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A Novel R2R3-MYB Transcription Factor Contributes to Petal Blotch

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A Novel R2R3-MYB Transcription Factor Contributes to Petal Blotch A Novel R2R3-MYB Transcription Factor Contributes to Petal Blotch Formation by Regulating Organ-Specific Expression of PsCHS in Tree Peony (Paeonia suffruticosa) 1 1,2 3 4 5 1,2 1,2 Zhaoyu Gu , Jin Zhu , Qing Hao , Yao-Wu Yuan , Yuan-Wen Duan , Siqi Men , Qianyu Wang , Regular Paper 6 1 1, 1,2, Qinzheng Hou , Zheng-An Liu , Qingyan Shu * and Liangsheng Wang * Downloaded from https://academic.oup.com/pcp/article-abstract/60/3/599/5215161 by University of Connecticut user on 27 March 2019 1Key Laboratory of Plant Resources/Beijing Botanical Garden, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China 2University of Chinese Academy of Sciences, Beijing 100049, China 3College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao, Shandong 266109, China 4Department of Ecology & Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA 5The Germplasm Bank of Wild Species, Kunming Institute of Botany, the Chinese Academy of Sciences, Kunming, Yunnan 650201, China 6College of Life Science, Northwest Normal University, Lanzhou, Gansu 730070, China *Corresponding authors: Liangsheng Wang, E-mail, [email protected]; Qingyan Shu, E-mail, [email protected]. (Received August 13, 2018; Accepted November 24, 2018) Flower color patterns play critical roles in plant–pollinator such as stripes, blotches, spots or more complex designs, are interactions and represent one of the most common adap- unique characteristics of angiosperms, as observed for example tations during angiosperm evolution. However, the molecu- in Asteraceae (e.g. Gorteria diffusa ‘Soeb’), Liliaceae (e.g. lar mechanisms underlying flower color pattern formation Nomocharis meleagrina), Linderniaceae (e.g. Torenia fournieri), are less understood in non-model organisms. The aim of this Iridaceae (e.g. Sparaxis elegans), Orchidaceae (e.g. Dendrobium study was to identify genes involved in the formation of nobile) and Paeoniaceae (e.g. Paeonia rockii) (Thomas et al. petal blotches in tree peony (Paeonia suffruticosa) through 2009, Gao et al. 2015, Zhang et al. 2015, Su et al. 2017). These transcriptome profiling and functional experiments. We patterns represent adaptations in the evolution of specialized identified an R2R3-MYB gene, PsMYB12, representing a dis- plant–pollinator interactions (H. Yuan et al. 2014, Zhang et al. tinct R2R3-MYB subgroup, with a spatiotemporal expression 2015). pattern tightly associated with petal blotch development. The formation of floral pigment patterns depends on the We further demonstrated that PsMYB12 interacts with a differential activation of pigment biosynthetic genes in devel- basic helix–loop–helix (bHLH) and a WD40 protein in a opmentally similar neighboring epidermal cells (Davies et al. regulatory complex that directly activates PsCHS expression, 2012). The anthocyanin pigments confer red, blue, pink or which is also specific to the petal blotches. Together, these purple colors, and the anthocyanin biosynthetic pathway findings advance our understanding of the molecular mech- (ABP) has been extensively studied in various plant species anisms of pigment pattern formation beyond model plants. (Grotewold 2006, Carbone et al. 2009, Schaart et al. 2013, Hsu They also benefit molecular breeding of tree peony cultivars et al. 2015). Anthocyanin biosynthesis starts with a condensa- with novel color patterns and promote germplasm tion of malonyl-CoA and 4-coumaroyl CoA into chalcone com- innovation. pounds, catalyzed by the enzyme chalcone synthase (CHS). Chalcones are then converted into dihydroflavonols by a Keywords: Anthocyanin patterning Chalcone synthase series of enzymes including chalcone isomerase (CHI), flava- Petal blotch PsMYB12 Transcriptional regulation Tree none 3-hydroxylase (F3H), flavonoid 3’-hydroxylase (F3’H) peony. and flavonoid 3’,5’-hydroxylase (F3’5’H), which together consti- tute the early ABP (Grotewold 2006, Petroni and Tonelli 2011). Introduction Finally, consecutive reactions catalyzed by dihydroflavonol 4- reductase (DFR) and leucoanthocyanindin dioxygenase (LDOX; Flower colors provide important visual signals in plant–pollin- anthocyanin synthase, ANS) yield colored anthocyanidins, ator communications (Davies et al. 2012, Glover 2014), and which are further methylated and/or glycosylated to form vari- changes in flower color may cause pollinator shifts, which in ous species-specific anthocyanins by enzymes such as UDP fla- turn lead to reproductive isolation and speciation (Bradshaw vonoid glucosyltransferase (UFGT) and flavonoid O- and Schemske 2003, Zufall and Rauscher 2004, Heuschen et al. methyltransferase (FOMT) (Holton and Cornish 1995). DFR, 2005, Koes et al. 2005, Hoballah et al. 2007, H. Yuan et al. 2014, ANS, UFGT and FOMT are all considered components of the Jones 1996). As such, flower color is considered a major factor late biosynthetic pathway (Winkel-Shirley 2001, Grotewold contributing to the large angiosperm diversity observed today 2006, Tanaka et al. 2008, Ma et al. 2009). All these key ABP (Glover 2014). In addition, contrasting flower color patterns, structural genes could be regulated by various R2R3-MYB Plant Cell Physiol. 60(3): 599–611 (2019) doi:10.1093/pcp/pcy232, Advance Access publication on 28 November 2018, available online at www.pcp.oxfordjournals.org ! The Author(s) 2018. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: [email protected] Z. Gu et al. | A novel R2R3-MYB transcription factor transcription factors or the conserved MYB–basic helix–loop– protein, which could activate the promoter of PsCHS. helix (bHLH)–WD40 (MBW) protein complex (Hichri et al. Significantly, this new R2R3-MYB subgroup is widely distribu- 2011, Petroni and Tonelli 2011, Schaart et al. 2013). Distinct ted among eudicots and is distinct from subgroups 5, 6 and 7, spatiotemporal expression patterns of the ABP structural the known transcriptional activators of CHS in other species genes or/and their transcriptional regulators have been impli- (Stracke et al. 2001, Stracke et al. 2007). It is also the first time cated in floral anthocyanin patterning in various fast-growing that a tree peony MBW complex has been reported. These herbaceous plants, including Clarkia gracilis, snapdragon findings not only enrich our understanding of anthocyanin pat- (Antirrhinum spp.), monkeyflowers (Mimulus spp.), Asiatic terning in angiosperms, but also benefit germplasm innovation Downloaded from https://academic.oup.com/pcp/article-abstract/60/3/599/5215161 by University of Connecticut user on 27 March 2019 hybrid lilies (Lilium spp.), Petunia hybrids and Phalaenopsis of important horticultural species. spp. (Quattrocchio et al. 2006, Schwinn et al. 2006, Martin and Glover 2007, Albert et al. 2011, Shang et al. 2011, Glover et al. 2013, Yamagishi et al. 2014, H. Yuan et al. 2014, Hsu et al. Results 2015). These studies have paved the way for exploring the Petal blotch coloration during flower mechanisms of floral anthocyanin patterning in important development horticultural plants that are relatively slow growing and experi- mentally challenging. To investigate the mechanism of petal blotch formation in tree Tree peony (Paeonia suffruticosa Andrew), a perennial de- peony, the representative cultivar ‘Qing Hai Hu Yin Bo’ was ciduous shrub, is one of the most culturally important horti- used. During its petal development, four readily recognizable cultural plants in China, with an industry worth an estimated stages of petal and blotch coloration were determined US$3.8 billion. Tree peony has been cultivated as an ornamental (Fig. 1A). At S1 (20 d before anthesis), petals were yellow- plant in China for >2,000 years. Because of its large, fragrant green without blotches. Bright purple or red blotches appeared and colorful flowers, tree peony was crowned the ‘King of flow- at the base of the yellow-green petals in S2 flowers (10 d before ers’ in the Chinese Tang Dynasty, symbolizing happiness and anthesis). At S3 (4 d before anthesis), blotches grew and their prosperity (Zhou et al. 2014), and has been highlighted in nu- color deepened with more pigment accumulation, and the merous ancient paintings and poems. There are >2,000 tree non-blotched part turned from yellow-green to white-pink. peony cultivars worldwide (e.g. ‘HighNoon’ and ‘Golden Isles’ At anthesis (S4), blotches did not change in color; however, from the USA, ‘Alice Harding’ and ‘Souvenir de Maxime Cornu’ the non-blotched areas turned completely white. from France, ‘Hohki’ and ‘Shimane Seidai’ from Japan) and We quantified anthocyanin levels in the blotched and non- >1,000 modern cultivars in China alone (Zhou et al. 2014). blotched petal areas during the S1 to S4 transition, and only Some cultivars produce flowers with purple petal blotches, found anthocyanin accumulation in the blotches. Four antho- enhancing their ornamental value (Wang et al. 2000). These cyanin types were identified: cyanidin-3-O-glucoside (Cy3G), anthocyanin-pigmented blotches are usually >3 mm in diam- cyanidin-3,5-di-O-glucoside (Cy3G5G), peonidin-3-O-glucoside eter; smaller pigment patches are often referred to as ‘spots’ (Pn3G) and peonidin-3,5-di-O-glucoside (Pn3G5G) (Fig. 1B). (Zhang et al. 2007, Yamagishi 2011). Total anthocyanin abundance started to increase in the –1 Previously, we reported the anthocyanin composition of the blotch portion of the petal at S2 (0.29 ± 0.00 mg g ) and S3 –1 –1 petal blotches of 35 tree peony cultivars and showed
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