequence as on the basis of absorption spectra obtained using a pho- L. cernuum, which shows full-pink tepal pigmentation, todiode array detector. Finally, for quantitative analysis, indicating that ‘Vermeer’ LhMYB12 is derived from the pigments were extracted in 5% formic acid and their L. cernuum. However, the MYB12 sequences in other absorbance was measured at 515 nm, as described pre- Asiatic hybrid lily cultivars are comparatively distantly viously (Yamagishi, 2016). related to the L. cernuum sequence. Thus, it is assumed MYB12 sequences in L. dauricum, L. bulbiferum, and that in other wild species, MYB12 genes have contrib- ‘Sugar Love’ were determined. The methods used for uted to the pink coloration in Asiatic hybrid lilies. RNA isolation, cDNA synthesis, PCR amplification of To screen the wild species that have potentially con- MYB12, and sequencing of the amplified products were tributed to the pink coloration in Asiatic hybrid lilies, same as those described in an earlier report (Yamagishi pigments were extracted from the tepals of seven Lilium et al., 2014a). Briefly, nearly full-length MYB12 se- species in this study. As pink water-soluble pigments quences were amplified by PCR using the primers (for- were detected from L. dauricum and L. bulbiferum, the ward; 5'-ATGTTTCAAACGTTTATTGCCTCCGC-3' anthocyanin pigments in these two species were further and reverse; 5'-CAACTTCGGAATCACTCCAAAG-3' analyzed in detail and their MYB12 genes were se- or 5'-TGTTTACATGGACCTTGCTAT-3') and tepal quenced to understand the origin of the genes that regu- cDNA. The purified PCR products were sequenced late the pink color of flowers in Asiatic hybrid lilies. from both sides. When double peaks were observed in the sequences, the alleles in the samples were inter- Materials and Methods preted as being heterozygous. Subsequently, PCR prod- Wild species of L. dauricum, L. bulbiferum var. ucts were cloned into pGEM-T Easy vector (Promega, bulbiferum, L. maculatum, L. lancifolium, L. callosum, Tokyo, Japan) and sequenced. The nucleotide se- L. leichtlinii, and L. davidii were used in this study. quences were aligned, a neighbor-joining (NJ) tree was L. bulbiferum, L. callosum, and L. davidii plants were constructed, and bootstrap analysis (1000 replicates) derived from the collections at the Yurigahara Park, was performed using the default parameters in Clustal Sapporo, Japan. L. lancifolium bulbs were purchased X version 2.0 (Larkin et al., 2007). from a local market and L. leichtlinii plants were col- Results lected from natural habitats in Hokkaido, Japan. These plants were grown at the experimental farm of Tepal pigments were
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