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Article

Genotype and Organ-Specific Variability in Antioxidant Capacities as Well as Polyamine and Osmolyte Levels in Eleven Lisianthus (Eustoma grandiflorum Raf.) Cultivars with Different Flowering Periods

by
Vanja Vuksanović
1,
Marko Kebert
2,
Lazar Pavlović
1,*,
Lazar Kesić
2,
Milena Rašeta
3,
Branislav Kovačević
2 and
Saša Orlović
1,2
1
Faculty of Agriculture, University of Novi Sad, Trg Dositeja Obradovića 8, 21000 Novi Sad, Serbia
2
Institute of Lowland Forestry and Environment, University of Novi Sad, Antona Čehova 13d, 21000 Novi Sad, Serbia
3
Department of Chemistry, Biochemistry, and Environmental Protection, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 3, 21000 Novi Sad, Serbia
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(11), 1193; https://doi.org/10.3390/horticulturae10111193
Submission received: 26 September 2024 / Revised: 21 October 2024 / Accepted: 23 October 2024 / Published: 13 November 2024
(This article belongs to the Special Issue New Insights into Stress Physiology and Resistance Regulation in Horticultural Plants)
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Versions Notes

Abstract

:
Lisianthus (Eustoma grandiflorum Raf. Shinn.) is a valued plant known for its diverse flower colors and long vase life. Despite considerable research on the physiological roles of osmolytes, polyamines, and phenolic compounds, there is a lack of understanding regarding their specific accumulation patterns across various lisianthus cultivars and organs. This study aims to compare eleven lisianthus cultivars with varying flowering periods according to their accumulation of osmolytes, polyamines, phenolic content, and antioxidant capacities and measure their resistance to abiotic stress factors. High-performance liquid chromatography coupled with fluorescent detection was employed to quantify putrescine (PUT), spermidine (SPD), and spermine (SPM). In addition, proline (PRO), glycine betaine (GB), antioxidant capacities, phenolic content, and flavonoid contents were assessed spectrophotometrically. This comprehensive analysis allowed for a detailed understanding of the biochemical markers. The result indicates a significant genotype and organ-dependent variation in accumulation patterns of inspected metabolites and antioxidant activities. The petals of Rosita Green exhibited the highest levels of phenols and flavonoids, whereas the petals of Rosita Blue Picote demonstrated the highest concentrations of osmolytes. Polyamines were found to be more concentrated in the petals than in the leaves. The average values indicated high levels of polyamines in the Mariachi Carmine (PUT 186.72 nmol g−1 DW) and Mariachi Pink (SPD 227.4 nmol g−1 DW) cultivars. These findings underscore the significance of inspected compounds in stress tolerance among cultivars with different flowering periods, providing insights for optimizing cultivation strategies for lisianthus.

Graphical Abstract

1. Introduction

Lisianthus (Eustoma grandiflorum (Raf.) Shinn.) is an ornamental plant that has gained significant commercial importance in recent years due to its wide range of colors, including the rare and valued blue color, its long vase life, and its diverse flowering periods [1]. This plant species has captured the attention of horticulturists, florists, and researchers alike, as it offers a unique combination of aesthetic appeal and adaptability to various growing conditions. As the demand for lisianthus continues to rise in the global flower market, optimizing cultivation practices and breeding programs to ensure a consistent supply of high-quality cut flowers becomes increasingly important [2].
Lisianthus is native to the prairies of the United States, including northern Mexico, Texas, Oklahoma, Kansas, Nebraska, Colorado, Wyoming, and South Dakota, and is commonly referred to as “Texas bluebell”, “prairie rose”, and “prairie gentian”. Although it has long been present in its natural habitat, its cultivation in horticulture is relatively recent [3]. The first hybrids of lisianthus were developed in America in the early 1980s, marking the beginning of its commercial cultivation [3]. Lisianthus quickly gained popularity despite being a new crop compared to traditional cut flowers like roses, chrysanthemums, and tulips. Its cultivation began in Japan in 1933, marking the start of its journey to global recognition, and today, it stands as one of the most popular cut flowers worldwide [4]. In Europe, lisianthus is among the top ten most in-demand flowers, reflecting its rapid establishment in the market [5]. The plant’s adaptability to various environmental stresses, including drought, salinity, and extreme temperatures, is a significant factor contributing to its successful cultivation [6]. This adaptability is largely attributed to the accumulation of specific organic compounds known as osmolytes, such as proline (PRO), glycine betaine (GB), and various polyamines (PAs), that play an important role maintaining cellular homeostasis and protecting cellular structures under stress conditions [7]. PAs, in addition to their role as antioxidants and osmolytes, are important plant growth regulators that are involved in a wide range of physiological processes, including cell division, flower development, embryogenesis, organogenesis senescence, and fruit maturation and development [8], as well as responses to abiotic and biotic stress and mitigation of oxidative stress through the modulation of various antioxidant enzymes [7,9].
To ensure plant survival, the antioxidant system must function effectively to balance the production and scavenging of reactive oxygen species (ROS) [10]. PAs such as PUT, SPM, and SPD inhibit the biosynthesis and action of ethylene in plants, making them crucial for delaying the senescence process [9]. For example, studies have shown that PAs can enhance the post-harvest quality of flowers by increasing the activity of antioxidant enzymes and reducing damage caused by ROS [11]. Previous studies have demonstrated the importance of osmolytes and PAs in the stress tolerance and flowering regulation of various plant species [12]. PAs have been linked to the regulation of flowering time in several plant species, suggesting their potential role in the diverse flowering characteristics observed in lisianthus cultivars [13]. They are thought to act similarly to hormones by delaying aging processes and enhancing tolerance to stress, including drought. PAs achieve this by stabilizing cell membranes, protecting proteins from degradation, and scavenging free radicals to mitigate oxidative damage in aging tissues [14]. When combined with anti-senescence regulators such as nitric oxide (NO) and various plant hormones—including ethylene, abscisic acid, and jasmonic acid—PAs offer a more comprehensive mechanism for controlling senescence. Research suggests that PAs influence processes like programmed cell death and the plant’s response to oxidative stress, ultimately helping plants cope with adverse environmental conditions [15,16]. Understanding the interplay between PAs and these hormones provides valuable insights into how plants regulate senescence under stress conditions. For example, research on gerbera cut flowers has demonstrated that treatments with SPM and γ-aminobutyric acid (GABA) significantly prolong vase life and improve qualitative features by enhancing antioxidant capacities and reducing physiological disorders such as neck bending [17]. Similarly, studies on roses [7] have highlighted the importance of these osmolytes in stress tolerance, underscoring their potential as suitable biomarkers for the selection of stress-resilient cultivars. Piri [11] investigated the impact of various concentrations of salicylic acid, SPD, and sodium nitroprusside on the longevity and post-harvest characteristics of lisianthus cut flowers, concluding that all three compounds had positive effects on inspected properties compared to the control. Rabnawaz et al. [18] found that GB seed priming significantly enhanced the growth and floral quality of carnations compared to untreated seeds.
Estimations of other biochemical markers such as total polyphenols, flavonoids, and antioxidant capacities have been measured by different chromophores such as DPPH, and ABTS assays have been used to assess the stress tolerance and adaptation of plants to various environmental conditions [19]. For example, in Gerbera jamesonii, salinity-induced oxidative stress was shown to affect the activation of multiple antioxidative defense systems, highlighting the importance of antioxidant defense in plant survival and adaptability to stressful conditions [20]. Despite the growing body of knowledge on the physiological functions of osmolytes, PAs, phenols, and other compounds with antioxidant properties, the specific variations in the accumulation patterns of these biochemical markers across different lisianthus cultivars and organs remain largely unexplored. This study aims to investigate the patterns of osmolyte and PA accumulation, as well as phenolic and flavonoid content and antioxidant capacities, in eleven distinct lisianthus cultivars with varying flowering periods. The findings of this study will establish the link between osmolyte and PA accumulation patterns and variability in lisianthus cultivars’ adaptability to environmental stresses and their difference in flowering periods, which can provide valuable insights for optimizing cultivation techniques and breeding strategies.
i.
To achieve that, we have quantified the concentrations of osmolytes (proline (PRO) and glycine betaine (GB)), PAs, phenols, and flavonoids in eleven different lisianthus cultivars with varying flowering periods, at leaf and petal levels.
ii.
We also assessed the antioxidant capacities of lisianthus cultivar extracts by using FRAP (ferric reducing antioxidant power), DPPH (2,2-diphenyl-1-picrylhydrazyl), and ABTS (2,2′-azino-bis-(3-ethylbenzothiazoline-6-sulfonic) acid) assays to establish the correlation between specific metabolites and total antioxidant capacities.

2. Materials and Methods

2.1. Plant Material and Sample Preparation

Eleven cultivars of lisianthus (Eustoma grandiflorum) with different flower colors and flowering times were selected for this study. Additional characteristics of the selected cultivars, including flower color and flowering time, are presented in Table 1.
Lisianthus seedlings of the cultivars Mariachi, Croma, Alissa, Arena, Rosanne, and Rosita were purchased from the company Van Egmond Lisianthus (Rijnsburg, The Netherlands) and transplanted at the 4–6 leaf stage in March 2023. Plants were grown under semi-controlled conditions (temperature 22–25 °C) in a greenhouse at a registered family farm in Central Serbia (geographic coordinates: 43°58′37″ N, 21°15′40″ E). Watering and fertilization were performed according to standard lisianthus cultivation practices in Serbia. Drip irrigation was used for watering, while fertilization was carried out every seven days using calcium-based fertilizers. Each cultivar comprised 100 seedlings, spaced 10 cm apart with rows 1 m apart.
During the flowering period of each cultivar, leaf and flower samples were collected separately using a completely randomized sampling method. For each cultivar, thirty leaves and petals were harvested from different plants to constitute one replicate, and a total of three replicates were obtained. All samples were immediately frozen in liquid nitrogen and then stored at −80 °C for later analysis. Subsequent steps involved freeze drying (by using lyophilizer for 24 h at −70 °C (modelAlpha 1-2 LDplus, Martin Christ, Osterode am Harz, Germany)).

2.2. Quantification of Polyamines (PAs) by High-Performance Liquid Chromatography

About 20 mg of lyophilized plant material (petal and leaf) (dry weight—DW) was extracted using 2 mL of 4% perchloric acid (v/v) solution. After cooling the resulting homogenate on ice for 1 h, it was centrifuged at 15,000× g for 30 min. Supernatants, along with standard solutions of PUT, SPD, and SPM, underwent a dansylation process following the method described by Scaramagli et al. [21] and Biondi et al. [22]. The resulting dansylated derivatives were then extracted with toluene, dried, and reconstituted in acetonitrile. PAs were separated and quantified using high-performance liquid chromatography (HPLC) with fluorescent detection (FD) (Nexera XR, Shimadzu, Kyoto, Japan), employing a reverse-phase C18 column (Spherisorb ODS, 2.5 μm particle diameter, 4.6 × 250 mm, Waters, Wexford, Ireland) and a programmed acetonitrile–water gradient [22,23]. The quantification results of PAs were expressed as nmol per gram of dry weight (nmol g−1 DW).

2.3. Spectrophotometric Quantification of Proline (PRO) and Glycine Betaine (GB)

(a)
Proline Content Determination: In 25 mg of freeze-dried plant material (particularly the petals and leaves), 2 mL of sulfosalicylic acid (3% w/v) was added. After centrifugation at 4000 rpm for 20 min, 0.7 mL of the supernatant was added to 0.7 mL of acid ninhydrin solution (2.5% ninhydrin in glacial acetic acid-distilled water and 85% orthophosphoric acid in a 6:3:1 ratio) and 0.7 mL of glacial acetic acid, then heated at 95 °C for 1 h. After heating, the tubes were placed in an ice bath to stop the reaction. The pinkish-colored compound resulting from the reaction of PRO and ninhydrin was extracted with 1 mL of toluene by vigorous vortexing. When the layers separated and the solution reached room temperature, the PRO concentration was determined spectrophotometrically at 520 nm using the MultiScan GO (ThermoScientific, Bremen, Germany) according to the method previously described by Bates et al. [23] The concentration of free PRO was determined using a standard calibration curve and expressed as micromoles per gram of dry weight (μmol g−1 DW).
(b)
Determination of Glycine Betaine Content: In 25 mg of freeze-dried plant material, 1 mL of 1M H2SO4 was added with vigorous vortexing. The extraction continued in an ultrasonic bath for 10 min. After extraction, the samples were centrifuged at 13,200 rpm at 4 °C for 30 min. Following centrifugation, 500 μL of the supernatant was combined with 200 μL of KI/I2, and the solution was left for 16 h at 4 °C. After a second centrifugation under the same conditions, QAC–periodide crystals in the sediment were dissolved in 2 mL of 1,2-dichloroethane using an ultrasonic bath. The absorbance of the mixture was measured at a wavelength of 365 nm using a MultiScan GO spectrophotometer (Thermo Scientific, Bremen, Germany). GB concentration was determined from a standard calibration curve, and the GB content was expressed as µmol g−1 DW [24].

2.4. Evaluation of Lisianthus Petal and Leaf Antioxidant Capacities

Extract preparation: The antioxidant capacity was assessed using 80% methanol (MeOH) extracts from 1 L of different cultivars of lisianthus. Approximately 20 mg of freeze-dried plant material, including petals and leaves separately, was macerated with 2 mL of 80% MeOH using a magnetic stirrer (MS-3000 High-speed magnetic stirrer, Biosan, Riga, Latvia) for 20 min. Subsequently, the mixture underwent centrifugation at 4 °C for 30 min (Microcentrifuge 5424 R, Eppendorf, Germany). The resulting extracts were then analyzed. The absorbances of the mixture were measured using the MultiScan GO (ThermoScientific, Bremen, Germany).
The ferric reducing antioxidant power (FRAP) was assessed spectrophotometrically following the method outlined by Benzie and Strain [25]. In brief, 225 μL of FRAP reagent, prepared by mixing acetate buffer, TPTZ solution, and FeCl3 × H2O in a 10:1:1 ratio, was added to 20 μL of methanol extract. A standard curve using ascorbic acid (AS) was constructed for quantification, and the results were expressed as mg of ascorbic acid equivalent per gram of dry weight (mg AAE g−1 DW).
For the determination of antioxidant activities including DPPH (2,2-diphenyl-2-picrylhydrazyl) activity and ABTS (2,2′-azinobis-(3-ethylbenzothiazoline-6-sulfonic acid)) assay, methods described by Miller and Rice-Evans [26], respectively, were used. The results were reported as percentages of radical scavenging capacity (RSC), representing the percentage of radical species neutralized by antioxidants present in the flower and leaf extract. Radical scavenger capacity against DPPH and ABTS radicals was calculated using a standard curve and expressed as mmol of Trolox equivalents per gram of dry weight of plant material (mM TE g−1 DW).

2.5. Total Phenolic and Flavonoid Content Qunatification

The total phenolic content (TPC) was determined spectrophotometrically using the Folin–Ciocalteu reagent method as described by Kim et al. [27], with gallic acid as the standard. In brief, 25 µL of methanol extract samples was added to a microplate, followed by the addition of 125 μL of 0.1 mol/L Folin–Ciocalteu’s reagent and 100 μL of 7.5% (w/v) Na2CO3. The results were expressed as mg of gallic acid equivalent (GAE) per gram of dry weight (mg GAE g−1 DW).
The total flavonoid content (TFC) was determined using a spectrophotometric method detailed by Chang et al. [28]. To measure TFC, 30 μL of methanol extract was mixed with 90 μL of methanol (MeOH), 6 μL of 1 M sodium acetate (NaCH3COO), 6 μL of 10% w/v aluminum chloride (AlCl3), and 150 μL of distilled water. A calibration curve was generated using the absorbance of known concentrations of quercetin for quantifying total flavonoids, and the results were expressed as mg of quercetin equivalent per gram of dry weight (mg QE g−1 DW).

2.6. Statistical Data Analysis

Obtained results were processed by the two-way factor analysis of variance, and the significance of the difference between individual organs, cultivars, and their interactions was tested by Tukey’s honestly significant difference test (HSD test) for a significance level of p = 0.05. The relationship between the investigated parameters was described using the Pearson correlation coefficient and principal component analysis (PCA). A correlation matrix was used for data entry in the principal component analysis, and the relationship between the traits was analyzed based on their loadings with the first two principal components. The STATISTICA 13 (13.3.721) software package [29] was used for data processing. For the visualization of data, R packages ggplot2 (3.5.1.) [30] and corrplot (0.95) [31] were used.

3. Results

3.1. Variability in Total Phenolic and Flavonoid Contents Among Lisianthus Cultivars

The total phenolic content (TPC) varied significantly between different cultivars and organs (Figure 1A). The highest TPC was recorded in the petals of the Rosita Green cultivar (14.3 mg. GAE g−1 DW), while the lowest TPC was in the leaves of the Mariachi Pink Picote cultivar (2.6 mg GAE g−1 DW). On average, petals had higher TPC than leaves, with petals being three times richer in phenols than leaves.
Total flavonoid content (TFC) also showed significant differences between cultivars and organs (Figure 1B). For example, in total, the content of flavonoids was 56% lower in the leaves compared to the petals. The highest content of flavonoids was recorded in the petals of the cultivars Croma Yellow (26.3 mg QE g−1 DW), Mariachi Blue (25.83 QE g−1 DW), and Rosita Green (23.86 QE g−1 DW). In comparison, the lowest content of TFC was measured in the leaves of the cultivar Rosita Blue Picote (2.9 mg QE g−1 DW).

3.2. Antioxidant Capacities Variability (FRAP, ABTS, DPPH) Across Lisianthus Cultivars

The highest FRAP value was recorded in the petals of the Rosita Green cultivar (30.9 mg ASC g−1 DW), while the lowest value was in the leaves of the Mariachi Pink Picote cultivar (9.4 mg AAE g−1 DW) (Figure 2A).
The ABTS radical scavenging in petals ability was approximately 2.1 times higher than in leaves. The highest ABTS radical scavenging ability was recorded in the petals of the Rosita Green cultivar (244.8 mM TE g−1 DW), while the lowest value was recorded in the leaves of the Mariachi Pink Picote cultivar (58.4 mM TE g−1 DW) (Figure 2B).
The highest DPPH radical scavenging ability was recorded in the petals of the Mariachi Lavender (83.8 mM TE g−1 DW) and Rosita Green (82.5 mM TE g−1 DW) cultivars, while the lowest value was in the leaves of the Rosane Brown cultivar (13.9 mM TE g−1 DW) (Figure 2C).

3.3. Osmolyte Variability Among Inspected Lisianthus Cultivars

Figure 3A presents the values of PRO and GB (Figure 3B) in the leaves and petals of different cultivars of lisianthus. The analysis of both parameters reveals significant variations in their concentrations among the cultivars and between different plant organs (leaves and petals).
The concentration of PRO in leaves varies significantly among cultivars, ranging from 8.12 µmol PRO g−1 DW in Croma Yellow to 31.01 µmol PRO g−1 DW in Mariachi Pink Picote. In petals, the highest PRO level is found in Rosita Blue Picote at 32.23 µmol PRO g−1 DW, while the lowest is in Arena Pure White at 13.278 µmol PRO g−1 DW. Notably, proline content in petals is 23% higher than in leaves.
Glycine betaine concentrations show even greater variability. In leaves, values range from 10.93 µmol GB g−1 DW in Alissa Champagne to 18.03 µmol GB g−1 DW in Croma Yellow. In petals, the highest concentration is recorded in Rosita Blue Picote at 36.66 µmol GB g−1 DW, while the lowest is found in Rosita Green at 3.31 µmol GB g−1 DW. The GB in petals is approximately 74.88% higher than that in leaves.

3.4. Polyamine Profiling Within Inspected Lisianthus Cultivars

This study assessed the PA content in both petals and leaves across different cultivars of Eustoma grandiflorum, with a specific focus on PUT, SPD, and SPM levels. The average concentrations of all PAs were statistically significantly higher in the petals compared to the leaves. SPD was the most prevalent PA in both leaves and petals, followed by PUT and finally SPM.
Putrescine (PUT) levels in the leaves varied widely, from 255.75 nmol g−1 DW in the Mariachi Pink cultivar to 1279.07 nmol g−1 DW in the Mariachi Carmine cultivar (Figure 4A). In contrast, the highest putrescine concentration in the petals was observed in the Mariachi Pink (1035.89 nmol g−1 DW) and Rosita Green (1015.62 nmol g−1 DW) cultivars. In comparison, the lowest values were recorded in the Croma Yellow (520.39 nmol g−1 DW) and Mariachi Lavender (511.63 nmol g−1 DW) cultivars (Figure 4A). The Mariachi Carmine cultivar had the highest average PUT level in the leaves, whereas the Mariachi Pink cultivar had the highest PUT level in the petals.
Spermine (SPM) also showed variability among cultivars and organs. In the leaves, the highest SPM level was found in the Mariachi Carmine cultivar (236.27 nmol g−1 DW), while the lowest was recorded in the Croma Yellow cultivar (115.98 nmol g−1 DW) (Figure 4B). In the petals, the highest SPM levels were observed in the Mariachi Blue (306.86 nmol g−1 DW) and Mariachi Carmine (285.64 nmol g−1 DW) cultivars, while the lowest levels were noted in the Alissa Champagne (18.35 nmol g−1 DW) and Croma Yellow (111.00 nmol g−1 DW) cultivars. The Mariachi Blue cultivar had the highest average SPM level in the petals.
Spermidine (SPD) was present in the highest concentrations in the Mariachi Carmine cultivar (1444.53 nmol g−1 DW) in the leaves and the Mariachi Pink (1558.03 nmol g−1 DW) cultivar in the petals (Figure 4C). The lowest concentrations of SPD were measured in the Croma Yellow cultivar in the petals (597.58 nmol g−1 DW) and in the leaves (756.20 nmol g−1 DW). The Mariachi Pink cultivar showed the highest average SPD value in the petals.
Analysis of variance (ANOVA) showed statistically significant differences between different cultivars and organs for all investigation parameters (Table 2).

3.5. Correlation Matrix

The correlation matrix reveals several key interdependencies among the examined parameters (Figure 5).
Phenolic compounds exhibit a strong positive correlation with antioxidant parameters, including FRAP, ABTS, and DPPH, highlighting their crucial role in the antioxidant activity of plants. Specifically, the high correlation between phenols and FRAP (r = 0.93), ABTS (r = 0.82), and DPPH (r = 0.81) suggests that phenolic compounds significantly contribute to the overall antioxidant capacity. Similarly, the correlation between flavonoids and phenols (r = 0.80) further confirms the connection between these bioactive compounds, which aligns with their shared role in antioxidant processes. Interestingly, PRO shows weak correlations with most parameters, indicating that its role might not be directly related to antioxidant responses but could be more specific to stress responses. On the other hand, SPD and SPM are highly correlated with each other (r = 0.70), which may suggest a link within their biosynthetic pathways or mutual conversion. Overall, these results emphasize the importance of phenolic compounds in antioxidant activity, while other metabolites such as PRO, SPD, and SPM may play specific, yet distinct, roles in the physiological processes of plants.

3.6. Principal Component Analysis

The loadings of original variables with the first two principal components that contributed to the total variance by 64.71% were used to analyze the relationship between examined traits (Figure 6). The first component, accounting for 48.87% of the total variance, is primarily determined by the total phenolic content, FRAP, ABTS, total flavonoid content, and DPPH, suggesting that these parameters exhibit similar patterns of variation. Conversely, the second principal component, which explains 15.94% of the variance, highlights variability associated with the contents of SPD and SPM.
Intriguingly, all of the data from the electron transfer-based spectrophotometric tests (TPC, TFC, DPPH, FRAP, and ABTS) exhibited positive correlations with one another and were clustered in quadrant II, but all of the osmolytes (polyamines, proline, and glycine betaine) were grouped together in quadrant III, clearly differentiating between the antioxidant tests and phenolics.

4. Discussion

This study was aimed to profile biochemical properties of eleven Eustoma grandiflorum cultivars by assessing total phenolic content (TPC), flavonoid content (TFC), antioxidant activities (FRAP, ABTS, and DPPH), glycine betaine (GB) content, and PA profiles, specifically focusing on PUT, SPD, and SPM. The results provide a detailed understanding of the metabolic and physiological differences among cultivars, shedding light on their potential applications and adaptations to different seasonal conditions.
Among the lisianthus cultivars examined, the Rosita Green cultivar is distinguished by its high levels of phenols and flavonoids, which are likely linked to its ability to withstand stress, particularly heat and drought stress, during the summer flowering period. It is well known that elevated stress resistance may be attributed to increased antioxidant response that mitigates oxidative stress during critical growth phase, whereas phenolics and especially flavonoids have an important role [10]. This adaptation enhances oxidative stress protection and prolongs flower longevity. In contrast, spring-flowering cultivars like Arena exhibit lower levels of these compounds, suggesting reduced resistance to oxidative stress compared to summer-flowering varieties such as Mariachi and Rosita, which accumulated higher levels of total phenols and flavonoids in response stress during the blooming. Our findings highly concur with the results of Davies et al. [32] who have highlighted significant variability in flavonoid biosynthesis among lisianthus cultivars. Intriguingly, according to Schmitzer et al., there is an intricate link between levels of polyphenol content and a flower’s color, which explains why cultivars with more intense colors, such as Croma Yellow and Mariachi Carmine, exhibit lower phenol levels [33]. Furthermore, as strong antioxidants, phenolics have another role in flower development and senescence, as antioxidant levels can fluctuate throughout the flower’s life cycle, affecting stress resistance and flower quality [13]. Our study confirms that cultivars like Mariachi Lavender and Rosita Green, which maintain high levels of phenols and high antioxidant capacities, exhibited extending vase life and ensured higher quality during transport. Additionally, this property may be attributed to high flavonoid content since many reports confirmed that variation in flavonoid composition among lisianthus petals strongly influences both flower color and resistance to oxidative stress [34]. Cultivars with higher concentrations of specific flavonoids may have enhanced longevity and commercial value. Our findings show that petals generally contain higher total phenolic content (TPC) and total flavonoid content (TFC) compared to leaves, with petals being three times richer in phenols. Understanding the interplay between phenolic content, flavonoids, flower color, and stress resistance is crucial for developing effective cultivation strategies.
We hypothesize that lisianthus cultivars with higher phenolic and flavonoid content, particularly in petals, such as Rosita Green and Mariachi Lavender, likely possess enhanced stress resistance, extended vase life, and improved quality, making them potentially more suitable for commercial cultivation and transport.
There are numerous examples that amino acid PRO plays a significant role in extending vase life and improving the physiological traits of flowers in different cultivars [35,36]. Likewise, Yaghoobi Kiaseh et al. [35] have demonstrated that exogenous application of PRO and arginine significantly improves the vase life of Alstroemeria ‘mars’ flowers by regulating post-harvest physiochemical parameters, suggesting that PRO helps reduction of oxidative stress and maintenance of flower quality during storage. Additionally, Kumar et al. [36] found that exogenous PRO can alleviate oxidative stress and increase vase life in roses (Rosa hybrida L. ‘Grand Gala’), indicating that PRO can act as an antioxidant and an osmoprotectant by stabilizing cell membranes and proteins, thus prolonging the vase life of flowers. Similarly, the same authors found that PRO can play an important role in senescence and delaying the aging process in rose (Rosa hybrida L. “First Red”) flowers [37]. Furthermore, the foliar application of PRO had strong effects on the morphological and physiological traits and flower quality of marigolds (Calendula officinalis L.) under drought-stress conditions [38]. Our results showed cultivar and organ-dependent variation of PRO content in lisianthus species, which may indicate that different cultivars depending on proline levels exhibit various resistance to adverse growing conditions and the capacity to extend vase life depends on proline levels. The higher PRO content observed in the Mariachi Pink Picote leaves and the Rosita Blue Picote petals may contribute to these cultivars’ enhanced oxidative stress resistance and prolonged vase life. GB content across different lisianthus cultivars and plant organs revealed notable variations. Petals generally exhibited higher GB concentrations compared to leaves, with the Rosita Green cultivar displaying particularly low GB levels in petals despite its high phenolic and flavonoid content. In contrast, the Croma Yellow cultivar showed significantly higher GB content in petals. This elevated GB level could indicate a role in stress adaptation, particularly relevant for cultivars flowering in the fall when environmental stress conditions may be more prevalent. Considering the fact that GB plays a crucial role in mitigating stress by maintaining osmotic balance, stabilizing cellular membranes, and reducing oxidative damage, we can observe that higher GB levels are more specific to late-flowering cultivars, distinguishing them from early-flowering cultivars that are more prone to exhibit a proline response [39]. These findings about the important role of GB in alleviation of oxidative stress and its trade-off mechanism with proline were previously supported by demonstration that the foliar application of GB can effectively alleviate heat stress in marigold cultivars, improving physiological parameters and reducing oxidative stress [40]. Similarly, Li et al. [41] observed that pre-harvest application of GB improved fruit quality attributes and reduced susceptibility to storage disorders in cherries. These studies underscore the beneficial effects of GB in enhancing stress tolerance and maintaining plant quality, which aligns with the observed high GB content in Croma Yellow.
PAs, including PUT, SPD, and SPM, are vital for plant growth, development, and stress responses. They participate in key physiological processes such as cell division, organ differentiation, and flower and leaf senescence [9,10,11,12,13]. This study revealed that PA concentrations are significantly higher in petals compared to leaves across various lisianthus cultivars, reinforcing their critical role in floral tissues. Among the cultivars examined, Mariachi Carmine consistently exhibited the highest levels of all analyzed PAs. This suggests that this cultivar may have enhanced metabolic activities and better adaptation to its growing conditions. Conversely, Croma Yellow displayed the lowest average PA levels, which could imply that these two cultivars are employing different adaptive mechanisms—Chroma Yellow employed increased GB content, while Mariachi Carmine responded with increased PAs levels. These observations align with Kebert et al. [7] and Farahi et al. [42], who noted variability in PA responses among different cultivars of rose, highlighting the potential for breeding programs aimed at improving flower longevity and quality. Our findings indicate that SPD is the most prevalent PA in both leaves and petals. Elevated SPD levels may positively influence post-harvest flower quality by extending vase life and maintaining aesthetic appeal, although it is well known that spermidine plays a crucial role in modulation of flower senescence [43]. Furthermore, SPD enhances cell membrane stability and extends vase life in lilies [44]. There is variability in PUT levels among cultivars, with particularly high levels in Mariachi Carmine and Mariachi Pink Picote. This variability presents opportunities for breeding programs aimed at improving flower longevity and overall quality. The seasonal flowering periods of the cultivars studied may also influence polyamine levels. Mariachi varieties, which flower in the summer, show higher polyamine concentrations, possibly due to more intense physiological processes during this period. In contrast, cultivars like Croma Yellow and Rosane, which bloom in the fall, and Rosita Blue Picotee and Arena Pure White, which flower in the spring, exhibit different polyamine profiles, reflecting their unique adaptive strategies. The dominance of SPD and its high variability among cultivars suggest potential applications for polyamines in post-harvest treatments to enhance flower quality and longevity. Future research should explore the use of exogenous polyamines to further assess their impact on vase life and overall flower quality. Foliar application of SPD and sodium nitroprusside both can improve flower growth and longevity, which further confirms that polyamines and sodium nitroprusside have priming properties to modulate flower longevity and overall fitness through their synergism with nitric-oxide (NO) [45,46,47].
The analysis of the first two principal components, which together account for the majority of the total variance, revealed a strong correlation between antioxidant capacities, including total phenolic and flavonoid content, FRAP, ABTS, and DPPH. This strong positive correlation may be attributed to the fact that all these assays share the same electron transfer-based mechanism as was mechanistically explained previously [48].
Integrating these findings, it becomes evident that while high levels of phenolic compounds and flavonoids contribute to antioxidant defense, the role of GB, PRO, and polyamines in stress response and flower longevity is also significant. Understanding these interactions can help in developing strategies to resist flower quality and resilience through targeted cultivation practices and post-harvest treatments.

5. Conclusions

This study reveals that summer-flowering lisianthus cultivars, such as Rosita Green and Mariachi, exhibit elevated levels of phenolic compounds, flavonoids, and polyamines, which enhance their stress resistance compared to spring-flowering cultivars like Arena, which have lower concentrations of these compounds. In contrast, autumn-flowering cultivars such as Croma Yellow and Rosane Brown present a more modest biochemical profile. Notably, Croma Yellow displays relatively high flavonoid content, whereas Rosane Brown has the lowest antioxidant capacity among the cultivars examined. This variation indicates that the flowering period plays a significant role in shaping the biochemical profiles of lisianthus cultivars, providing valuable insights for targeted breeding and cultivation strategies aimed at improving stress tolerance and commercial viability.

Author Contributions

Conceptualization, V.V. and M.K.; methodology V.V., M.K. and M.R.; software, L.P.; formal analysis, V.V., M.K., L.K. and M.R.; data curation, L.P., V.V., B.K. and M.K.; writing—original draft preparation, V.V.; writing—review and editing, V.V., M.R., L.P., L.K., V.V., B.K. and S.O.; visualization, L.P.; supervision, S.O.; funding acquisition, S.O. All authors have read and agreed to the published version of the manuscript.

Funding

The authors declare financial support was received for research, authorship, and/or publication of this article. This research has been supported by the Ministry of Science, Technological Development, and Innovation of the Republic of Serbia, Contract No. 451-03-66/2024-03/200117, 451-03-65/2024-03/200117 and 451-03-66/2024-03/200197. In addition, this manuscript covered one of the research topics conducted by the researchers gathered in the Center of Excellence Agro-Ur-For at the Faculty of Agriculture in Novi Sad, supported by the Ministry of Science, Technological Development, and Innovation, contract number 451-03-4551/2024-04/17.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

We acknowledge the Ministry of Science, Technological Development, and Innovation of the Republic of Serbia.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Genotype and organ-specific variability of lisianthus cultivars regarding (A) total phenolic content (mg GAE g−1 DW) and (B) total flavonoid content (mg QE g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
Figure 1. Genotype and organ-specific variability of lisianthus cultivars regarding (A) total phenolic content (mg GAE g−1 DW) and (B) total flavonoid content (mg QE g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
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Figure 2. Genotype and organ-specific variability of lisianthus cultivars regarding (A) ferric reducing antioxidant power (FRAP; mg AAE g−1 DW), (B) 2,2′-azinobis-3-ethyl benzothiazoline-6-sulfonic acid (ABTS; mM TE g−1 DW), and (C) 2, 2-diphenyl-2-picrylhydrazyl (DPPH; mM TE g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
Figure 2. Genotype and organ-specific variability of lisianthus cultivars regarding (A) ferric reducing antioxidant power (FRAP; mg AAE g−1 DW), (B) 2,2′-azinobis-3-ethyl benzothiazoline-6-sulfonic acid (ABTS; mM TE g−1 DW), and (C) 2, 2-diphenyl-2-picrylhydrazyl (DPPH; mM TE g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
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Figure 3. Genotype and organ-specific variability of osmolyte content in lisianthus cultivars regarding (A) proline content (µmol PRO g−1 DW) and (B) glycine betaine content (µmol GB g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
Figure 3. Genotype and organ-specific variability of osmolyte content in lisianthus cultivars regarding (A) proline content (µmol PRO g−1 DW) and (B) glycine betaine content (µmol GB g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
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Figure 4. Genotype and organ-dependent polyamine variability in various lisianthus cultivars regarding (A) putrescine (nmol g−1 DW), (B) spermidine (nmol g−1 DW), and (C) spermine (nmol g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
Figure 4. Genotype and organ-dependent polyamine variability in various lisianthus cultivars regarding (A) putrescine (nmol g−1 DW), (B) spermidine (nmol g−1 DW), and (C) spermine (nmol g−1 DW). Distinct lowercase letters denote statistically significant differences among lisianthus cultivars based on Tukey’s honestly significant difference (HSD) post hoc test (p ≤ 0.05). The data are presented as mean ± standard error (SE). The leaf symbol indicates activity in leaves, while the flower symbol represents antioxidant activities of petal extract.
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Figure 5. The Pearson correlation coefficient matrix of the analyzed parameters in lisianthus cultivars. Blue squares indicate a strong and significant correlation among the examined parameters, whereas red squares indicate a lower level of interaction based on the corresponding Pearson coefficient. Abbreviations of examined parameters: total phenolic content (TPC); total flavonoid content (TFC); ferric reducing antioxidant power (FRAP); 2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS); 2,2-diphenyl-2-picrylhydrazyl (DPPH); free proline content (PRO); glycine betaine (GB); putrescine (PUT); spermidine (SPD); spermine (SPM).
Figure 5. The Pearson correlation coefficient matrix of the analyzed parameters in lisianthus cultivars. Blue squares indicate a strong and significant correlation among the examined parameters, whereas red squares indicate a lower level of interaction based on the corresponding Pearson coefficient. Abbreviations of examined parameters: total phenolic content (TPC); total flavonoid content (TFC); ferric reducing antioxidant power (FRAP); 2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS); 2,2-diphenyl-2-picrylhydrazyl (DPPH); free proline content (PRO); glycine betaine (GB); putrescine (PUT); spermidine (SPD); spermine (SPM).
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Figure 6. Loadings of the first two principal components for examined parameters. Abbreviations of examined parameters: total phenolic content (TPC); total flavonoid content (TFC); ferric reducing antioxidant power (FRAP); 2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS); 2,2-diphenyl-2-picrylhydrazyl (DPPH); free proline content (PRO); glycine betaine (GB); putrescine (PUT); spermidine (SPD); spermine (SPM).
Figure 6. Loadings of the first two principal components for examined parameters. Abbreviations of examined parameters: total phenolic content (TPC); total flavonoid content (TFC); ferric reducing antioxidant power (FRAP); 2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS); 2,2-diphenyl-2-picrylhydrazyl (DPPH); free proline content (PRO); glycine betaine (GB); putrescine (PUT); spermidine (SPD); spermine (SPM).
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Table 1. Characteristics of eleven examined lisianthus cultivars.
Table 1. Characteristics of eleven examined lisianthus cultivars.
Cultivar NameHarvest PeriodOther Characteristics
Horticulturae 10 01193 i001Mariachi BlueSummer (July, August)
▪
Quadruple flower with large 5–7 cm diameter blooms;
▪
long stems up to 100 cm;
▪
excellent rose-shaped flower heads with thick petals.
Horticulturae 10 01193 i002Mariachi PinkSummer (July, August)
▪
Quadruple flower with large 5–7 cm diameter blooms;
▪
long stems up to 100 cm;
▪
excellent rose-shaped flower heads with thick petals.
Horticulturae 10 01193 i003Mariachi CarmineSummer (July, August)
▪
Quadruple flower with large 5–7 cm diameter blooms;
▪
long stems up to 100 cm;
▪
excellent rose-shaped flower heads with thick petals.
Horticulturae 10 01193 i004Mariachi Pink PicoteSummer (July, August)
▪
Quadruple flower with large 5–7 cm diameter blooms;
▪
long stems up to 100 cm;
▪
excellent rose-shaped flower heads with thick petals for long.
Horticulturae 10 01193 i005Mariachi LavenderSummer (July, August)
▪
Quadruple flower with large 5–7 cm diameter blooms;
▪
long stems up to 100 cm;
▪
excellent rose-shaped flower heads with thick petals for long.
Horticulturae 10 01193 i006Alissa ChampagneSummer (July, August)
▪
Large, well-filled double flowers;
▪
hard petals, less risk of damage;
▪
big, round flower buds;
▪
long vase life.
Horticulturae 10 01193 i007Croma YellowFall (September)
▪
Excellent rose-like flowers;
▪
strong petals and extra-double flowers set it apart as a premium variety.
Horticulturae 10 01193 i008Rosita GreenSummer (July, August)
▪
Loaded with more usable buds and medium-sized,
▪
rose-shaped flowers,
▪
thick petals, top flowering, and strong stems make
▪
easy transport without Botrytis problems.
Horticulturae 10 01193 i009Arena Pure WhiteSpring to early summer (May, June)
▪
High-quality and fully double flowers on strong and sturdy stems;
▪
thick petals help transportability;
▪
large buds on the top increase the attractive character of the stems.
Horticulturae 10 01193 i010Rosanne BrownFall (September)
▪
Hard flower petals, less risk of damage;
▪
good transportability.
Horticulturae 10 01193 i011Rosita Blue PicoteSpring to early summer (May, June)
▪
Rosita is the standard in double-flowered lisianthus;
▪
thick petals and strong stems;
▪
easy to transport without Botrytis problems.
Table 2. Results of F-test on examined characters in lisianthus cultivars (1).
Table 2. Results of F-test on examined characters in lisianthus cultivars (1).
TraitCultivar (A)Organ (B)Interaction (AXB)
Total phenolic content87.6 **3639.5 **40.9 **
Total flavonid content106.7 **3445.7 **72.18 **
Ferric reducing antioxidant power47.5 **871.6 **22.9 **
ABTS radical scavenging activity24.3 **435.7 **12.9 **
DPPH radical scavenging activity117.3 **1470.0 **143.6 **
Proline content302.5 **437.0 **113.1 **
Glycine betaine144.9 **1548.1 **129.2 **
Putrescine21.0 **93.7 **19.5 **
Spermidine19.1 **22.0 *3.4 **
Spermine17.1 **6.0 **8.4 **
(1) (*): significant for (p > 0.05); (**): significant for (p > 0.01).
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MDPI and ACS Style

Vuksanović, V.; Kebert, M.; Pavlović, L.; Kesić, L.; Rašeta, M.; Kovačević, B.; Orlović, S. Genotype and Organ-Specific Variability in Antioxidant Capacities as Well as Polyamine and Osmolyte Levels in Eleven Lisianthus (Eustoma grandiflorum Raf.) Cultivars with Different Flowering Periods. Horticulturae 2024, 10, 1193. https://doi.org/10.3390/horticulturae10111193

AMA Style

Vuksanović V, Kebert M, Pavlović L, Kesić L, Rašeta M, Kovačević B, Orlović S. Genotype and Organ-Specific Variability in Antioxidant Capacities as Well as Polyamine and Osmolyte Levels in Eleven Lisianthus (Eustoma grandiflorum Raf.) Cultivars with Different Flowering Periods. Horticulturae. 2024; 10(11):1193. https://doi.org/10.3390/horticulturae10111193

Chicago/Turabian Style

Vuksanović, Vanja, Marko Kebert, Lazar Pavlović, Lazar Kesić, Milena Rašeta, Branislav Kovačević, and Saša Orlović. 2024. "Genotype and Organ-Specific Variability in Antioxidant Capacities as Well as Polyamine and Osmolyte Levels in Eleven Lisianthus (Eustoma grandiflorum Raf.) Cultivars with Different Flowering Periods" Horticulturae 10, no. 11: 1193. https://doi.org/10.3390/horticulturae10111193

APA Style

Vuksanović, V., Kebert, M., Pavlović, L., Kesić, L., Rašeta, M., Kovačević, B., & Orlović, S. (2024). Genotype and Organ-Specific Variability in Antioxidant Capacities as Well as Polyamine and Osmolyte Levels in Eleven Lisianthus (Eustoma grandiflorum Raf.) Cultivars with Different Flowering Periods. Horticulturae, 10(11), 1193. https://doi.org/10.3390/horticulturae10111193

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