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ASHS 2024 Annual Conference

 

Phenylalanine Mitigates the Phenotypic Color Variations in Pressed Petals of Petunia hybrida ‘Red Sun’

Authors:
Jing Li College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Zhengtao Huang College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Jing Yang College of Landscape Architecture, Sichuan Agricultural University, Chengdu 611130, China

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Chengcheng Xie College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Qiang Wu College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Xuzixin Zhou College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Abstract

The art of pressed flowers is a method of artistic expression involving the pressing of flowers, leaves, and other plant organs for artistic creative purposes. However, the pressing process often results in color variation of the plant material, which significantly diminishes the quality of artistic works and must be solved using appropriate techniques. During this research, phenylalanine (10 mmol⋅L−1) was used to treat the petals of postharvest Petunia flowers to investigate the impact of phenylalanine on mitigating color variation, and the effect of phenylalanine on inhibiting the color variation of Petunia petals during the pressing process was evaluated by color measurement, physicochemical indices, and gene expression level analyses. Using the CIEL*a*b* color measurements, the samples from the test group had significantly higher brightness (L*) and red coloration (a*) at the final stage (S4) than the control group. In addition, phenylalanine had a significant inhibitory effect on malondialdehyde and superoxide anion accumulations in Petunia petals during pressing and reduced the enzymatic activities of superoxide dismutase, polyphenol oxidase, and catalase. The quantitative reverse-transcription polymerase chain reaction analysis showed that the transcript levels of CHS, DFR, F3′5′H, and UFGT genes in the petals of the treatment group continued to increase during the pressing process, and the transcript levels of key genes in the anthocyanin metabolic pathway of the treated samples were higher than those of the control group at the final stage (S4). These results indicated that phenylalanine can effectively diminish the color variation of Petunia petals in the pressing process, which could serve as a theoretical basis for the development of a comprehensive technology system aimed at preserving the color of pressed horticultural plants.

The art of pressed flowers (APF) refers to a kind of art form that uses pressed dried plants as materials for designing and producing decorative paintings and other botanical products of artistic and practical value. The most obvious feature of APF is not the use of the paintbrush, but the use of the original color, shape, and texture of the plant material itself to create works of art, and the characteristics of the plant material can maintain a natural state for a long time without significant variation in a sealed and dried space (Sprich 1977; Sylvia 1963). However, because of the different phenotypes and internal components of plants, it is inevitable that deformation, mildew, and color variations occur during the plant pressing process, thus directly affecting the ornamental and financial values of artistic works.

Despite the early origins of AFT in European countries, the field still lacks comprehensive and systematic theoretical research, with only a limited portion of existing studies introducing the artistic aspects of AFT and the role of AFT in horticultural therapy (Lee et al. 2007; Nameless 1938; Pallas 2000). In contrast, there have been abundant studies of postharvest preservation of horticultural fruits and vegetables, including mango (Mangifera indica L.), strawberry (Fragaria ×ananassa), loquat [Eriobotrya japonica (Thunb.) Lindl.] and tomato (Solanum lycopersicum L.), and these studies involved the methods and mechanisms of postharvest preservation from physiological, biochemical, and molecular biological perspectives (Changwal et al. 2021; Shah et al. 2023; Virgen-Ortiz et al. 2020; Yuan et al. 2023). There is a limited body of research regarding postharvest applications of ornamental horticultural plants, and the majority of existing studies of ornamental plants have primarily concentrated on genetic breeding and enhancing economic traits, such as color and fragrance (Habibi et al. 2022; Odgerel et al. 2022; Xie et al. 2012; Yu et al. 2022; Zhang et al. 2022a). Among these studies, those of plant color phenotypes were particularly rich and comprehensive. For example, the metabolic pathways and molecular regulatory mechanisms of the three primary classes of pigments in plants (chlorophylls, carotenoids, and anthocyanins) have been thoroughly reported (Arnon 1949; Cazzonelli and Pogson 2010; Sunil and Shetty 2022). In particular, the anthocyanin metabolic pathway consists of a series of enzymes that are encoded by specific genes, such as phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), dihydroflavanol 4-reductase (DFR), flavonoid 3′-hydroxylase (F3′H), and UDP-glucose:flavonoid 3-O-glucosyltransferase (UFGT). PAL is the first and critical step in the metabolism of anthocyanins (Winkel-Shirley, 2001). The metabolism of anthocyanin is subject to regulation by various exogenous substances, and it has been demonstrated that phenylalanine plays a beneficial regulatory role in maintaining postharvest fruit color and freshness by upregulating the expression of PAL (Park et al. 2011). Additionally, the utilization of amino acid treatment on vegetables has been found to decrease the activity of polyphenol oxidase (PPO), effectively impeding the postharvest browning process (Gao et al. 2018).

Petunia serves as a prominent model organism in genetic transformation studies, particularly during the investigation of plant flower color because of its diverse range of color variations (Yue et al. 2018). To investigate the color variation of Petunia petals during the process of flower pressing after harvesting and to find ways to alleviate color variation, the red variety of Petunia ‘Red Sun’ was used as the material during this study, and untreated petals and phenylalanine-treated petals were pressed using a pressed flower toolkit. In this study, the color change pattern and inhibitory effect of phenylalanine on the color variation of Petunia petals during the process of flower pressing were creatively investigated by the CIEL*a*b* color measurements, physiological and biochemical indices, and quantitative reverse-transcription polymerase chain reaction (qRT-PCR) assay. The research can provide a theoretical foundation for the application of APF for postharvest ornamental plants and effectively improve the quality of APF works.

Materials and Methods

Preparation and treatments of samples

Preparation of samples.

The 1-year-old Petunia variety ‘Red Sun’ flowers were sourced from the experimental garden of Yibin Vocational and Technical College (Fig. 1). A total of 50 fresh and consistently sized flowers (∼5 cm in diameter with five petals) were collected. To acquire optimal flatness of the samples for subsequent experiments, the petals were evenly divided into two sections using scissors. Then, the samples were prepared for pretreatment. To mitigate wastage, the surplus pressed petals resulting from the study were gathered and stored within a drought package for subsequent artistic creation.

Fig. 1.
Fig. 1.

Petunia hybrida ‘Red Sun’ used for this study. (A) ‘Red Sun’ plant. (B) Part of the postharvested flowers of ‘Red Sun’. Bar = 5 cm.

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Sample treatments.

The phenylalanine treatment was appropriately adjusted based on the methodology used by a previous study (Sogvar et al. 2020). A portion of the samples underwent treatment with a 10-mmol⋅L−1 phenylalanine solution for a duration of 20 min, whereas the remaining samples, referred to as the control group, were treated with water for the same period. After a thorough immersion process, samples from both groups were carefully dried using absorbent paper, and the stage was subsequently regarded as S1 (0 h). Subsequently, samples were inserted between pressed paper within a pressed flower toolkit (PFT), and the PFT was tightly bound with strings (Fig. 2). During the pressing phase, samples were adopted at 24-h intervals, defined as S2 (24 h), S3 (48 h), and S4 (72 h). A portion of these samples was allocated for phenotypic observation and physicochemical assessments, whereas the remaining portion was rapidly frozen in liquid nitrogen and preserved at −80 °C for subsequent qRT-PCR assays. All assays were conducted with three biological replicates.

Fig. 2.
Fig. 2.

The pressed flower toolkit and its internal structure. The central section can be arranged in multiple layers, with each layer overlapping during the following sequence: drying board–sponge–pressed paper–material–pressed paper–sponge–drying board.

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

CIEL*a*b* coloration determination

To mitigate the substantial error associated with visual color perception, a colorimeter was used to ascertain the precise color of the petal samples and acquire more accurate data. A CM-2600d color analyzer (Konica Minolta, Japan) was used for color digitization. The measurement of ‘Red Sun’ petals was conducted, with each sample being measured at least three times. The CIE color indices L*, a* and b* were used: L* represents brightness, which spanned from 0 to 100, and higher values correspond to more brightness in the sample; a* represents the green (−a*,0) and red (0, + a*) values, with smaller negative values indicating a higher presence of green in the sample and larger positive values indicating a higher presence of red; and similarly, b* represents the yellow (−b*, 0) and blue (0, +b*) values, with smaller negative values indicating a higher presence of yellow and larger positive values indicating a higher presence of blue (McGuire 1992).

Determination of anthocyanin and total flavonoids

The determination of the total anthocyanin content in the samples was conducted using the pH differential method. A 1-g sample mixed with 4.0 mL of 95% acidified ethanol (0.1 mol⋅L−1 HCl) was shaken for 4 h and then centrifuged at 10,000 rpm for 20 min at 4 °C; then, its supernatant was collected. The supernatant was diluted with appropriate buffers for data analysis, and the total anthocyanin content was calculated according to the reference (Lee et al. 2005).

The extraction and detection of total flavonoids were adopted from previous research. One gram of the sample was pulverized at a low temperature and subsequently subjected to a sequential reaction with sodium nitrite, aluminum nitrate, and sodium hydroxide. Then, the resulting supernatant was analyzed using a spectrophotometer to determine the total flavonoid content (Orsavová et al. 2023).

Determination of H2O2, O2•−, and malondialdehyde contents and DPPH scavenging rate

The concentrations of H2O2, O2•−, and malondialdehyde (MDA) were determined and computed using methods outlined by Hasanuzzaman and Fujita (2011). The antioxidant capacity of the samples was evaluated by measuring the DPPH radical scavenging rate (He et al. 2020).

Enzyme activities of superoxide dismutase, catalase, peroxidase, and PPO

A fresh sample of 0.1 g was homogenized using 1 mL of a 0.05 M phosphate buffer (pH 7.8) solution and 3 g of PVP. Subsequently, the resulting mixture was transferred into a 10-mL centrifuge tube containing 7 mL of phosphate buffer and subjected to centrifugation at 4500 rpm for 20 min at a temperature of 4 °C. The resulting supernatant was adjusted to a final volume of 10 mL and used for the detection of enzyme activity according to previous methods.

The methodology described by Abassi et al. (1998) was used to measure superoxide dismutase (SOD) activity. The absorbance of the reaction solution was assessed at a wavelength of 560 nm using a spectrophotometer at 30-second intervals for a duration of 3 min. The resulting SOD activity was expressed in units per gram per minute (U⋅g−1⋅min−1).

The examination of peroxidase (POD) activity was conducted in accordance with the methodology proposed by Lee and Kim (1994). The mixture comprised 10 mM of phosphate-buffered saline, 20 mM guaiacol, 50 mM H2O2, and 10 µL of enzyme extraction. The reaction was initiated by the addition of H2O2, and the absorbance was measured at 470 nm every 30 s for a duration of 3 min. The enzyme activity was quantified as U⋅g−1⋅min−1.

The measurement of catalase (CAT) activity was conducted in accordance with a previously established protocol (Yin et al. 2012). The absorbance of the reaction solution was monitored at a wavelength of 240 nm, with recordings obtained every 30 s over a duration of 3 min. The resulting CAT activity was quantified and expressed as U⋅g−1⋅min−1.

The activity of PPO was assessed by a previous protocol (Maioli et al. 2020). One gram of fresh sample was pulverized using liquid nitrogen and 50 mg of polyvinylpolypyrrolidone. Then, the mixture was resuspended in 4 mL of 0.1 M sodium phosphate buffer at pH 7.2. Subsequently, the samples were subjected to sonication in a water bath for 10 min at a temperature of 20 °C, followed by centrifugation at 12,000 rpm for 15 min at 4 °C. The resulting supernatant was collected for further analysis. The PPO activity was determined at 415 nm and expressed as U⋅g−1⋅min−1.

Total RNA extraction and cDNA synthesis

Total RNA from the samples was isolated using the LABGENE® Plant RNA Extraction Kit. Subsequently, the acquired total RNA was subjected to quality assessment and subsequently converted into complementary DNA (cDNA) through RT using the Evo M-MLV RT Kit (Hunan Accurate Biotechnology Co., Ltd., Hunan, China). The resulting cDNA was then stored at −20 °C.

qPCR analysis of anthocyanin-related genes

Total RNA was subjected to RT using an Evo M-MLV RT for PCR kit (Hunan Accurate Biotechnology Co., Ltd.) to generate first strand cDNA. The qPCR was conducted on a CFX96 real-time PCR detection system (Bio-Rad, Hercules, CA, USA) using a SYBR Green Premix Pro TaqHS qPCR kit (Hunan Accurate Biotechnology Co., Ltd.). The 2−ΔΔCT method was used for quantitative analysis of the relative expression levels (Livak and Schmittgen 2001). The primers used in the assay are shown in Table 1.

Table 1.

Primers used for the quantitative polymerase chain reaction assay.

Table 1.

Statistical data analysis

Statistical analyses were conducted using SPSS 22, and significant differences were assessed at a significance level of P < 0.05 using the t test and Waller-Duncan test. Visual representations of the data were generated using GraphPad Prism version 9.0.

Results

Analysis of phenotypes.

In terms of phenotypic characteristics, the petals within the control group exhibited a notable decline in red pigmentation and assumed a dark purple color at S4. Conversely, the application of phenylalanine to the samples resulted in a significant alleviation of the fading process, manifesting a purplish-red color on the third day compared with the control group (Fig. 3). According to the results of CIEL*a*b*, the L* (brightness) and a* (green–red chroma) values were more responsive to the color variation in Petunia petals. It was observed that the treated group had a lesser decrease in L* and a* values than the control group, and that the L* and a* values of the treated group were 48.62 and 12.94 during the S3 period, which were significantly higher than the values of the control group during the same period. This indicated that the changes in brightness and redness values of Petunia petals treated with phenylalanine decreased during the pressing process.

Fig. 3.
Fig. 3.

Phenotypic observation and measurement of ‘Red Sun’ petals at different stages. (A) Samples of the control group at different stages. (B) Samples of the treatment group at different stages. (C) Variation in the CIEL*a*b* indices of ‘Red Sun’ petals during pressing. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Analysis of anthocyanin and total flavonoids.

The primary determinants of color change in pressed Petunia flowers were alterations of anthocyanins and flavonoids. The decrease in anthocyanin content from S1 to S2 in the phenylalanine-treated pressed flower petals was smaller than that in the control group, and the total anthocyanin content at S4 was 0.763 mg⋅g−1, which was higher than that in the control group (0.605 mg⋅g−1) (Fig. 4). The total flavonoid content of the two groups was significantly reduced during the pressing process, but the total flavonoid content of the treated group was smaller than that of the control group at S4, which indicated that the phenylalanine alleviated the degradation of anthocyanin in Petunia petals but had no significant mitigating effect on flavonoid degradation.

Fig. 4.
Fig. 4.

Changes in the contents of anthocyanins and flavonoids during the pressing process. (A) Variation in the anthocyanin content during the pressing process. (B) Variation in the flavonoid content during the pressing process. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Effect of ROS damage during the pressing process.

The anthocyanin content is affected by reactive oxygen species (ROS), and ROS-related indicators can indirectly reflect the degree of oxidative stress on Petunia petals; therefore, reducing the effects of oxidative stress on Petunia petals is conducive to the maintenance of color phenotypes (Wang et al. 2022). The measured indices showed that Petunia petals treated with phenylalanine accumulated less MDA and superoxide anion. The contents of MDA and superoxide anion in the treated group were 9.026 and 19.51 at S4, which were 0.61- and 0.86-times those of the control group, respectively. The increase in these two indices in the treated group was significantly smaller than that in the control group from S1 to S4, whereas the changes in the scavenging rate of hydrogen peroxide and DPPH did not show any significant difference (Fig. 5). These results indicated that phenylalanine possessed the capacity to alleviate the impact of MDA and superoxide anion on Petunia pressed petals.

Fig. 5.
Fig. 5.

Assessment of indicators related to reactive oxygen species (ROS) oxidative stress. (A) Variation in hydrogen peroxide content during the pressing process. (B) Variation in superoxide anion content during the pressing process. (C) Variation in malondialdehyde (MDA) content during the pressing process. (D) Variation in DPPH radical scavenging activity during the pressing process. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Analysis of enzyme activities of SOD, POD, CAT, and PPO.

The enzymatic activities of SOD, POD, CAT, and PPO have strong associations with the mechanism of browning. According to Fig. 6, the enzyme activities of SOD, CAT, and PPO were significantly lower than those of the control group in the petals treated with phenylalanine at S2 and S3, and the enzyme activities of SOD and PPO were 0.77- and 0.74-times higher than those of the control group at S4. However, the enzyme activity of POD in the treated group increased from S2 and was 2.25-times higher than that of the control group at S4, whereas the POD enzyme activity in the control group continued to decrease. These results showed that phenylalanine inhibited the activities of SOD, CAT, and PPO enzymes and alleviated the decrease in POD enzyme activity during the pressing process, which delayed the browning of Petunia pressed petals.

Fig. 6.
Fig. 6.

Changes in the enzymatic activity of superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and polyphenol oxidase (PPO). (A) Enzymatic activity of SOD. (B) Enzymatic activity of POD. (C) Enzymatic activity of CAT. (D) Enzymatic activity of PPO. Ck, control group. Tr, treatment group. The error bars represent ±SE of the biological replicates. Letters indicate that the values of different stages in the same group have significant differences (P < 0.05). *Significant difference between the values of two groups during the same stage (P < 0.05).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Transcript levels of anthocyanin-related genes.

Changes in anthocyanin content were related to the expression levels of key genes in the anthocyanin biosynthetic pathway, and the transcript levels of key structural genes involved in the anthocyanin synthesis pathway were assessed using qRT-PCR. Based on the analysis of gene expression levels of a group at different stages, with the exception of F3′H, the transcript levels of all the tested genes exhibited higher expression at S4 than at S1 (Fig. 7). Specifically, the gene expression levels of CHI, F3′5′H, DFR, and UFGT displayed a gradual increase from S1 to S4, whereas the expression levels of PAL and F3H declined after reaching peaks at S2. According to gene expression between the two groups at the same stage (Table 2), all genes except CHS exhibited significantly higher expression levels compared with the control group at S4. These results indicated that phenylalanine activated the expression of key genes of the anthocyanin metabolism pathway in Petunia pressed flower petals.

Fig. 7.
Fig. 7.

Changes in gene expression levels of samples in the same group at different stages (S1 as the reference). Ck, control group. Tr, treatment group. The error bars represent ±SE of the biological replicates. Letters indicate that the values of different stages in the same group have significant differences (P < 0.05).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

Table 2.

Fold changes in the expression levels of related genes of control group and treated group during the same stage (control group as the reference).

Table 2.

Discussion

The anthocyanin biosynthetic pathway has been comprehensively elucidated in various model plants and horticultural crops, and phenylalanine has been identified as a crucial precursor in the biosynthesis of anthocyanin and plays a significant role in this process (Aghdam 2019; Perkowski and Warpeha 2019; Yang et al. 2022). Previous studies have used phenylalanine as an exogenous reagent in the treatment of horticultural plants, revealing that exogenous phenylalanine effectively enhanced the accumulation of anthocyanins in fruits (Edahiro et al. 2005; Sogvar et al. 2020). However, the results of the study showed that phenylalanine did not directly increase the anthocyanin content of Petunia ‘Red Sun’ petals during flower pressing, in contrast to the findings of previous studies. In fact, the color change of the epidermis during ripening of horticultural fruits was not caused by a single pigment; instead, it resulted from comprehensive changes in the content and proportion of multiple pigments (Wu et al. 2022). Data regarding the phenotypic color of pressed flower petals and CIEL*a*b* indicated that exogenous phenylalanine reduced the magnitude of changes in a* and L* values of Petunia petals in the treated group, which were redder and brighter than those in the control group, and this suggested that phenylalanine may slow the rate of degradation by facilitating synthesis of anthocyanins as well as the rate of the reaction of dark-colored metabolites in browning. Therefore, the proportions of the two main substances changed, which resulted in better color preservation of the petals in the treatment group.

Anthocyanin belongs to the flavonoid products, produced in a branch of the flavonoid metabolic pathway, and it was believed that there was competition among substrates of the metabolic branch of anthocyanin and the metabolic branches of other flavonoids. The key enzymes of its metabolic branch and the expression of genes had an important impact on the metabolic branch during the competition for upstream substrates (Shimada et al. 2005; Xie et al. 2004). Phenylalanine functioned as the primary reaction substrate and underwent catalysis by key enzymes, including PAL, CHS, CHI, DFR, ANS, and UFGT, resulting in the production of anthocyanins. Another portion of phenylalanine was subjected to catalysis by enzymes within competitive metabolic branches, leading to the formation of colorless flavonoids (Jiang et al. 2020). It can be inferred that exogenous phenylalanine probably resulted in an increase in the quantity of anthocyanin reaction substrates within the petals of Petunia, and this increase subsequently facilitated the generation of a great number of flavonoid reaction products, including anthocyanins, which indirectly slowed the decline in the overall content of anthocyanin (Sogvar et al. 2020). In addition, phenylalanine, as an exogenous factor, can directly regulate the gene expression patterns of key enzymes in metabolic pathways. Previous studies indicated that there was a large number of responsive cis elements in the promoter of genes in the anthocyanin metabolic pathway, including light-responsive elements, low-temperature-responsive elements, methyl jasmonate-responsive elements, salicylic acid-responsive elements, and others, and that the different response elements had the effect of promoting or inhibiting the expression of genes (Zhu et al. 2015). Based on the anthocyanin content, total flavonoid content, and qRT-PCR results of Petunia petals, the promoters of CHI, DFR, and UFGT in the anthocyanin metabolic pathway may contain cis elements responsive to phenylalanine, which were able to positively regulate gene expression and increase the competition of the anthocyanin branch for the upstream substrate (Chen et al. 2023; Yan et al. 2021). Therefore, the reason for the rapid decrease in the total amount of flavonoids in the treated group may be closely related to the increased conversion of intermediates to anthocyanins.

Enzymatic browning refers to the oxidation of phenolic substrates to quinone promoted by PPO, which reacts with amino acids, metal ions, proteins, and other plant constituents to ultimately form dark-colored substances, whereas PPO and POD can promote the conversion of phenolic substrates into black compounds in the presence of ROS (Mayer 2006; Moon et al. 2020; Zhang et al. 2019). The changes in L* and PPO enzymatic activity in this study indicated that phenylalanine was able to mitigate the browning effect of Petunia postharvest petals during pressing, which approximates the results of a previous study in which low concentrations of phenylalanine inhibited browning (Ali et al. 2016). In addition, as nonenzymatic antioxidants and signaling molecules, anthocyanins can alleviate oxidative stress and reduce the overall level of ROS, which further negatively regulates the enzymatic activities of POD, SOD, and CAT (Xu and Rothstein 2018; Xu et al. 2017). In addition, POD also acted as a metabolite catalyzing enzyme located downstream of PAL in the same metabolic pathway (Ko00940) (Fig. 8), and some intermediates were catalyzed to form reaction substrates such as caffeyl alcohol when generating intermediates of anthocyanins, which probably led to the increase in the enzymatic activity of POD (Ramzan et al. 2023; Zhang et al. 2022b). In general, the use of phenylalanine for color preservation of postharvest Petunia petals was feasible, which is innovative in technology of color preservation in APF. However, based on the nascent stage of APF research, a complete technical system has not yet been formed, and further exploration of methods of color preservation in APF is needed.

Fig. 8.
Fig. 8.

Phenylpropanoid pathway (ko00940) in the Kyoto Encyclopedia of Genes and Genomes (KEGG). The purple blocks represent enzymes and corresponding encoding genes, and the red-marked blocks are peroxidase (POD) enzymes and encoding genes (EC 1.11.1.7).

Citation: HortScience 58, 12; 10.21273/HORTSCI17383-23

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  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods. 25(4):408. https://doi.org/10.1006/meth.2001.1262.

    • Search Google Scholar
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  • Maioli A, Gianoglio S, Moglia A, Acquadro A, Valentino D. 2020. Simultaneous CRISPR/Cas9 editing of three PPO genes reduces fruit flesh browning in Solanum melongena L. Front Plant Sci. 11. https://doi.org/10.3389/fpls.2020.607161.

    • Search Google Scholar
    • Export Citation
  • Mayer AM. 2006. Polyphenol oxidases in plants and fungi: Going places? A review. Phytochemistry. 67(21):23182331. https://doi.org/10.1016/j.phytochem.2006.08.006.

    • Search Google Scholar
    • Export Citation
  • McGuire GR. 1992. Reporting of objective color measurements. HortScience. 27(12):12541255. https://doi.org/10.21273/HORTSCI.27.12.1254.

    • Search Google Scholar
    • Export Citation
  • Moon K, Kwon E, Lee B, Kim C. 2020. Recent trends in controlling the enzymatic browning of fruit and vegetable products. Molecules. 25(12):2754. https://doi.org/10.3390/molecules25122754.

    • Search Google Scholar
    • Export Citation
  • Nameless R. 1938. Pressed flower are popular for nature collections. Sci News. 33(26):414415.

  • Odgerel K, Jose J, Karsai-Rektenwald F, Ficzek G, Simon G, Végvári G, Bánfalvi Z. 2022. Effects of the repression of GIGANTEA gene StGI.04 on the potato leaf transcriptome and the anthocyanin content of tuber skin. BMC Plant Biol. 22(1):249. https://doi.org/10.1186/s12870-022-03636-3.

    • Search Google Scholar
    • Export Citation
  • Orsavová J, Juríková T, Bednaříková R, Mlček J. 2023. Total phenolic and total flavonoid content, individual phenolic compounds and antioxidant activity in sweet rowanberry cultivars. Antioxidants (Basel, Switzerland). 12(4):913. https://doi.org/10.3390/antiox12040913.

    • Search Google Scholar
    • Export Citation
  • Pallas B. 2000. Make a pressed flower picture. Woman’s Day. 70(63):13.

  • Park N, Xu H, Li X, Jang I, Park S, Ahn G, Lim Y, Kim S, Park S. 2011. Anthocyanin accumulation and expression of anthocyanin biosynthetic genes in radish (Raphanus sativus). J Agr Food Chem. 59(11):60346039. https://doi.org/10.1021/jf200824c.

    • Search Google Scholar
    • Export Citation
  • Perkowski MC, Warpeha KM. 2019. Review: Phenylalanine roles in the seed-to-seedling stage: Not just an amino acid. Plant Sci. 289:110223. https://doi.org/10.1016/j.plantsci.2019.110223.

    • Search Google Scholar
    • Export Citation
  • Ramzan T, Shahbaz M, Maqsood M, Zulfiqar U, Saman R, Lili N, Irshad M, Maqsood S, Haider A, Shahzad B, Gaafar A, Haider F. 2023. Phenylalanine supply alleviates the drought stress in mustard (Brassica campestris) by modulating plant growth, photosynthesis, and antioxidant defense system. Plant Physiol Biochem. 201:107828. https://doi.org/10.1016/j.plaphy.2023.107828.

    • Search Google Scholar
    • Export Citation
  • Shah H, Khan A, Singh Z, Ayyub S. 2023. Postharvest biology and technology of loquat (Eriobotrya japonica Lindl.). Foods (Basel, Switzerland). 12(6):1329. https://doi.org/10.3390/foods12061329.

    • Search Google Scholar
    • Export Citation
  • Shimada N, Sasaki R, Sato S, Kaneko T, Tabata S, Aoki T, Ayabe S. 2005. A comprehensive analysis of six dihydroflavonol 4-reductases encoded by a gene cluster of the Lotus japonicus genome. J Expt Bot. 56(419):25732585. https://doi.org/10.1093/jxb/eri251.

    • Search Google Scholar
    • Export Citation
  • Sogvar O, Rabiei V, Razavi F, Gohari G. 2020. Phenylalanine alleviates postharvest chilling injury of plum fruit by modulating antioxidant system and enhancing the accumulation of phenolic compounds. Food Technol Biotechnol. 58(4):433444. https://doi.org/10.17113/ftb.58.04.20.6717.

    • Search Google Scholar
    • Export Citation
  • Sprich R. 1977. Pressed flowers/fresh flowers: New directions in psychoanalytic criticism. Colby Quarterly. 13:6772.

  • Sunil L, Shetty N. 2022. Biosynthesis and regulation of anthocyanin pathway genes. Appl Microbiol Biotechnol. 106(5-6):17831798. https://doi.org/10.1007/s00253-022-11835-z.

    • Search Google Scholar
    • Export Citation
  • Sylvia P. 1963. Pressed flower pictures and citrus skin. J R Soc Arts. 111(5081):431.

  • Virgen-Ortiz J, Morales-Ventura J, Colín-Chávez C, Esquivel-Chávez F, Vargas-Arispuro I, Aispuro-Hernández E, Martínez-Téllez M. 2020. Postharvest application of pectic-oligosaccharides on quality attributes, activities of defense-related enzymes, and anthocyanin accumulation in strawberry. J Sci Food Agr. 100(5):19491961. https://doi.org/10.1002/jsfa.10207.

    • Search Google Scholar
    • Export Citation
  • Wang J, Li D, Peng Y, Cai M, Liang Z, Yuan Z, Du X, Wang J, Schnable P, Gu R, Li L. 2022. The anthocyanin accumulation related ZmBZ1, facilitates seedling salinity stress tolerance via ROS scavenging. Int J Mol Sci. 23(24):16123. https://doi.org/10.3390/ijms232416123.

    • Search Google Scholar
    • Export Citation
  • Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126(2):485493. https://doi.org/10.1104/pp.126.2.485.

    • Search Google Scholar
    • Export Citation
  • Wu S, Wu D, Song J, Zhang Y, Tan Q, Yang T, Yang J, Wang J, Xu J, Xu W, Liu A. 2022. Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening. Hortic Res. 9:Uhac102. https://doi.org/10.1093/hr/uhac102.

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    • Export Citation
  • Xie D, Jackson LA, Cooper JD, Ferreira D, Paiva NL. 2004. Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol-4-reductase from Medicago truncatula. Plant Physiol. 134(3):979994. https://doi.org/10.1104/pp.103.030221.

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  • Xie X, Li S, Zhang R, Zhao J, Chen Y, Zhao Q, Yao Y, You C, Zhang X, Hao Y. 2012. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit coloration in response to low temperature in apples. Plant Cell Environ. 35(11):18841897. https://doi.org/10.1111/j.1365-3040.2012.02523.x.

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  • Xu Z, Mahmood K, Rothstein S. 2017. ROS induces anthocyanin production via late biosynthetic genes and anthocyanin deficiency confers the hypersensitivity to ROS-Generating stresses in Arabidopsis. Plant Cell Physiol. 58(8):13641377. https://doi.org/10.1093/pcp/pcx073.

    • Search Google Scholar
    • Export Citation
  • Xu Z, Rothstein S. 2018. ROS-induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis. Plant Signal Behav. 13(3):E1451708. https://doi.org/10.1080/15592324.2018.1451708.

    • Search Google Scholar
    • Export Citation
  • Yan H, Pei X, Zhang H, Li X, Zhang X, Zhao M, Chiang V, Sederoff R, Zhao X. 2021. MYB-mediated regulation of anthocyanin biosynthesis. Int J Mol Sci. 22(6):3103. https://doi.org/10.3390/ijms22063103.

    • Search Google Scholar
    • Export Citation
  • Yang L, Li W, Fu F, Qu J, Sun F, Yu H, Zhang J. 2022. Characterization of phenylalanine ammonia-lyase genes facilitating flavonoid biosynthesis from two species of medicinal plant Anoectochilus. PeerJ. 10:E13614. https://doi.org/10.7717/peerj.13614.

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  • Yin J, Bai S, Wu F, Lu G, Yang H. 2012. Effect of nitric oxide on the activity of phenylalanine ammonia-lyase and antioxidative response in sweetpotato root in relation to wound-healing. Postharvest Biol Technol. 74:125131. https://doi.org/10.1016/j.postharvbio.2012.06.011.

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  • Yu L, Sun Y, Zhang X, Chen M, Wu T, Zhang J, Xing Y, Tian J, Yao Y. 2022. ROS1 promotes low temperature-induced anthocyanin accumulation in apple by demethylating the promoter of anthocyanin-associated genes. Hortic Res. https://doi.org/10.1093/hr/uhac007.

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  • Fig. 1.

    Petunia hybrida ‘Red Sun’ used for this study. (A) ‘Red Sun’ plant. (B) Part of the postharvested flowers of ‘Red Sun’. Bar = 5 cm.

  • Fig. 2.

    The pressed flower toolkit and its internal structure. The central section can be arranged in multiple layers, with each layer overlapping during the following sequence: drying board–sponge–pressed paper–material–pressed paper–sponge–drying board.

  • Fig. 3.

    Phenotypic observation and measurement of ‘Red Sun’ petals at different stages. (A) Samples of the control group at different stages. (B) Samples of the treatment group at different stages. (C) Variation in the CIEL*a*b* indices of ‘Red Sun’ petals during pressing. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

  • Fig. 4.

    Changes in the contents of anthocyanins and flavonoids during the pressing process. (A) Variation in the anthocyanin content during the pressing process. (B) Variation in the flavonoid content during the pressing process. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

  • Fig. 5.

    Assessment of indicators related to reactive oxygen species (ROS) oxidative stress. (A) Variation in hydrogen peroxide content during the pressing process. (B) Variation in superoxide anion content during the pressing process. (C) Variation in malondialdehyde (MDA) content during the pressing process. (D) Variation in DPPH radical scavenging activity during the pressing process. Ck, control group. Tr, treatment group. The error bars represent ±SE of biological replicates. Letters represent significant differences (P < 0.05).

  • Fig. 6.

    Changes in the enzymatic activity of superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and polyphenol oxidase (PPO). (A) Enzymatic activity of SOD. (B) Enzymatic activity of POD. (C) Enzymatic activity of CAT. (D) Enzymatic activity of PPO. Ck, control group. Tr, treatment group. The error bars represent ±SE of the biological replicates. Letters indicate that the values of different stages in the same group have significant differences (P < 0.05). *Significant difference between the values of two groups during the same stage (P < 0.05).

  • Fig. 7.

    Changes in gene expression levels of samples in the same group at different stages (S1 as the reference). Ck, control group. Tr, treatment group. The error bars represent ±SE of the biological replicates. Letters indicate that the values of different stages in the same group have significant differences (P < 0.05).

  • Fig. 8.

    Phenylpropanoid pathway (ko00940) in the Kyoto Encyclopedia of Genes and Genomes (KEGG). The purple blocks represent enzymes and corresponding encoding genes, and the red-marked blocks are peroxidase (POD) enzymes and encoding genes (EC 1.11.1.7).

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    • Search Google Scholar
    • Export Citation
  • Maioli A, Gianoglio S, Moglia A, Acquadro A, Valentino D. 2020. Simultaneous CRISPR/Cas9 editing of three PPO genes reduces fruit flesh browning in Solanum melongena L. Front Plant Sci. 11. https://doi.org/10.3389/fpls.2020.607161.

    • Search Google Scholar
    • Export Citation
  • Mayer AM. 2006. Polyphenol oxidases in plants and fungi: Going places? A review. Phytochemistry. 67(21):23182331. https://doi.org/10.1016/j.phytochem.2006.08.006.

    • Search Google Scholar
    • Export Citation
  • McGuire GR. 1992. Reporting of objective color measurements. HortScience. 27(12):12541255. https://doi.org/10.21273/HORTSCI.27.12.1254.

    • Search Google Scholar
    • Export Citation
  • Moon K, Kwon E, Lee B, Kim C. 2020. Recent trends in controlling the enzymatic browning of fruit and vegetable products. Molecules. 25(12):2754. https://doi.org/10.3390/molecules25122754.

    • Search Google Scholar
    • Export Citation
  • Nameless R. 1938. Pressed flower are popular for nature collections. Sci News. 33(26):414415.

  • Odgerel K, Jose J, Karsai-Rektenwald F, Ficzek G, Simon G, Végvári G, Bánfalvi Z. 2022. Effects of the repression of GIGANTEA gene StGI.04 on the potato leaf transcriptome and the anthocyanin content of tuber skin. BMC Plant Biol. 22(1):249. https://doi.org/10.1186/s12870-022-03636-3.

    • Search Google Scholar
    • Export Citation
  • Orsavová J, Juríková T, Bednaříková R, Mlček J. 2023. Total phenolic and total flavonoid content, individual phenolic compounds and antioxidant activity in sweet rowanberry cultivars. Antioxidants (Basel, Switzerland). 12(4):913. https://doi.org/10.3390/antiox12040913.

    • Search Google Scholar
    • Export Citation
  • Pallas B. 2000. Make a pressed flower picture. Woman’s Day. 70(63):13.

  • Park N, Xu H, Li X, Jang I, Park S, Ahn G, Lim Y, Kim S, Park S. 2011. Anthocyanin accumulation and expression of anthocyanin biosynthetic genes in radish (Raphanus sativus). J Agr Food Chem. 59(11):60346039. https://doi.org/10.1021/jf200824c.

    • Search Google Scholar
    • Export Citation
  • Perkowski MC, Warpeha KM. 2019. Review: Phenylalanine roles in the seed-to-seedling stage: Not just an amino acid. Plant Sci. 289:110223. https://doi.org/10.1016/j.plantsci.2019.110223.

    • Search Google Scholar
    • Export Citation
  • Ramzan T, Shahbaz M, Maqsood M, Zulfiqar U, Saman R, Lili N, Irshad M, Maqsood S, Haider A, Shahzad B, Gaafar A, Haider F. 2023. Phenylalanine supply alleviates the drought stress in mustard (Brassica campestris) by modulating plant growth, photosynthesis, and antioxidant defense system. Plant Physiol Biochem. 201:107828. https://doi.org/10.1016/j.plaphy.2023.107828.

    • Search Google Scholar
    • Export Citation
  • Shah H, Khan A, Singh Z, Ayyub S. 2023. Postharvest biology and technology of loquat (Eriobotrya japonica Lindl.). Foods (Basel, Switzerland). 12(6):1329. https://doi.org/10.3390/foods12061329.

    • Search Google Scholar
    • Export Citation
  • Shimada N, Sasaki R, Sato S, Kaneko T, Tabata S, Aoki T, Ayabe S. 2005. A comprehensive analysis of six dihydroflavonol 4-reductases encoded by a gene cluster of the Lotus japonicus genome. J Expt Bot. 56(419):25732585. https://doi.org/10.1093/jxb/eri251.

    • Search Google Scholar
    • Export Citation
  • Sogvar O, Rabiei V, Razavi F, Gohari G. 2020. Phenylalanine alleviates postharvest chilling injury of plum fruit by modulating antioxidant system and enhancing the accumulation of phenolic compounds. Food Technol Biotechnol. 58(4):433444. https://doi.org/10.17113/ftb.58.04.20.6717.

    • Search Google Scholar
    • Export Citation
  • Sprich R. 1977. Pressed flowers/fresh flowers: New directions in psychoanalytic criticism. Colby Quarterly. 13:6772.

  • Sunil L, Shetty N. 2022. Biosynthesis and regulation of anthocyanin pathway genes. Appl Microbiol Biotechnol. 106(5-6):17831798. https://doi.org/10.1007/s00253-022-11835-z.

    • Search Google Scholar
    • Export Citation
  • Sylvia P. 1963. Pressed flower pictures and citrus skin. J R Soc Arts. 111(5081):431.

  • Virgen-Ortiz J, Morales-Ventura J, Colín-Chávez C, Esquivel-Chávez F, Vargas-Arispuro I, Aispuro-Hernández E, Martínez-Téllez M. 2020. Postharvest application of pectic-oligosaccharides on quality attributes, activities of defense-related enzymes, and anthocyanin accumulation in strawberry. J Sci Food Agr. 100(5):19491961. https://doi.org/10.1002/jsfa.10207.

    • Search Google Scholar
    • Export Citation
  • Wang J, Li D, Peng Y, Cai M, Liang Z, Yuan Z, Du X, Wang J, Schnable P, Gu R, Li L. 2022. The anthocyanin accumulation related ZmBZ1, facilitates seedling salinity stress tolerance via ROS scavenging. Int J Mol Sci. 23(24):16123. https://doi.org/10.3390/ijms232416123.

    • Search Google Scholar
    • Export Citation
  • Winkel-Shirley B. 2001. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126(2):485493. https://doi.org/10.1104/pp.126.2.485.

    • Search Google Scholar
    • Export Citation
  • Wu S, Wu D, Song J, Zhang Y, Tan Q, Yang T, Yang J, Wang J, Xu J, Xu W, Liu A. 2022. Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening. Hortic Res. 9:Uhac102. https://doi.org/10.1093/hr/uhac102.

    • Search Google Scholar
    • Export Citation
  • Xie D, Jackson LA, Cooper JD, Ferreira D, Paiva NL. 2004. Molecular and biochemical analysis of two cDNA clones encoding dihydroflavonol-4-reductase from Medicago truncatula. Plant Physiol. 134(3):979994. https://doi.org/10.1104/pp.103.030221.

    • Search Google Scholar
    • Export Citation
  • Xie X, Li S, Zhang R, Zhao J, Chen Y, Zhao Q, Yao Y, You C, Zhang X, Hao Y. 2012. The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit coloration in response to low temperature in apples. Plant Cell Environ. 35(11):18841897. https://doi.org/10.1111/j.1365-3040.2012.02523.x.

    • Search Google Scholar
    • Export Citation
  • Xu Z, Mahmood K, Rothstein S. 2017. ROS induces anthocyanin production via late biosynthetic genes and anthocyanin deficiency confers the hypersensitivity to ROS-Generating stresses in Arabidopsis. Plant Cell Physiol. 58(8):13641377. https://doi.org/10.1093/pcp/pcx073.

    • Search Google Scholar
    • Export Citation
  • Xu Z, Rothstein S. 2018. ROS-induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis. Plant Signal Behav. 13(3):E1451708. https://doi.org/10.1080/15592324.2018.1451708.

    • Search Google Scholar
    • Export Citation
  • Yan H, Pei X, Zhang H, Li X, Zhang X, Zhao M, Chiang V, Sederoff R, Zhao X. 2021. MYB-mediated regulation of anthocyanin biosynthesis. Int J Mol Sci. 22(6):3103. https://doi.org/10.3390/ijms22063103.

    • Search Google Scholar
    • Export Citation
  • Yang L, Li W, Fu F, Qu J, Sun F, Yu H, Zhang J. 2022. Characterization of phenylalanine ammonia-lyase genes facilitating flavonoid biosynthesis from two species of medicinal plant Anoectochilus. PeerJ. 10:E13614. https://doi.org/10.7717/peerj.13614.

    • Search Google Scholar
    • Export Citation
  • Yin J, Bai S, Wu F, Lu G, Yang H. 2012. Effect of nitric oxide on the activity of phenylalanine ammonia-lyase and antioxidative response in sweetpotato root in relation to wound-healing. Postharvest Biol Technol. 74:125131. https://doi.org/10.1016/j.postharvbio.2012.06.011.

    • Search Google Scholar
    • Export Citation
  • Yu L, Sun Y, Zhang X, Chen M, Wu T, Zhang J, Xing Y, Tian J, Yao Y. 2022. ROS1 promotes low temperature-induced anthocyanin accumulation in apple by demethylating the promoter of anthocyanin-associated genes. Hortic Res. https://doi.org/10.1093/hr/uhac007.

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Jing Li College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Zhengtao Huang College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Jing Yang College of Landscape Architecture, Sichuan Agricultural University, Chengdu 611130, China

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Chengcheng Xie College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Qiang Wu College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Xuzixin Zhou College of Creative Arts and Tourism, Yibin Vocational and Technical College, Yibin 644000, China

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Contributor Notes

This study was funded by the key project of Culture and Tourism Industry Innovation and Entrepreneurship Incubation Center (ybzy20kypt07) and the key cooperation of Culture and Tourism Industry Innovation Science and Technology (ybzy20cxtd04).

We are grateful to the funding projects (ybzy20kypt07 and ybzy20cxtd04) provided by Yibin vocational and technical college. We thank A.J.E. for providing language modifications for this paper.

X.Z. is the corresponding author. E-mail: zhouxuzixin@outlook.com.

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