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Article

Effects of Seed Priming with Gamma Radiation on Growth, Photosynthetic Functionality, and Essential Oil and Phytochemical Contents of Savory Plants

by
Vahideh Mohammadi
1,
Mahboobeh Zare Mehrjerdi
1,*,
Anshu Rastogi
2,
Nazim S. Gruda
3,* and
Sasan Aliniaeifard
1,4,*
1
Department of Horticulture, College of Agricultural Technology (Aburaihan), University of Tehran, Tehran 3391653755, Iran
2
Laboratory of Bioclimatology, Department of Ecology and Environmental Protection, Faculty of Environmental Engineering and Mechanical Engineering, Poznan University of Life Sciences, Piątkowska 94, 60-649 Poznań, Poland
3
Department of Horticultural Science, INRES-Institute of Crop Science and Resource Conservation, University of Bonn, 53121 Bonn, Germany
4
Controlled Environment Agriculture Center, College of Agriculture and Natural Resources, University of Tehran, Tehran 3391653755, Iran
*
Authors to whom correspondence should be addressed.
Horticulturae 2024, 10(7), 677; https://doi.org/10.3390/horticulturae10070677
Submission received: 23 May 2024 / Revised: 19 June 2024 / Accepted: 21 June 2024 / Published: 26 June 2024
(This article belongs to the Special Issue Medicinal Herbs: Latest Advances and Prospects)
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Versions Notes

Abstract

:
Gamma radiation has been suggested to have post-effects on emerging plants when applied to the seeds. In the present study, we aimed to induce alterations in photosynthetic functionality and subsequent modifications in secondary metabolites of summer savory following seed priming with gamma radiation. Savory seeds were treated with 0, 50, 100, 200, and 300 Gy gamma radiation in a completely randomized design with ten replications for morphological and photosynthetic parameters and three for phytochemical assessments. The results showed that gamma radiation on seeds adversely affected photosynthetic performance, especially at the highest doses. It negatively influenced the growth, while increasing the shoot branching, the number of nodes, and the diameter of the stem. Gamma radiation on seeds generally reduced pigmentation in savory leaves, such as chlorophylls, carotenoids, and anthocyanins. However, soluble sugar, starch, total phenolics, and total flavonoid contents were elevated in the leaves of plants that emerged from gamma-primed seeds. Gamma radiation priming reduced essential oil’s percentage and yield. Carvacrol and limonene components of essential oil were diminished, whereas linalool and thymol were increased. In conclusion, due to its inherent stress-inducing effects, and despite some positive effects on phytochemicals, seed priming with gamma radiation adversely influenced growth, photosynthesis, and quantity and quality of savory essential oils. Further research is still needed to target the use of gamma radiations before harvesting the seeds or determine the cytogenetic characteristics of irradiated plants.

1. Introduction

Summer savory (Satureja hortensis L.) belongs to the Lamiaceae family [1]. The essential oil of this plant contains large amounts of phenolic compounds such as thymol, carvacrol, ρ-cymene, γ-terpinene, and linalool [2,3]. Typically gathered at the flowering stage, savory’s aerial parts have a variety of medicinal uses, including aiding digestion and acting as a diuretic, astringent, carminative, and anti-diarrheal. Summer savory essential oil is traditionally employed in the culinary and medicinal sectors [4,5]. The leaves of this plant are rich in phenolic compounds, especially rosmarinic acid and flavonoids, which have a high antioxidant capacity [6]. These substances can postpone or prevent oxidative damage by free radical and non-free radical species [7]. Phenolic compounds and flavonoids also have anti-inflammatory properties [8].
Gamma radiation has been reported to cause oxidative stress by excessive production of reactive oxygen species (ROS) such as superoxide radicals, hydroxyl radicals, and hydrogen peroxide, which quickly respond to almost all structural and functional organic molecules, including proteins, lipids, and nucleic acids. They cause disturbances in cell metabolism [9]. ROS can react with almost all cellular components. Such interaction causes chain reactions of free radicals and finally causes membrane lipid peroxidation. As a result, the membrane becomes less stable and more permeable, damaging the structure of the cell and interfering with regular physiological processes [10]. It has been demonstrated that high doses of ionizing radiation cause physiological changes in plants, including an increase in respiration, the formation of ethylene, and the promotion of enzyme activity (especially for phenolic metabolism and accumulation of certain protein species). These effects result from the direct interaction between ionizing radiation and macromolecular structures and ROS produced via the radio dissociation of water [11]. Ionizing radiation based on particles or electromagnetic waves that make an ionizing effect are classified and have different ionization mechanisms. The physical properties of ionizing radiations (e.g., X-radiation, gamma radiation, ultraviolet radiation, alpha particles, beta, and neutrons) are different. Therefore, their potential and biological application for breeding has been investigated. These radiations have stimulating, moderate, and harmful effects on plant growth and development, depending on the ionizing radiation level utilized on plant organs [12]. Structural and functional alterations brought on by ionizing radiation on the DNA molecule are involved at the intracellular levels. The nature of DNA changes, including changes in bases, base exchange, deletion of bases, and chromosomal aberrations, are the reasons for changes in the macroscopic phenotype [13]. Plants show different adaptive responses to the radiation. Radiation adaptation and DNA repair mechanisms can shield the plant genome from drastic alterations [14]. The plant’s response to exposure to low doses is quite different from its reaction to high doses of exposure to gamma radiation. Studies indicated that exposure to low doses of gamma radiation is more likely to produce beneficial physiological effects than high doses [15,16]. Exposure to low-dose radiation induces the production of active metabolites, including flavonoids, salicylic acids, phenolic compounds, caffeic acids, coumaric acids, and anthocyanins, in medicinal plants [17]. Gamma radiation belongs to ionizing radiation, interacting with atoms or molecules to create cell-free radicals. These radicals can change essential components of plant cells. It has been reported that plants’ anatomy, morphology, physiology, and biochemistry would be affected by the level of radiation. These changes include alterations in photosynthesis and pigments, dilation of thylakoid membranes, regulation of the antioxidant system, and accumulation of phenolic compounds [18,19,20].
Chloroplasts are much more sensitive to radiation than other cell organs, and an increase in chlorophyll pigments following irradiation has been reported [16]. Therefore, the photosynthesis system is the most sensitive process for irradiated plants [21]. Studies have shown that gamma radiation stimulates the response to plant stress, increasing the concentration of secondary metabolites [22]. For instance, in rosemary, stevia, and fenugreek, gamma radiation exposure has reported an increase in secondary-metabolite production [23,24,25]. Chlorophyll fluorescence is a proper approach to investigating the healthiness of photosynthetic apparatus. It is a sensitive tool for detecting photosystems and electron transport system damage. Chlorophyll fluorescence is a detectable signal that can be cheap, fast, and simple for photosynthetic investigations [26,27,28,29]. Photosynthetic measurements are considered a critical indicator for investigating plant stress. However, studying the gas exchange response of photosynthesis based on measuring the rate of photosynthesis provides incomplete information about the structural damage to photosynthesis.
Given that different doses of gamma radiation can affect plants’ growth, photosynthesis, and phytochemistry in various ways (mainly through its stress-inducing effects), investigating these effects can be valuable for improving the quantity and quality of medicinal plants. To the best of our knowledge, no study has examined the effects of gamma radiation priming on the growth, photosynthetic activity, secondary metabolites, and phytochemical responses of summer savory plants. Therefore, this study evaluated the impact of different gamma radiation doses on summer savory’s photosynthetic, morphological, and phytochemical traits, aiming to identify the optimal dose to enhance yield and quality. Summer savory was selected for its rich phytochemical composition and the pharmaceutical significance of its essential oils, making it an ideal candidate for research on improving phytochemical and essential oil quality and quantity and understanding plant responses to various exogenous treatments.

2. Materials and Methods

2.1. Plant Material and Seed Treatments

To study the effect of gamma radiation on photosynthesis, primary and secondary metabolites of summer savory (Satureja hortensis L.) savory seeds were obtained from Pakan Bazr Isfahan Company. Seeds were treated with different doses (0, 50, 100, 200, and 300 Gray (Gy) of gamma radiation (approximately one thousand seeds in one gram). The seeds were treated with the same radiation intensity and for different durations with the Cobalt 60 device. After disinfection, seeds were cultured in trays containing coco peat and perlite (3:1 v:v). In the four-leaf stage, the plants were transferred to pots containing field soil (Table 1), sand, and leaf mold (with the ratios 1:1:1). The experiment was performed in a greenhouse with a temperature of 20–25 °C and 16/8 h light/dark photoperiod. Sampling for plant analysis was performed at the flowering stage, and plant leaves were used for biochemical tests.

2.2. Morphological and Growth Measurements

Morphological and growth traits, including plant height, number of leaves, leaf length, stem diameter, number of branches, number of nodes, fresh and dry weight of shoots, fresh and dry weight of roots, root volume, and root length, were measured at the flowering stage of plants. Shoot and root dry weights were assessed after the samples were placed in a 70 °C oven for 48 h just after the harvest. Root volume was determined using a graduated cylinder containing a certain amount of water and by selecting the difference between the initial volume and the volume of water after root placement [30].

2.3. Polyphasic Chlorophyll Fluorescence Transient Evaluation

Young, fully developed leaves of the plant were used in the flowering stage to evaluate the photosynthetic functionality. Before measurement, the leaves were kept in the dark for 20 min. Following dark adaptation, the leaves were placed in the leaf chamber of a Flourometer (PAR-Flour Pen FP 100 MAX, Photon Systems Instruments, Brno, Czech Republic) and FlourCam (FC 1000-H, Photon Systems Instruments, Brno, Czech Republic).
The fluorescence transient consists of the following phases: O to J, J to I, and I to P. Overall, F0 is indicative of the “open” (O) state of the OJIP transient, which is the fluorescence intensity of open PSII reaction centers (RCs). FM came from the maximal chlorophyll fluorescence intensity emitted from closed PSII RCs. FV is indicative of the variable chlorophyll fluorescence (FV = FM − F0), and, finally, FV/FM (see equation in Table 2) is the maximum photochemical efficiency of PSII [28].

2.4. Photosynthetic Pigments

To measure chlorophyll a and b and total chlorophyll and carotenoids, 100 mg of powdered plant samples was ground with 2 mL of 80% acetone and centrifuged at 4000× g for six min. The supernatant adsorption at 470, 646, and 663 nm was read by a spectrophotometer. The values were recorded based on the following formulas [31]:
Chlorophyll a = (12.21 × A663nm) − (2.81 × A646nm)
Chlorophyll b = (20.13 × A646nm) − (5.03 × A663nm)
Carotenoid = ((1000 × A470nm) − (3.27 × Chlorophyll a) − (104 × Chlorophyll b))/229
For quantifying anthocyanin content, 160 mg of leaf powder was mixed with 5 mL hydrochloric acid in methanol (1%). Following incubation at 4 °C for 24 h, samples were centrifuged at 7000× g for 5 min, and the adsorption of the supernatant was read at 530 and 657 nm. The amount of anthocyanin was calculated using the following equation [32]:
Anthocyanin = A530nm − (0.25 × A657nm)

2.5. Soluble and Storage Carbohydrates

To evaluate soluble sugar, 200 mg of leaf tissue was first pulverized and then transferred to Falcon tube with 10 mL of 95% ethanol. Then, it was centrifuged at 5000× g for 10 min. Afterward, the supernatant was transferred to a new Falcon tube, and 10 mL of 70% ethanol was added to the existing precipitate. The previous steps were repeated. This was performed twice, and the supernatant was added to the earlier supernatants. Total soluble sugar was determined by reacting 500 µL of the supernatant with a 1.5 mL Antron reagent (mixture of 150 mg of pure Antron with 100 mL of 72% sulfuric acid). The samples were placed in a water bath at 100 °C for 10 min. After cooling the samples, the absorbance was recorded at 625 nm [33]. Concentrations of 0, 25, 75, and 100 μg/mL glucose were used to draw the standard curve.
Sediments left over from the previous experiment and completely dried were used to determine storage carbohydrates. First, 1.52 mL of cold distilled water was added to the sediments. They were shaken for 15 min after adding 1.62 mL of 52% perchloric acid. Then, 5 mL of distilled water was added and centrifuged at 5000× g for 10 min in a supernatant. All previous steps were repeated, and a new supernatant was added to the previous one. The resulting solutions were placed in ice for 30 min. Then, they were transferred to a balloon with filter paper, and their volume increased to 50 mL with distilled water. After that, 100 μL of the solution with distilled water reached a volume of 5 mL. Then, 1.5 mL of Antron was added to 500 μL of the resulting extract and placed in a hot water bath at 100 °C for 7.5 min. After cooling at room temperature, adsorption was recorded by a spectrophotometer at 630 nm [34].

2.6. Total Phenolic, Total Flavonoid Contents, and Antioxidant Capacity

The plant methanol extract was used to measure total phenolic, total flavonoid, and antioxidant capacity. For this purpose, one gram of plant powder of each sample was mixed with 10 mL of 80% methanol and incubated for 24 h at room temperature. The samples were centrifuged at 13,000× g for 20 min. Finally, the supernatant was collected and stored in a freezer at −70 °C until the evaluations were performed.
The Follin–Ciocâlteu reagent was used to evaluate the total phenolic content. For this purpose, 250 µL of methanol extract was mixed with 1750 µL of distilled water and 100 µL of Follin–Ciocâlteu. After 10 min, 20 mL of 20% sodium carbonate (Na2CO3) was added. The samples were kept at room temperature and in the dark for 2 h, and then their absorbance at 730 nm was read by a spectrophotometer. Concentrations of 0, 100, 200, 300, 400, and 500 μg/mL gallic acid were used to draw the standard curve [35].
The amounts of total flavonoids were determined using the aluminum chloride colorimetric method. In total, 100 μL of potassium acetate, 100 μL aluminum chloride, and 2.8 mL of distilled water were added to 0.5 mL of methanol extract. The samples were placed at room temperature for 30 min, and the absorbance was read at 415 nm [36]. The standard curve was prepared using quercetin in methanol solvent at 250-to-1000 μg/mL concentrations.
The DPPH free radical scavenging method was used to determine the antioxidant capacity. First, 200 μL of methanol extract was mixed with 1800 μL of distilled water and 1 mL of 0.1 mM DPPH solution. The samples were then placed at room temperature and in the dark for 30 min, and, finally, their absorbance was measured at 515 nm. The percentage of free radical scavenging was recorded based on the following equation [35]:
Scavenging activity (%) = 1 − (As/Ac) × 100
where Ac is the control’s absorbance, and As is the sample’s absorbance.

2.7. Extraction and Gas Chromatography–Mass Spectrometry (GC/MS) Analysis of Essential Oil

The aerial parts of the plants harvested at the flowering stage were dried under shade. Their essential oils were obtained using a Clevenger apparatus for 3 h. The percentage of essential oil in each treatment was determined. Essential oil yield was obtained from the ratio between the percentage of essential oil and shoot dry weight. A gas chromatography device with a mass spectrometer was used to identify the compounds in the essential oil and determine their percentage. A DB-5 column with the following characteristics, including 30 m length, 0.25 mm inner diameter, and 0.25 μm thickness, was used for separation. The column heat program started with an initial temperature of 60 °C and increased at 3 °C per minute to 220 °C. It then reached 260 °C at 20 °C per min and remained at this temperature for 5 min. The injection chamber temperature was 260 °C, and helium gas was used at a speed of 30.6 cm/s. The MS was operated in scan mode, scanning ions from 40 to 300 m/z at a rate of 1 scan/s under 70 eV ionization conditions.

2.8. Statistical Analysis

Experiments were analyzed using a completely randomized design with at least three replications. Ten replications were used for morphological analysis, and three were used for measuring other traits. Data analysis and graphing were performed with SAS (Version 9.4 TS Level 1M, SAS Institute Inc.; Cary, NC, USA) and Excel software (version 2016). Duncan’s multi-range test at the 5% probability level analyzed significant differences among treatments.

3. Results

3.1. Gamma Radiation Causes Changes in Growth and Morphological Traits

Exposure of seeds to gamma radiation resulted in changes in growth and morphological characteristics in savory. The height of plants decreased as a consequence of gamma radiation. The shortest plants emerged from the seeds treated with 300 Gy of gamma radiation (the height decreased by 13.96% compared to the control). The number of nodes and branches gradually increased by increasing the dose of gamma radiation to 200 Gy; the number of branches almost tripled by 200 Gy compared to the number of branches in control plants. However, the highest dose of gamma radiation negatively affected the number of nodes and branches. High radiation doses (200 and 300 Gy) reduced the number of leaves compared to the control. The largest leaves were observed in the control plants. The thickest stem diameter was detected in plants that emerged from the seeds exposed to 200 Gy. The longest roots were seen in plants that emerged from the seeds treated with 50 and 100 Gy gamma radiations (Table 3).
The highest fresh and dry weight of shoots was recorded in plants that emerged from the seeds treated with 100 Gy. Doses of 100 Gy caused a 26.76% increase, while a dose of 50 Gy caused a 12% decrease in the fresh weight of the shoot when compared to the control plants. Similar results were obtained for fresh weight, based on the effect of gamma radiation on shoot dry weight. Root fresh weight was gradually decreased by increasing the dosage of gamma ray; the lowest root fresh weight was detected at the highest gamma radiation (300 Gy), which was 2.5 times lower than the root fresh weight of control. The dose of 300 Gy also reduced the dry weight of the roots, while the other gamma-radiation doses did not affect the dry weight of the roots (Table 4).

3.2. Gamma Radiation Had Negative Impacts on Photosynthesis Functionality

Chlorophyll fluorescence analysis and imaging were used to see the impact of seed treatment with gamma radiation on the photosynthetic functionality of summer savory plants. The photosynthetic functionality was investigated long after the stress (in the flowering stage). Photosynthetic functionality in the flowering stage was affected by a dose of 300 Gy gamma radiation, which caused a 1.82% and 18.92% decrease in FV/FM and PIABS compared to the control (Figure 1a and Figure 2). It also caused a 6%, 4%, and 15% increase in ABS/RC, TR0/RC, and DI0/RC compared to the control (Figure 1). Chlorophyll fluorescence imaging of savory plants grown from gamma-treated seeds showed a substantial decrease by 300 Gy gamma radiation (Figure 1).

3.3. Negative Effects of Many Doses of Gamma Radiations on Photosynthetic Pigments

Chlorophyll pigmentation decreased in the plants grown from gamma-radiated seed. The lowest levels of chlorophyll a and b were detected in plants that emerged from seeds radiated with 300 Gy. The highest level of chlorophyll b was detected in plants that emerged from seeds radiated with 100 Gy, 3.5 times more than the control. The total chlorophyll level decreased due to treatment with different doses of gamma radiation, except for the 100 Gy. The total chlorophyll increased by 42% in plants that emerged from seeds radiated with 100 Gy compared to the control. Doses of 50 and 100 Gy decreased, and 200 Gy increased, the carotenoid contents. All doses of gamma radiation adversely affected the anthocyanins content and chlorophyll a/chlorophyll b ratio (Figure 3). The lowest chlorophyll a/chlorophyll b ratio was detected in plants that emerged from seeds radiated with 100 Gy.

3.4. The Effects of Gamma Radiation on the Amount of Soluble and Storage Carbohydrates

Gamma radiation increased the soluble sugars, and the highest amount was detected in the 100 Gy, where the sugar concentration increased more than 2.5 times compared to the control. Doses of 100 and 200 Gy of gamma radiation increased the amount of starch, so the dose of 100 Gy increased the starch about eight times compared to the control plants (Table 4).

3.5. Increase of Total Phenolic and Total Flavonoid Contents under Gamma Radiation Treatment and Lack of Effect of It on Antioxidant Capacity

The total phenolic content in plants increased due to gamma radiation on savory seeds. The highest amount was observed at a dose of 300 Gy (increased by 42% compared to the control). All gamma radiation doses increased the total flavonoid content by more than 20% compared to the control. In addition, the exposure to 100 Gy gamma radiation substantially heightened the yield of phenols and flavonoids in each plant, exceeding 50% compared to the control (Table 5). The results of the variance analysis of the data showed no significant difference between the antioxidant capacities of savory plants grown from gamma-treated seeds by different doses of radiation.

3.6. The Negative Effect of Gamma Radiation on the Percentage and Yield of Essential Oil and the Change of Yield of Critical oil Components

The gamma irradiation of seeds decreased the percentage and yield of the essential oil in savory at the flowering stage and affected the essential oil’s components. The yield of carvacrol and limonene decreased in plants that emerged from gamma-irradiated seeds. Although the essential oil of control plants did not contain linalool, different doses of gamma radiation often increased linalool activity, which was significant at 50 Gy. The yield of thymol was also often improved by radiation, so it was almost three times higher than that of the control plants at a dose of 300 Gy (Figure 4 and Table 6).

3.7. Principal Component Analysis

In this study, a Principal Component Analysis (PCA) was conducted to examine the correlations between various characteristics of summer savory plants under different doses of gamma radiation. The PCA plot shows three principal components that explain 47.5%, 30.99%, and 11.94% of the total data variance, respectively, covering 90.44%. This indicates the importance of the variance explained by these three components and their sufficiency for data analysis (Figure 5). The different characteristics of the plant examined in this analysis include plant height (PH), number of branches (NB), number of nodes (NN), number of leaves (NL), leaf length (LL), stem diameter (SD), root length (RL), stem fresh weight (SFW), stem dry weight (SDW), root fresh weight (RFW), root dry weight (RDW), total chlorophyll (TC), soluble carbohydrates (SoC), storage carbohydrates (StC), essential oil yield (EOY), and essential oil percentage (EOP).
The vectors of SD and RL are in opposite directions, indicating a negative correlation between them. High doses of radiation (200 and 300 Gy) had a negative impact on RL, causing a reduction, while having a positive effect on SD. Furthermore, SFW and SDW had a positive correlation with each other and with the second component (PC2). Gamma radiation at a dose of 100 Gy had the most positive impact on these characteristics, whereas higher doses showed a negative effect.
Different doses of gamma radiation had varying effects on the characteristics of summer savory plants. In this regard, 0 Gy was considered as the control, which showed natural variations. A dose of 50 Gy had a mild positive impact on characteristics like PH and NB. A dose of 100 Gy had the most positive impact on characteristics such as SFW, NN, and TC. Doses of 200 and 300 Gy had negative impacts on characteristics like RL and RDW, indicating damage due to high radiation exposure.
The PH (plant height), NB (number of branches), NN (number of nodes), NL (number of leaves), LL (leaf length), SD (stem diameter), RL (root length), SFW (shoot fresh weight), SDW (shoot dry weight), RFW (root fresh weight), RDW (root dry weight), TC (total chlorophyll), SoC (soluble carbohydrate), StC (storage carbohydrate), EOY (essential oil yield), and EOP (essential oil percentage).

4. Discussion

Plant responses to gamma radiation differ based on individual responses and phenotypic plasticity [37].
In this study, gamma radiation reduced the plant height, number of leaves, and leaf length, especially at high doses. The number of branches, nodes, stem diameter, and root length increased after gamma radiation. Doses of 100 Gy increased the fresh and dry weight of the aerial parts. The fresh and dry weight of the roots was reduced to 300 Gy. It has been reported that plant growth following gamma radiation is attributed to auxin degradation, alterations in ascorbic acid content, and physiological and biochemical disorders [38]. Gamma radiation causes the failure or non-synthesis of growth regulators, especially cytokinin and auxin, and ultimately reduces growth parameters [39]. However, the promotive effect of low doses of gamma radiation on plant growth may result from the induction of cell division and processes that influence nucleic acid synthesis [40]. In Terminalia arjuna Roxb., radiation with different doses of gamma radiation often reduced plant height and increased root length. Also, 25 and 50 Gy doses increased seedling dry weight [41]. In a study on peppermint seeds (Mentha piperita L.) treated with different doses of gamma radiation, it was observed that the number of leaves, number of nodes, plant height, root length, and fresh and dry weight of the plant decreased with increasing gamma doses [42].
FV/FM shows the maximum quantum yield of PSII machinery [43], which strongly correlates with the quantum efficiency of the pure photosynthesis system. A low FV/FM indicates the photoinhibition of leaves by stress [44,45]. Under non-stress conditions, FV/FM is almost constant [46]. The less open RCs are present in plants that face stress, and the Fv/FM decreases. It has also been found that the increase in maximum fluorescence from minimum fluorescence in transient OJIP has intermediate peaks and slopes that can be used to test plant stress sensitivity, which is summarized in the yield index [47,48]. γ Gamma radiation at a dose of 300 Gy decreased the FV/FM and PIABS. PIABS is one of the indicators used to examine the conditions of photosynthetic samples [49]. PIABS shows the performance of photosystem II, and the decrease in PIABS can be attributed to the inhibition of electron transfer due to reduced performance [50,51]. ABS/RC is representative of the adequate size of the receptor in the active RCs and is calculated by the total number of photons absorbed by the chlorophyll molecules from all RCs divided by the total number of active RCs. This parameter is affected by the ratio of active to inactive RCs [49]. An increase in the ABS/RC can occur because of an increase in the size of energy receptors for active RCs in photosystem II or a change in the energy connection between photosystem II units, which occurs in Quinone A resuscitation [52]. The TR0/RC parameter represents the excited electrons trapped by the open reaction and Quinone A reduction centers [51]. Increasing this parameter further inhibits quinone oxidation and evokes it to Quinone A, and restricting electron transport beyond photosystem II will lead to excessive regeneration of Quinone A [53]. Gamma radiation at 300 Gy increased ABS/RC and TR0/RC. ET0/RC operates with TR0/RC and active response centers. Increased TR0/RC leads to decreased electron transfer (ET0/RC), indicating photosystem II RCs’ inactivity [54,55]. Following gamma radiation treatment in red pepper cultivars (Yeomyung and Joheung), gamma radiation did not cause a significant difference in FV/FM between treatments [19]. Conversely, the FV/FM of buckwheat (Fagopyrum dibotrys Hara) exposed to 5, 10, 15, and 20 Gy decreased compared with the control plants [56].
Experimental evidence shows that chloroplasts are susceptible to high-dose exposure to gamma radiation, as it causes the breakdown of the structure of thylakoids, thereby down-regulating photosynthetic efficiency [16,20]. Because photosynthesis provides the energy needed for the plant life cycle, down-regulation of photosynthetic machinery due to ionizing radiation exposure negatively affects plant growth and productivity [57,58].
Gamma radiation affects chlorophyll content. High doses of gamma radiation reduce photosynthesis because of impaired chlorophyll biosynthesis or chlorophyll degradation, associated with loss of photosynthetic capacity [59,60,61]. The function of carotenoids as photosynthetic pigments and endogenous antioxidants, by absorbing excess energy and turning off reactive oxygen and chlorophyll protection, is also associated with photon energy absorption [62,63]. Low doses of gamma radiation reduced the carotenoid content (applying 200 Gy increased the carotenoids). The treatment of Datura innoxia seeds with doses of 5, 10, 20, 40, 60, and 80 Gy of gamma radiation showed that the levels of carotenoids, chlorophyll a, and chlorophyll b increased at 5 Gy and decreased at other doses [64]. In a study by Hajizadeh et al., Lilium (Lilium longiflorom cv. Tresor) was treated with doses of 10, 20, 30, 40, and 50 Gy of gamma radiation, and it was observed that different doses of γ, except 30 Gy, reduced the chlorophyll a, chlorophyll b, and total chlorophyll [65]. Free radicals are removed from the cell using antioxidant compounds such as anthocyanin [66,67]. This study shows that gamma radiation reduced savory anthocyanin. Reduction of anthocyanin in Sainfoin (Onobrychis viciifolia Scop.) with increasing doses of gamma radiation has been reported [68]. Studies have shown that gamma radiation, in addition to stimulating H2O2 production, leads to the accumulation of other types of ROS in the cell [69,70]. These destructive substances act as signals that initiate the genes’ expression to facilitate tolerance to stress conditions [67].
Accumulating organic substances (soluble and storage carbohydrates) is essential for initiating and maintaining inter-cellular osmotic pressure [71]. Many plants under stress conditions accumulate starch and soluble carbohydrates [72,73]. This accumulation is related to disturbed carbohydrate consumption [74]. In our study, gamma radiation led to an increase in soluble carbohydrates and starch. The effect of gamma radiation on the total carbohydrate content of German chamomile (Chamomilla recutita L.) and red sandalwood (Pterocarpus santalinus L.) showed that different doses of gamma radiation induced the accumulation of carbohydrates [75,76].
In the present study, the treatment of seeds with gamma radiation increased phenolics and total flavonoids in savory at the flowering stage. The application of gamma radiation at doses of 100, 200, and 300 Gy resulted in an increased yield of phenols and flavonoids in each plant. The highest phenol and flavonoid yield enhancement across all plants was observed at 100 Gy. Phenolic compounds are essential in plant defense against radiation [77]. Flavonoids are one of the secondary metabolites that are widely present in plants. They reduce the damage caused by radiation stress [78]. Depending on the radiation dose, gamma radiation interacts with various cell atoms and molecules, particularly water molecules, to form free radicals that can alter crucial components of plant cells [16]. The production of free radicals serves as a stress indicator and triggers stress reactions, which may raise the concentration of polyphenolic acids [79]. Phenolic compounds have a role in protecting plants against gamma radiation [80]. An increase in total phenol can be attributed to the activity of phenylalanine ammonia-lyase (PAL), which is one of the key enzymes involved in synthesizing phenolic compounds [81]. Gamma radiation has increased PAL activity [82]. Gamma radiation can release phenolic compounds from glycosidic components, break down huge phenolic compounds into more minor compounds, and ultimately increase the total phenolic content [83]. Increases in total phenols and flavonoids under the effect of gamma radiation have been reported in rosemary (Rosmarinus officinalis L.) and fenugreek (Trigonella foenum-graecum) [23,78]. In this study, the antioxidant capacity of savory was not significantly different after seed treatment with varying doses of gamma radiation. The survey of DPPH radical scavenging assay in arjuna plants under different doses of gamma radiation did not show a significant difference in the antioxidant capacity of plants [41].
Terpenes and their derivatives, such as terpenoid molecules, comprise most of the secondary metabolites found in plants called essential oils. Sesquiterpenes and monoterpenes are often their primary constituents [84]. Internal and external variables can influence the quantity and content of essential oils from plant sources. Genetic, physiological, and developmental variables are the most common internal causes. In contrast, external variables often include seasonality, temperature, circadian rhythm, water and nutrition availability, air pollution, altitude, mechanical stimulation, encroaching pathogens, and extraction conditions [85]. Gamma radiation’s effects on the components of essential oils depend on the radiation dosage, dose rate, kind of plant, temperature, and sample condition. The production of essential oils and the amount of their components can change depending on how much exposure to gamma radiation is received [86]. Changes in essential oil production may result from recombining radiolytic products over time. When the same component is found in different plant species, the effects of radiation on volatile molecules vary. For instance, it has been shown that monoterpene linalool has considerable gamma radiation sensitivity as an essential oil in the leaf of Ocimum basilicum L. [87]. However, Thymus vulgaris leaf essential oil includes a radiation-resistant component [88]. The carvacrol concentration in aerial part essential oil from Zataria multiflora Boiss. was considerably reduced in the same context [89]. Moreover, α-pinene content was significantly reduced in the essential oil of Angelica gigas Nakai [90]. However, α-pinene content is induced by exposure of the aerial part of Zataria multiflora Boiss. to gamma radiation [88]. In this study, radiation reduced the percentage and yield of essential oil and affected its components. Gamma radiation decreased carvacrol and limonene, increasing linalool and thymol in the essential oil of savory plants. A decrease in the percentage of essential oil and carvacrol and an increase in the thymol were observed in gamma radiation-dried Satureja spicigera (C. Koch) Boiss [91].

5. Conclusions

Despite enormous reports on essential oil improvement in plants by the gamma radiation of seeds, savory did not show a similar pattern. Gamma rays negatively affected photosynthetic functionality, especially at a dose of 300 Gy. Plants from gamma-treated seeds had smaller sizes and more branches than the control. Radiation reduced the chlorophyll and anthocyanin levels, whereas gamma radiation elevated the soluble sugars, starch, phenolics, and flavonoids. Even though radiation decreased the essential oil percentage and yield, it can be considered a method to increase the yield of linalool and thymol when these two compounds are the targets. Furthermore, it was found that, through its stressful impact, gamma radiation can alter the quantity and quality of savory essential oils. Despite the adverse effects on growth and photosynthesis, gamma radiation could enhance the levels of phenols and flavonoids in summer savory. However, additional research is needed to refine and optimize the irradiation process, focusing on mitigating any adverse impacts on essential oil composition. Future studies could explore the use of gamma radiation before seed harvesting and investigate its effects on photosynthesis, essential oil performance, and the cytogenetic characteristics of irradiated plants. Moreover, examining the expression patterns of genes involved in the biosynthesis of phytochemicals or secondary metabolites in plants exposed to radiation would be of particular interest.

Author Contributions

Carring out the experiment writing the original draft, software, V.M. Conceptualization, investigation, resources, project administration, review and editing, validation, and supervision, M.Z.M. and S.A. Writing—review and editing, visualization, supervision, N.S.G. Writing—review and editing, visualization, A.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data would be available on request.

Acknowledgments

The authors would like to thank the University of Tehran and Parcham company for facilitating performing this experiment.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effect of different doses of applied on the summer savory seeds on the flux of excitation energy of summer savory plants emerged from gamma radiation-treated seeds: (a) maximum efficiency of photosystem II (FV/FM), (b) system efficiency index per absorbed light (PIABS), (c) light absorption per reaction center (ABS/RC), (d) electron trapping per reaction center (TR0/RC), (e) electron transfer in each reaction center (ET0/RC), and (f) energy dissipated per reaction center (DI0/RC) were measured in the dark-adapted summer savory leaves at the flowering stage. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01; n.s., non-significant.
Figure 1. Effect of different doses of applied on the summer savory seeds on the flux of excitation energy of summer savory plants emerged from gamma radiation-treated seeds: (a) maximum efficiency of photosystem II (FV/FM), (b) system efficiency index per absorbed light (PIABS), (c) light absorption per reaction center (ABS/RC), (d) electron trapping per reaction center (TR0/RC), (e) electron transfer in each reaction center (ET0/RC), and (f) energy dissipated per reaction center (DI0/RC) were measured in the dark-adapted summer savory leaves at the flowering stage. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01; n.s., non-significant.
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Figure 2. Maximum quantum efficiency of photosystem II (FV/FM) obtained from chlorophyll fluorescence imaging of savory plants grown from gamma-treated seeds at doses of 0, 50, 100, 200, and 300 Gy.
Figure 2. Maximum quantum efficiency of photosystem II (FV/FM) obtained from chlorophyll fluorescence imaging of savory plants grown from gamma-treated seeds at doses of 0, 50, 100, 200, and 300 Gy.
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Figure 3. Effect of different doses of gamma radiation on the photosynthetic pigments of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation: (a) chlorophyll, (b) chlorophyll a/chlorophyll b, (c) carotenoids, and (d) anthocyanins. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01.
Figure 3. Effect of different doses of gamma radiation on the photosynthetic pigments of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation: (a) chlorophyll, (b) chlorophyll a/chlorophyll b, (c) carotenoids, and (d) anthocyanins. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01.
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Figure 4. Effect of different doses of gamma radiation on the essential oil of summer savory plants emerged from gamma radiation-treated seeds: (a) essential oil percentage, (b) essential oil yield, and (c,d) yield of essential oil components. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01.
Figure 4. Effect of different doses of gamma radiation on the essential oil of summer savory plants emerged from gamma radiation-treated seeds: (a) essential oil percentage, (b) essential oil yield, and (c,d) yield of essential oil components. Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. Bars represent mean value of three replications ± standard deviation. ** Significant differences at p ≤ 0.01.
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Figure 5. PCA map showing the relationship among the photosynthesis, growth, morphology, physiology, and secondary-metabolite characteristics of summer savory and doses (0, 50, 100, 200, and 300 Gray) of gamma radiation.
Figure 5. PCA map showing the relationship among the photosynthesis, growth, morphology, physiology, and secondary-metabolite characteristics of summer savory and doses (0, 50, 100, 200, and 300 Gray) of gamma radiation.
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Table 1. Physicochemical characteristics of the potting soil.
Table 1. Physicochemical characteristics of the potting soil.
TextureSand (%)Clay (%)Loam (%)PHEC (dsm−1)N (%)P (%)K (%)
Sand–loam58.215.226.66.12.80.0834525
EC, electrical conductivity. Values are average of three replications.
Table 2. Parameters obtained from OJIP transient, including their abbreviations, formulas, and definitions.
Table 2. Parameters obtained from OJIP transient, including their abbreviations, formulas, and definitions.
AbbreviationEquationDefinition
FV/FMTR0/ABS = [1 − (F0/FM)]Relative maximal variable fluorescence
ABS/RCM0 (1/VJ) (1/ϕP0)Light absorbance by PSII antenna chlorophylls based on reaction center
TR0/RCM0 (1/VJ)Trapped energy flux per reaction center
ET0/RCM0 (1/VJ) ψ0Flux of electron transport on the basis of reaction center
DI0/RC(ABS/RC) − (TR0/RC)Flux of energy dissipated as heat, fluorescence, or transferred to the other systems at time 0
PIABS(RC/ABS) × (ϕP0/(1 − ϕP0)) × (ψ0/(1 − ψ0))Performance index per absorbed light
Table 3. Effect of different doses of gamma radiation on the morphological traits of summer savory in the flowering stage obtained from seeds treated with gamma radiation.
Table 3. Effect of different doses of gamma radiation on the morphological traits of summer savory in the flowering stage obtained from seeds treated with gamma radiation.
Gamma Radiation (Gray)Plant Height (cm)Number of BranchesNumber of NodesNumber of LeavesLeaves Length (cm)
034.667 ± 0.75 a14.667 ± 0.66 d29.111 ± 0.66 b84.889 ± 0.66 a4.694 ± 0.125 a
5032.583 ± 0.33 b18.111 ± 0.66 c28.333 ± 0.50 b86.444 ± 0.66 a4.417 ± 0.20 bc
10034.111 ± 1.08 ab28.111 ± 0.33 b33.778 ± 0.66 a86.111 ± 0.66 a4.250 ± 0.12 c
20032.778 ± 0.83 b33.111 ± 1.33 a34.778 ± 0.5 a81.778 ± 1.33 b4.583 ± 0.08 ab
30029.833 ± 0.50 c19.444 ± 0.16 c26.667 ± 1.16 c77.778 ± 0.83 c4.361 ± 0.04 bc
*********
Gamma Radiation (Gray)Stem Diameters (mm)Root Length (cm)
01.820 ± 0.06 d4.333 ± 0.25 c
502.100 ± 0.02 bc6.500 ± 0.37 a
1001.967 ± 0.15 cd6.333 ± 0.25 a
2002.377 ± 0.12 a4.667 ± 0.25 bc
3002.217 ± 0.02 ab5.167 ± 0.12 b
****
Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. All values are means ± standard deviation. ** Significant differences at p ≤ 0.01. * Significant differences at p ≤ 0.05.
Table 4. Different doses of gamma radiation affect the growth characteristics of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation.
Table 4. Different doses of gamma radiation affect the growth characteristics of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation.
Gamma Radiation (Gray)Shoot Fresh Weight (g)Shoot Dry Weight (g)Root Fresh Weight (g)Root Dry Weight (g)
017.420 ± 0.79 bc3.600 ± 0.28 b3.865 ± 0.10 a0.325 ± 0.01 a
5015.313 ± 0.245 d2.810 ± 0.15 c3.935 ± 0.11 a0.320 ± 00 a
10023.203 ± 1.365 a4.563 ± 0.17 a2.597 ± 0.14 b0.300 ± 0.04 a
20018.373 ± 0.50 b3.937 ± 0.34 b2.325 ± 0.04 c0.325 ± 0.01 a
30016.583 ± 0.84 cd2.963 ± 0.33 c1.515 ± 0.01 d0.255 ± 0.02 b
*******
Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. All values are means ± standard deviation. ** Significant differences at p ≤ 0.01. * Significant differences at p ≤ 0.05.
Table 5. Effect of different doses of gamma radiation on the soluble sugar, starch, total phenol, and total flavonoid contents of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation.
Table 5. Effect of different doses of gamma radiation on the soluble sugar, starch, total phenol, and total flavonoid contents of summer savory plants in the flowering stage obtained from seeds treated with gamma radiation.
Gamma Radiation (Gray)Soluble Sugar (mg/gFW)Starch (mg/gFW)Total Phenol (mg Galic Acid/gFW)Total Flavonoid (mg Quercetin/gFW)
031.805 ± 3.34 c11.550 ± 11.54 c2.878 ± 0.07 e0.407 ± 0.008 b
5047.041 ± 3.43 b12.166 ± 12.16 c3.049 ± 0.07 d0.503 ± 0.01 a
10085.878 ± 10.03 a88.609 ± 88.60 a3.448 ± 0.07 c0.509 ± 0.02 a
20052.589 ± 7.74 b25.465 ± 25.46 b3.613 ± 0.07 b0.518 ± 0.02 a
30047.922 ± 2.37 b12.255 ± 12.25 c4.086 ± 0.07 a0.525 ± 0.02 a
********
Gamma Radiation (Gray)Phenol Yield (mg Galic Acid/Plant)Flavonoid Yield (mg Quercetin/Plant)
050.132 ± 1.23 c7.093 ± 0.15 d
5046.695 ± 1.08 d7.705 ± 0.28 d
10080.002 ± 1.64 a11.818 ± 0.51 a
20066.380 ± 1.10 b9.485 ± 0.40 b
30067.767 ± 1.17 b8.711 ± 0.36 c
****
Experiments were analyzed using a completely randomized design. Different letters indicate significant differences between treatments according to Duncan’s multiple range test at the 95% confidence level. All values are means ± standard deviation. ** Significant differences at p ≤ 0.01.
Table 6. Effect of gamma radiation on essential oil yield and composition of summer savory.
Table 6. Effect of gamma radiation on essential oil yield and composition of summer savory.
RICompoundDifferent Doses of Gamma Radiation (Gray)
050100200300
929α-thujene1.791.551.291.360.24
937α-pinene1.030.850.740.770.15
973sabinene0.13____
980β-pinene0.440.360.350.39_
985myrcene2.422.352.172.170.86
1011α-phellandrene0.390.370.350.35_
1022α-terpinene4.934.744.354.531.94
1031ρ-cymene1.782.072.934.273.21
1035limonene0.360.360.370.40_
10381,8-cineole0.240.280.250.300.07
1049E-B-ocimene0.13____
1067γ-terpinene45.5544.9845.6349.5228.31
1076cis-sabinene hydrate___0.270.32
1105linalool_0.48_0.210.31
1164borneol____0.15
1169terpinene-4-ol0.15_0.200.210.30
1257carvacrol methyl ether_0.430.13__
1294thymol0.200.84_0.311.55
1306carvacrol39.4539.4339.2933.5360.41
1354carvacrol acetate0.230.280.230.260.38
1424(E)-caryophyllen0.300.280.390.530.73
1499bicyclogermacrene0.14____
1506β-bisabolene0.340.370.560.621.07
The retention indices (RIs) of the compounds were determined via the co-injection of a homologous series of n-alkanes C8–C24 on the DB-5 column, _ not detected.
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Mohammadi, V.; Zare Mehrjerdi, M.; Rastogi, A.; Gruda, N.S.; Aliniaeifard, S. Effects of Seed Priming with Gamma Radiation on Growth, Photosynthetic Functionality, and Essential Oil and Phytochemical Contents of Savory Plants. Horticulturae 2024, 10, 677. https://doi.org/10.3390/horticulturae10070677

AMA Style

Mohammadi V, Zare Mehrjerdi M, Rastogi A, Gruda NS, Aliniaeifard S. Effects of Seed Priming with Gamma Radiation on Growth, Photosynthetic Functionality, and Essential Oil and Phytochemical Contents of Savory Plants. Horticulturae. 2024; 10(7):677. https://doi.org/10.3390/horticulturae10070677

Chicago/Turabian Style

Mohammadi, Vahideh, Mahboobeh Zare Mehrjerdi, Anshu Rastogi, Nazim S. Gruda, and Sasan Aliniaeifard. 2024. "Effects of Seed Priming with Gamma Radiation on Growth, Photosynthetic Functionality, and Essential Oil and Phytochemical Contents of Savory Plants" Horticulturae 10, no. 7: 677. https://doi.org/10.3390/horticulturae10070677

APA Style

Mohammadi, V., Zare Mehrjerdi, M., Rastogi, A., Gruda, N. S., & Aliniaeifard, S. (2024). Effects of Seed Priming with Gamma Radiation on Growth, Photosynthetic Functionality, and Essential Oil and Phytochemical Contents of Savory Plants. Horticulturae, 10(7), 677. https://doi.org/10.3390/horticulturae10070677

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