Effect of Harvesting Time on Chemical Components of Sage (Salvia officinalis L.) From Iran
الموضوعات : Research On Crop EcophysiologyAhmad Reza Golparvar 1 , Amin Hadipanah 2 , HAMIDEH ZAMANPOUR SHAHMANSOURI 3
1 - Department of Plant Breeding, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran
2 -
3 - Department of Plant Biology, Faculty of Sciences, Shahrekord University, Shahrekord, Iran
الکلمات المفتاحية: Keywords: Salvia officinalis L., Chemical constitutes, Essential oil, Harvest time.,
ملخص المقالة :
ABSTRACT Sage (Salvia officinalis L.) is perennial shrub and is one of the most important medicinal plants of the Lamiaceae family. The objective of this study was to evaluate the effect of different harvesting stages on contents, and essential oil components of sage. The essential oil from the aerial parts of the plant that were collected at different times was extracted by hydro-distillation in 2021 in the province of Isfahan in center Iran. Plants were harvested in four stages, i.e. the before blooming, beginning of blooming, full blooming and fruit stage. Results of mean comparisons revealed that the highest oil percentage (1.7%) was obtained at the stage of before blooming and the lowest oil percentage (0.36%) was obtained at the stage of fruit set. Based on results obtained from GC/MS analysis, in total, 39, 36, 32 and 37 constituents were identified in the essential oils of sage in the before blooming, beginning of blooming, full blooming and fruit stages, respectively. The major identified essential oil compounds were α-thujone (26.18–39.53%), camphor (10.39–19.78%), β-thujone (4.65–14.12%) and 1,8-cineol (7.75–13.98%). α-thujone as one of the major constituents of all samples was lower in the stage of before blooming (26.18%) and gradually increased in subsequent harvesting times to reach a maximum in the fruiting set (39.53%). Camphor was another compound where the highest (19.78%) was observed in beginning of blooming stage. The results showed that the harvesting time may have a significant effect on the essential oil yield and composition of sage. Our findings in sage, may pave the way to optimize the quality and quantity of sage essential oil to identify the best harvest time for pharmaceutical industries.
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Mohammadi-Cheraghabadi M, Modarres-Sanavy SAM, Sefidkon F, Mokhtassi-Bidgoli A, Hazrati S. 2023. Harvest time explains substantially more variance in yield, essential oil and quality performances of Salvia officinalis than irrigation and putrescine application. Physiology and Molecular Biology of Plants. 29(1): 109-20.
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Ahmad reza golparvar1, Amin Hadipanah2, Hamideh Zamanpour Shahmansouri2
1-Department of Agronomy and plant Breeding, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan, Iran
2-Department of Plant Biology, Faculty of Sciences, Shahrekord University, Shahrekord, Iran
* Corresponding author. E-mail address: dragolparvar@gmail.com
Received: 5 June 2023 Accepted: 6 July 2023
Abstract
Sage (Salvia officinalis L.) is perennial shrub and is one of the most important medicinal plants of the Lamiaceae family. The objective of this study was to evaluate the effect of different harvesting stages on contents, and essential oil components of sage. The essential oil from the aerial parts of the plant that were collected at different times was extracted by hydro-distillation in 2021 in the province of Isfahan in center Iran. Plants were harvested in four stages, i.e. the before blooming, beginning of blooming, full blooming and fruit stage. Results of mean comparisons revealed that the highest oil percentage (1.7%) was obtained at the stage of before blooming and the lowest oil percentage (0.36%) was obtained at the stage of fruit set. Based on results obtained from GC/MS analysis, in total, 39, 36, 32 and 37 constituents were identified in the essential oils of sage in the before blooming, beginning of blooming, full blooming and fruit stages, respectively. The major identified essential oil compounds were α-thujone (26.18–39.53%), camphor (10.39–19.78%), β-thujone (4.65–14.12%) and 1,8-cineol (7.75–13.98%). α-thujone as one of the major constituents of all samples was lower in the stage of before blooming (26.18%) and gradually increased in subsequent harvesting times to reach a maximum in the fruiting set (39.53%). Camphor was another compound where the highest (19.78%) was observed in beginning of blooming stage. The results showed that the harvesting time may have a significant effect on the essential oil yield and composition of sage. Our findings in sage, may pave the way to optimize the quality and quantity of sage essential oil to identify the best harvest time for pharmaceutical industries.
Keywords: Salvia officinalis L., Chemical constitutes, Essential oil, Harvest time.
Introduction
Salvia spp., with more than 1000 species, is categorized as the largest and important genus belongs to the Mentheae tribe within the Nepetoideae subfamily of the Lamiaceae family. The genus salvia in three regions of the world: Central and South America (500 spp.), Western Asia (200 spp.) and Eastern Asia (100 spp.). The genus Salvia in Iran includes 58 species, 17 of which are endemic (Walker et al., 2004; Kharazian, 2014). Sage (S. officinalis L.) is an herbaceous, perennial plant, evergreen with woody stems and gray-green leaves. Sage is native to the Middle East and the Mediterranean region and cultivated throughout the world (Golparvar and Hadipanah, 2013).
The leaves of sage, contain essential oil widely used as a raw material in pharmaceutical, perfumery, and food industries (Martins et al., 2015). According to the reviewed literature, the sage plant has shown various biological activities including antibacterial, antiviral, antifungal, antioxidant, anti-diabetes, anticholinesterase, antispasmodic, anti-inflammatory properties, and also sage essential oil is traditionally used to treat diseases including bronchitis, menstrual disorders, colds, bleeding and tuberculosis (Eidi and Eidi, 2009; Abu-Darwish et al., 2013; Kontogianni et al., 2013; Dammak et al., 2019; Golparvar et al., 2017; Ilić et al., 2023). According to the results of phytochemical analysis of sage plant, the main constitutes of the oils are monoterpenes (α–and β-thujone, 1,8–cineole, camphor, borneol and etc.), sesquiterpenes (caryophyllene oxide and viridiflorol), and other compounds include alkaloids and phenolics (coumarins and flavonoids) (Lu and Foo, 2000; Vosoughi et al., 2018; Ilić et al., 2023).
Harvesting time can be suggested according to area and its environmental conditions. So that, the type and amount of essential oil compounds are functions of environmental factors (Hadipanah et al., 2011). For example, Mirza et al. (2011) reported the major constituents of essential oils in (S. officinalis L.) at early, full and after flowering stages were α-thujene (20.8%, 27.1%, 35/9%) camphor (29.2%, 14.6%, 17.2%) and β-thujene (15.1%, 14.6%, 4.1%), respectively. In addition, results a study by Baranauskiene et al. (2011) indicated that α-thujone as one of the major constituents of sage were from May 23 to June 20 steadily increased from 29.4 to 39.7% and also viridiflorol was another compound where from May 23 to June 7 increased at the same period. In a study by Mohammadi-Cheraghabadi et al. (2023) the highest essential oil yield and concentrations of borneol, camphor and α-thujone of S. officinalis were higher in summer than spring. These quantitative characters may depend on the cultivation the climatic conditions (the soil water amount, the temperature, the light intensity) (Letchamo et al., 1994) or may be genetically determined (Ložien and Venskutonis, 2003). Controlled growth systems also make it feasible to contemplate manipulation of phenotypic variation in the concentration of medicinally important compounds present at harvest (Canter et al., 2005). Thus, the main objective of this study was to determine the optimal harvest time for sage essential oil production.
Materials and methods
Plant material
Sage (S. officinalis) seeds were obtained from Pakan Bazr Company, Isfahan, Iran. In the spring 2021, the seedlings of S. officinalis were transplanted to research farm at Islamic Azad University, Khorasgan (Isfahan) (Isfahan, Iran) with the geographical coordinates of 32º 38' N, 51º 47' E (1550 m above sea level). The climate of the area of study is classified as arid and warm region (according to the Koppen climate classification). According to the soil analysis, the soil at the experimental site was categorized as a clay loam (based on the soil texture triangle). The results of soil chemical analysis were; pH 7.25, E.C. = 2.5 dS m-1, and contains total N (0.43 %), total P2O5 (26 ppm) and total K2O (287 ppm).
Experimental design and treatments
The experiment was done in a split plot arrangement based on the randomized complete block design (RCBD) with three replications. Each experimental plot was 2.5×5 m, and plants were grown in 5 rows, with a spacing of 30 cm in rows 50 cm apart per replication. During the growth time, irrigation was performed according to the crop’s needs in relation to the soil properties. Weeding was performed by hand. There were no pests or diseases observed during the plant growth. Finally, the aerial parts of sage harvested in four stages, i.e. the before blooming, beginning of blooming, full blooming and fruit set in September 2022.
Essential Oil Extraction
In order to measure the essential oil content of the harvested material, the aerial parts of the plants were cut at a height of 10 cm above soil levels and dried under shade at room temperature (25 ± 5 °C) for 10 days. For about 100 g of dried aerial part of sage for three hours in Clevenger-type apparatus were subjected with 500 mL distilled water to hydro-distillation, then for drying obtained oils, anhydrous sodium sulphate applied and before analysis stored in sealed vials at 4 °C. The obtained oils essential oils were clear and yellow liquid.
GC/MS analysis
Compositions of the essential oils were determined by GC–MS. The GC/MS analysis was carried out with an Agilent 5975 GC-MSD system. HP-5MS column (30 m x 0.25 mm, 0.25 μm film thickness) was used with helium as carrier gas with flow rate of 1.0 mL/min. The oven temperature was kept 20°C at 50°C for 4 min and programmed to 280°C at a rate of 5°C /min, and kept 20°C constant at 280 °C for 5 min, at split mode. The injector temperature was at 20°C at 280°C. Transfer 20 line temperatures 280°C. MS were taken at 70 eV. Mass range was from m/z 35 to 450. Identification of the essential oil components was accomplished based on comparison of retention times with those of authentic standards and by comparison of their mass spectral fragmentation patterns (WILLEY/ChemStation data system) (Adams, 2017).
Statistical analysis
The data was statistically analyzed by SPSS16 software, the experiment was done in a split plot arrangement based on the randomized complete block design (RCBD) with three replications. For means comparison analysis was used Duncan’s multiple range test method (DMRT) at p ≤ 0.05 level.
Results and discussion
Results of this study indicated that harvesting time affected (P < 0.01) on plant height, fresh weight and dry weight of sage (Fig. 1A & B). According to Figure 1A and B, results of mean comparisons plant height, fresh weight and dry weight revealed that the highest plant height (32.29 cm), fresh weight (3467.7 kg/ha) and dry weight (1236.65 kg/ha) were observed at the stage of fruit set and the lowest plant height (19.57 cm), fresh weight (1451.5 kg/ha) and dry weight (391.6 kg/ha) were obtained at the stage of before blooming setting.
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Figure 1. Effect of harvesting time on plant height (A), fresh weight and dry weight (B) in sage (Salvia officinalis L.). Different letters above the bars indicate statistically significant differences (P < 0.01).
The essential oil extracted from the sage aerial parts was colorless or pale yellow. Therefore, based on the extraction of essential oils by the hydro-distillation method with a Clevenger-type apparatus, a significant difference was observed in the amount of essential oil yielded in different harvesting time. The higher yield of essential oil was observed from before blooming (1.7 %) and the lowest amount of essential oil was observed from fruit stage (0.36 %). The results of the analysis of the constituents of the essential oil are reported in Table 1. Based on results obtained from GC/MS analysis, a total of 39, 36, 32 and 37 compounds were identified in the essential oils of sage in the before blooming, beginning of blooming, full blooming and fruit stages, respectively. The results of the experiment showed that the quality of the essential oil was affected by the harvest time at different stages. Results of this study demonstrated that main volatile oil components were monoterpenes. The major identified essential oil compounds were α-thujone (26.18–39.53%), camphor (10.39–19.78%), β-thujone (4.65–14.12%) and 1,8-cineol (7.75–13.98%).
Table 1. The effect of harvesting time on chemical compositions of the essential oil from S. officinalis
No | Compound | RI | Before blooming | Beginning of blooming | Full blooming | Fruit set | ANOVA |
| Monoterpene hydrocarbons |
|
|
|
|
|
|
1 | Cis-Salvene | 852 | 0.33 ± 0.03 | 1.21 ± 0.05 | 0.00 ± 0.00 | 0.17 ± 0.07 |
|
2 | Trans-Salvene | 859 | 0.08 ± 0.02 | 0.94 ± 0.05 | 0.24 ± 0.04 | 0.02 ± 0.01 |
|
3 | Tricyclene | 915 | 0.00 ± 0.00 | 0.28 ± 0.03 | 0.03 ± 0.01 | 0.21 ± 0.07 |
|
4 | Thujene | 928 | 0.21 ± 0.04 | 0.06 ± 0.02 | 0.00 ± 0.00 | 0.00 ± 0.00 |
|
5 | α-Pinene | 937 | 3.89 ±0.21c | 7.63 ± 0.64a | 5.43 ± 0.54b | 6.91 ± 0.84ab | p ≤ 0.01 |
6 | Camphene | 955 | 4.58 ± 0.12a | 3.86 ± 0.11ab | 2.98 ± 0.09b | 3.76 ± 0.06ab | p ≤ 0.01 |
7 | Sabinene | 974 | 0.15 ± 0.02 | 0.12 ± 0.03 | 0.25 ± 0.05 | 0.49 ± 0.04 |
|
8 | β-Pinene | 978 | 1.03 ± 0.04 | 2.47 ± 0.03 | 0.95 ± 0.06 | 0.36 ± 0.05 |
|
9 | 1-Octan-3-ol | 985 | 0.65 ± 0.02 | 0.00 ± 0.00 | 0.21 ± 0.01 | 0.04 ± 0.02 |
|
10 | Myrcene | 992 | 0.44 ± 0.11 | 0.67 ± 0.02 | 0.47 ± 0.03 | 0.52 ± 0.01 |
|
11 | 3-Octanol | 995 | 0.07 ± 0.03 | 0.00 ± 0.00 | 0.01 ± 0.01 | 0.02 ± 0.01 |
|
12 | α -Phellandrene | 999 | 0.28± 0.04 | 0.05 ± 0.01 | 0.23 ± 0.02 | 0.41 ± 0.04 |
|
13 | α-Terpinene | 1008 | 1.19 ± 0.00 | 0.37 ± 0.01 | 0.05 ± 0.02 | 0.01 ± 0.00 |
|
14 | p-Cymene | 1021 | 1.57± 0.23 | 1.21 ± 0.12 | 0.01 ± 0.01 | 0.52 ± 0.02 |
|
15 | Limonene | 1025 | 1.95± 0.26 | 1.17 ± 0.15 | 0.97 ± 0.05 | 0.65 ± 0.07 |
|
16 | 1,8-Cineole | 1027 | 7.75 ± 0.36b | 8.65 ± 0.47b | 11.73 ± 0.74ab | 13.98 ± 0.98a | p ≤ 0.01 |
17 | Cis -Ocimene | 1030 | 0.01 ± 0.01 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
|
18 | γ-Terpinene | 1044 | 0.61 ± 0.02 | 0.67 ± 0.03 | 0.85 ± 0.05 | 0.35 ± 0.01 |
|
19 | Cis- Sabinene hydrate | 1050 | 0.05 ± 0.01 | 0.18 ± 0.02 | 0.00 ± 0.00 | 0.21 ± 0.01 |
|
20 | Linalool oxide | 1076 | 0.12 ± 0.02 | 0.42 ± 0.05 | 0.00 ± 0.00 | 0.00 ± 0.00 |
|
21 | α-Terpinolene | 1083 | 0.23 ± 0.02 | 0.61 ± 0.06 | 1.24 ± 0.21 | 0.68 ± 0.11 |
|
22 | Trans-Sabinene hydrate | 1093 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.01 ± 0.00 | 0.24 ± 0.02 |
|
23 | Linalool | 1099 | 0.82 ± 0.02 | 0.01 ± 0.01 | 1.26 ± 0.35 | 0.95 ± 0.22 |
|
24 | α-Thujone | 1107 | 26.18 ± 1.05b | 27.67 ± 0.87b | 34.47 ± 1.35ab | 39.53 ± 1.15a | p ≤ 0.01 |
25 | β-Thujone | 1115 | 14.12 ± 0.97a | 10.89 ± 1.24ab | 9.36 ± 0.64ab | 4.65 ± 0.09b | p ≤ 0.01 |
26 | α-Campholene aldehyde | 1119 | 0.00 ± 0.00 | 0.01 ± 0.01 | 0.00 ± 0.00 | 0.00 ± 0.00 |
|
27 | Camphore | 1126 | 18.41 ± 0.68a | 19.78 ± 1.23a | 15.45 ± 0.98ab | 10.39 ± 0.87b | p ≤ 0.01 |
28 | Borneol | 1163 | 5.47 ± 0.41ab | 2.69 ± 0.11b | 6.36 ± 0.25a | 6.85 ± 0.33a | p ≤ 0.01 |
29 | Terpinene-4-ol | 1177 | 0.62 ± 0.03 | 0.17 ± 0.01 | 0.68 ± 0.02 | 0.41 ± 0.01 |
|
30 | α-Terpineol | 1188 | 0.34 ± 0.04 | 0.46 ± 0.05 | 0.04 ± 0.01 | 0.32 ± 0.02 |
|
31 | Trans-Sabinyl acetate | 1289 | 0.01 ± 0.01 | 0.00 ± 0.00 | 0.01 ± 0.00 | 0.06 ± 0.02 |
|
32 | Carvacrol | 1300 | 0.41 ± 0.02 | 0.00 ± 0.00 | 0.00 ± 0.00 | 0.00 ± 0.00 |
|
33 | Carvacryl acetate | 1352 | 0.01 ± 0.01 | 0.01 ± 0.00 | 0.00 ± 0.00 | 0.01 ± 0.01 |
|
| Sesquiterpenes hydrocarbons |
|
|
|
|
|
|
34 | β-Caryophyllene | 1418 | 1.99 ± 0.25 | 0.32 ± 0.08 | 0.72 ± 0.04 | 0.28 ± 0.02 |
|
35 | α-Humulene | 1452 | 0.67 ± 0.05 | 0.38 ± 0.03 | 0.02 ± 0.01 | 0.01 ± 0.01 |
|
36 | Naphthalene | 1480 | 0.25 ± 0.02 | 0.01 ± 0.01 | 0.41 ± 0.03 | 0.05 ± 0.01 |
|
37 | Ledene | 1499 | 0.01 ± 0.00 | 0.08 ± 0.02 | 0.00 ± 0.00 | 0.02 ± 0.01 |
|
| Oxygenated Sesquiterpenes |
|
|
|
|
|
|
38 | Caryophyllene oxide | 1582 | 0.31 ± 0.09 | 1.57 ± 0.21 | 0.01 ± 0.01 | 0.35 ± 0.04 |
|
39 | Viridiflorol | 1591 | 3.82 ± 0.45ab | 2.39 ± 0.21b | 4.02 ± 0.84a | 4.32 ± 0.45a | p ≤ 0.01 |
40 | β-Selinene | 1604 | 0.08 ± 0.01 | 0.82 ± 0.07 | 0.06 ± 0.02 | 0.01 ± 0.01 |
|
41 | Humullene epoxide П | 1606 | 0.01 ± 0.01 | 0.01 ± 0.00 | 0.00 ± 0.00 | 0.02 ± 0.01 |
|
42 | Manool | 2056 | 0.75 ± 0.02 | 0.41 ± 0.03 | 0.01 ± 0.01 | 0.01 ± 0.00 |
|
| Total |
| 99.47 | 98.25 | 98.52 | 97.78 |
|
| Oil yield (%) | - | 1.7a | 0.98ab | 0.57b | 0.36c |
|
Means ± SD with different letter in a row are statistically significant at 5% level probability by DMRT (Duncan’s multiple range test) method; RI = Retention indices in elution order from DB-5 column.
Many environmental factors, such as plant genetic, geographical origin, weather conditions, geobotanical conditions, cultivation method, stress type, time of plant collection, storage method, plant age, extraction method, herbivore or microbial attack, and genetic changes, can play an important role in changing the composition of the extracted essential oils from medicinal plants (Letchamo et al., 1994; Ložien and Venskutonis, 2003; Thompson et al., 2003; Golparvar and Hadipanah, 2024). While the percentage of each major constituent in the oil was found to vary during all the harvesting times. Among the terpenoids, α-thujone had the highest value among the identified compounds. Among the harvest time, the highest (39.53%) and lowest (26.18%) values of α-thujone were related to fruit stage and before blooming stage, respectively. In addition, camphore was another dominant compound in all stages of the harvesting times. The highest (19.78%) and lowest (10.39%) values of this compound were obtained from beginning of blooming stage and fruit stage, respectively. Another dominant compound was β-thujone, according to results showing the highest (14.12 %) and lowest (4.65 %) amounts were related to before blooming stage and fruit stage, respectively. 1,8-cineole and borneol were other compounds whose highest values were obtained in fruit stage with 13.98% and 6.85% values, respectively. Other identified aroma compounds included α-pinene, camphene and viridiflorol, but all in much smaller quantities. To the best of our knowledge, two harvest times in sage, including fruit stage and before blooming stage are suggested, considering the yield, quantity and quality of the essential oil. Moreover, it is known that terpenoid synthesis proceeds through a variety of intermediates and that thujones (is a ketone and a monoterpene that occurs in two diastereomeric forms: α-thujone and β-thujone) and camphor originate from different reactive carbocations. Dominance of one or the other compound in the essential oil of sage should be reasonably correlated with the activation of the specific metabolic pathway (Croteau and Karp, 1976).
For example, Hazrati et al. (2022) reported that the effect of harvesting times (day/night) have a significant effect on essential oil yield and composition of (Salvia officinalis). They stated the quantitative and qualitative properties of essential oil in sage are subjected to significant hourly changes (different hours of the day and night) during the day/night time. In addition, results a study by Arraiza et al. (2012) indicated that the highest oil yield of (Salvia officinalis L.) was obtained in the stage of full flowering and the highest concentration of α-thujone (40.1 - 46.5%) in the period of initial flowering. In another study the yield of essential oil of sage in different stages was floral budding (0.9%), vegetative (0.7%), flowering (0.5%), immature fruit (0.4%) and ripen fruit (0.2%) (Hossein Mirjalili et al., 2006). Results of a study by Golparvar et al. (2012) indicated that the highest thymol content of Thymus daenensis obtained at the stage of before blooming, also Salehi et al. (2014) reported the optimum of harvest time of Thymus vulgaris was extracted at the beginning of flowering stage. A comparison of our results with different reports, differences in the volatile composition of the plants could be attributed to genetic (genus, species, and ecotype), chemotype, distinct environmental and climatic conditions, seasonal sampling periods, geographic origins, plant populations, vegetative plant phases, and extraction and quantification methods.
Conclusion
The results obtained in our study indicated that the highest plant height, fresh weight and dry weight obtained at fruit set stage. Also, the results showed that the harvesting time have a significant effect on the essential oil yield and composition of sage. To gain the highest essential oil yield, the best harvesting time was found at before blooming stage. α-thujone was detected at the highest amount when the plants were collected at fruit stage and lowest value was obtained at before blooming stage. In addition, camphor was another dominant compound, and the highest amount of this compound was obtained in beginning of blooming stage. Our findings clearly demonstrate that there are notable changes to the essential oil's quantitative and qualitative characteristics during harvesting time.
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