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Change of Petals' Color and Chemical Components in Oenothera Flowers

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Change of Petals' Color and Chemical Components in Oenothera Flowers molecules Article Change of Petals0 Color and Chemical Components in Oenothera Flowers during Senescence Yada Teppabut 1, Kin-ichi Oyama 2 ID , Tadao Kondo 1 and Kumi Yoshida 1,* 1 Graduate School of Informatics, Nagoya University, Chikusa, Nagoya 464-8601, Japan; [email protected] (Y.T.); [email protected] (T.K.) 2 Research Institute for Materials Science, Nagoya University, Chikusa, Nagoya 464-8602, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-052-789-5638 Academic Editors: Tsukasa Iwashina and Thomas J. Schmidt Received: 26 May 2018; Accepted: 9 July 2018; Published: 12 July 2018 Abstract: Oenothera flower petals change color during senescence. When in full bloom, the flowers of O. tetraptera are white and those of O. laciniata and O. stricta are yellow. However, the colors change to pink and orange, respectively, when the petals fade. We analyzed the flavonoid components in these petals as a function of senescence using HPLC-DAD and LC-MS. In all three species, cyanidin 3-glucoside (Cy3G) was found in faded petals. The content of Cy3G increased in senescence. In full bloom (0 h), no Cy3G was detected in any of the petals. However, after 12 h, the content of Cy3G in O. tetraptera was 0.97 µmol/g fresh weight (FW) and the content of Cy3G in O. laciniata was 1.82 µmol/g FW. Together with anthocyanins, major flavonoid components in petals were identified. Quercitrin was detected in the petals of O. tetraptera and isosalipurposide was found in the petals of O. laciniata and O. stricta. The content of quercitrin did not change during senescence, but the content of isosalipurposide in O. laciniata increased from 3.4 µmol/g FW at 0 h to 4.8 µmol/g FW at 12 h. The color change in all three Oenothera flowers was confirmed to be due to the de novo biosynthesis of Cy3G. Keywords: cyanidin 3-O-glucoside; flower senescence; isosalipurposide; Oenothera; petal color change; quercitrin 1. Introduction Flower color is an important characteristic for plants since it is related to pollination [1–3]. One of the many ways angiosperm plants attract pollinators is floral color changes [2,3]. Various mechanisms of color change have been reported such as changes in pH [4,5] and losses of pigment [6]. However, the most common physiological process is the appearance of a pigment especially an anthocyanin [2]. Anthocyanins provide the widest range of colors among the three major classes of flower pigments: anthocyanins, betalains, and carotenoids [7,8]. Many studies have explored the biosynthesis of these pigments [6–11]. In the case of anthocyanin, it is synthesized from phenylalanine, which is an amino acid, via a phenylpropanoid [10–13]. The pathway starts with the synthesis of naringenin chalcone from 4-coumaroyl-CoA and malonyl-CoA by chalcone synthase (CHS). Afterward, the chalcone is converted into flavanone, dihydroflavonol, and then leucoanthocyanidin [7,8,10,11]. Next, leucoanthocyanidin is oxidized and glycosylated to develop anthocyanin [7,8,10,11,14]. A large number of plant taxa show floral color changes and one of them is genus Oenothera, evening primrose, which is known to undergo a flower color change during senescence. The flowers of this genus bloom in the evening and fade in the morning. When fully opened, the petals of O. tetraptera are white and then they become pink in the morning (Figure1a). Those of O. laciniata as well as O. stricta Molecules 2018, 23, 1698; doi:10.3390/molecules23071698 www.mdpi.com/journal/molecules Molecules 2018, 23, x FOR PEER REVIEW 2 of 8 Molecules 2018, 23, 1698 2 of 8 tetraptera are white and then they become pink in the morning (Figure 1a). Those of O. laciniata as well as O. stricta are yellow and then they turn orange as they fade (Figure 1b,c). These phenomena stronglyare yellow indicate and then that they an turn anthocyanin orange as they is fadebiosynthesized (Figure1b,c). during These phenomena senescence. strongly However, indicate the physiologicalthat an anthocyanin process is of biosynthesized color changes during in Oenothera senescence. has not However, been confirmed. the physiological We investigated process of petal color colorchanges change in Oenothera in thesehas flowers not been and confirmed.studied the We mechanisms investigated of petalsuch colorchanges. change Petal in components these flowers were and isolatedstudied theand mechanisms the constituents of such were changes. identified. Petal Afte componentsrward, the werecomponents isolated were and thequantified constituents according were toidentified. the flower Afterward, fading stage. the components were quantified according to the flower fading stage. Figure 1. FlowerFlower color color change change in inOenotheraOenothera petalspetals during during senescence. senescence. (a) (Oenotheraa) Oenothera tetraptera tetraptera, (b), (Oenotherab) Oenothera laciniata laciniata, and, and (c) Oenothera (c) Oenothera stricta stricta. Scale. Scale bars: bars: 1 cm. 1 cm. 2. Results 2.1. Analysis of Petal Components of O. tetraptera As shown in Figure 11a,a, thethe petalspetals ofof O. tetraptera bloom in white in the the evening evening at at approximately approximately 21:00 and become pink after 12 h. To determine the chemical compounds responsible for the color change, thethe petalspetals of ofO. O. tetraptera tetrapterawere were collected collected at aat full a full blooming blooming white white stage stage (0 h) (0 and h) theand faded the faded stage (12stage h). (12 Then h). theThen petals the petals were extractedwere extracte withd acidic with solutionacidic solution (3% TFA (3% in TFA 50% CHin 50%3CN CH aq.).3CN Each aq.). extract Each wasextract analyzed was analyzed by 3D-HPLC by 3D-HPLC (Figure (Figure2). In the 2). white In the petals white at petals 0 h, 2atwas 0 h, the2 was major the component.major component. In the pinkIn the petals, pink petals, which which had undergonehad undergone senescence, senescence, peak peak1 appeared. 1 appeared. Combined Combined with withthe the resultsresults of co-chromatography and the spectrum obtained from 3D-HPLC and LC-MS analysis (Figure S1) using an authentic authentic sample, sample, 1 1waswas identified identified to tobe becyanidin cyanidin 3-glucoside 3-glucoside (Cy3G, (Cy3G, Figure Figure 3) [15].3)[ Using15]. Using the same the procedure,same procedure, 2 was2 determinedwas determined to be quercitrin to be quercitrin (quercetin (quercetin 3-rhamnoside, 3-rhamnoside, Figure Figure 3, and3, Figure and Figure S1). This S1). Thisresult result revealed revealed that the that red the color red color change change is due is to due the to appearance the appearance of Cy3G of Cy3G during during senescence. senescence. Since the components in O. tetraptera petals were identified, identified, quantitative analysis analysis of of Cy3G Cy3G ( (11)) and quercitrin ( 2) during senescence was carried out. The The pe petalstals at at 0 0 h, h, 4 4 h, h, 7 7 h, h, and and 12 h after blooming were collected (Figure(Figure4 4a)a) and and their their reflection reflection spectra spectra were were recorded recorded (Figure (Figure4b). 4b). The Theλ λvismaxvismax of the colored petals waswas 541541 nmnm atat eacheach stagestage andand thethe intensityintensity atatλ λvismaxvismax increased during flower flower development (Figure (Figure 44b).b). This This corresponded corresponded with with the the L*L value* value of ofthe the CIELAB CIELAB color color coordinate coordinate of the of petalsthe petals decreasing decreasing and and the thea* valuea* value increasing increasing after after blooming blooming (Table (Table 1).1). In In addition, addition, the the pH ofof thethe pressed juicejuice waswas measuredmeasured andand no no obvious obvious changes changes in in pH pH were were observed observed during during senescence senescence (Table (Table1). This1). This indicates indicates that that the the color color change change was was not duenot du to ae pHto a changepH change in the in petals. the petals. When When extraction extraction from fromeach petaleach petal was followedwas followed by HPLC by HPLC analysis, analysis, the changesthe changes in the in contentthe content of Cy3G of Cy3G (1) and(1) and quercitrin quercitrin (2) were(2) were quantified quantified (Figure (Figure4c,d). The4c,d). content The content of Cy3G of increased Cy3G increased during flower during senescence flower senescence and reached and its MoleculesMolecules 20182018, 23, 23, x, 1698FOR PEER REVIEW 3 of3 of 8 8 Molecules 2018, 23, x FOR PEER REVIEW 3 of 8 reached its highest level (0.97 µmol/g FW) 12 h after blooming (Figure 4c). In contrast, the content of reached its highest level (0.97 µmol/g FW) 12 h after blooming (Figure 4c). In contrast, the content of quercitrinhighest level (2) at (0.97 0 h afterµmol/g blooming FW) 12 was h after 13.86 blooming µmol/g FW, (Figure which4c). is In approximately contrast, the content 14 times of more quercitrin than quercitrin (2) at 0 h after blooming was 13.86 µmol/g FW, which is approximately 14 times more than the(2 )highest at 0 h after level blooming of Cy3G. was The 13.86 contentµmol/g did not FW, sign whichificantly is approximately change during 14 timessenescence more than(Figure the 4d). highest levelthe highest of Cy3G. level The of contentCy3G. The did content not significantly did not sign changeificantly during change senescence during (Figuresenescence4d). (Figure 4d). FigureFigure 2. 2.HPLC chromatograms of the extracts of the petals of O. tetrapteraO. tetraptera. (a) Whitea petals at 0 h. (b) Figure 2. HPLCHPLC chromatograms chromatograms of of the the extracts extracts of of the the petals petals of ofO. tetraptera. (a.() White) White petals petals at 0 at h. 0(b h.) Pink(b) Pinkpetals petals at 12 ath. 12 h. Pink petals at 12 h.
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