Metabolic modulation of Basil (Ocimum basilicum L.): an insight into growth, metabolomics and antioxidant activity under varying temperature and light conditions

Ryu, Da Hye; Cho, Jwa Yeong; Hamayun, Muhammad; Lee, Dong Gyu; Kim, Ho-Youn

doi:10.1186/s40538-023-00532-2

Metabolic modulation of Basil (Ocimum basilicum L.): an insight into growth, metabolomics and antioxidant activity under varying temperature and light conditions

Research
Open access
Published: 15 January 2024

Volume 11, article number 10, (2024)
Cite this article

Download PDF

You have full access to this open access article

Chemical and Biological Technologies in Agriculture Submit manuscript

Metabolic modulation of Basil (Ocimum basilicum L.): an insight into growth, metabolomics and antioxidant activity under varying temperature and light conditions

Download PDF

Da Hye Ryu¹^na1,
Jwa Yeong Cho^1,2^na1,
Muhammad Hamayun³,
Dong Gyu Lee¹ &
…
Ho-Youn Kim^1,2

960 Accesses
Explore all metrics

Abstract

Background

Temperature and light are two critical environmental stimuli that greatly impact our agricultural industry. We explored the effects of varying temperature and light conditions on the metabolomics of basil, a plant widely used in cuisine and for medicinal purposes worldwide. Basil plants were subjected to elevated temperatures of 30 °C, 35 °C, and 40 °C, along with two light intensities (D11 and D23).

Results

Our results showed that the maximum shoot length (42.98 cm) was achieved at T30 and D23, the maximum leaf area (6.92 cm) at T30/D11, and the highest number of leaves (472) at T40/D11. However, at the higher temperature of T40, the number of leaves increased, but shoot length and leaf size significantly decreased (p < 0.05). Maxim shoot biomass (81 gm) and root biomass (91.2 gm) was recorded at T35/D23 treatments. Metabolomic studies of basil revealed that rosmarinic acid (RA), and linalool and eugenol were the major phenolic and volatile organic compounds (VOCs) under different growth conditions. RA levels were higher at 30 °C, correlated with elevated shikimate levels, indicating a carbon supply through the TCA cycle. In contrast, the growth conditions of 35 °C/D11 (μmol/m²/d) up-regulated the glyoxylate cycle (fumaric acid and malic acid) as part of stomatal closure, preventing ROS accumulation and resulting in increased VOC emission. Exposure to the higher temperature of 40 °C induced higher amino acid accumulation, improving temperature stresstolerance.

Conclusions

This study suggests that elevated temperature and light intensity affected the overall health of basil plants by modulating underlying growth mechanisms. Furthermore, elevated temperature plays a vital role in plant defense mechanisms by mediating the production of secondary metabolites associated with plant defense responses.

Graphical Abstract

γ-Aminobutyric acid (GABA) priming alleviates acid-aluminum toxicity to roots of cree** bentgrass via enhancements in antioxidant defense and organic metabolites remodeling

Article 19 June 2024

Mitigation of drought stress in Zea mays L. through plant growth-promoting rhizobacteria assisted by foliar sorghum water extract

Article 14 June 2024

Exploration of Drought Tolerant PGPR and Their role in Regulating Antioxidant Enzymes in Maize (Zea mays L.)

Article 17 June 2024

Introduction

Plants are sensitive to environmental stimuli and adaptable to changes in their surroundings [1]. Temperature and light are the most critical environmental cues that influence the growth and development of plants by providing seasonal information [2]. The interrelated and complex effects of temperature and light trigger various plant responses. Light significantly contributes to acclimation responses to both low and high temperatures and can influence the extent of stress damage [3]. Plant photoreceptors, like phytochrome and cryptochrome, crucially recognize the quality, quantity, and direction of light, as well as temperature sensing. They differentially affect phytohormone signaling based on temperature levels [1, 4, 5]. Photoreceptors are responsible for both light quality and high temperatures, showing that photo- and thermo-morphogenesis share a core signaling pathway, indicating their interdependence [6,7,8,9,10,11]. While normal conditions tend to counteract light signals in stem growth adjustment, a temporary temperature increase supports the light-induced inhibition of hypocotyl growth [12]. Karayekov, Sellaro [12] demonstrated that the high-temperature response in Arabidopsis depends on the presence or absence of light, with a significant effect in response to light but not in the dark. Additionally, various developmental processes, such as seed germination, seedling de-etiolation, vegetative growth, and flowering, are induced by unfavorable conditions [6, 7]. These responses are considered part of the defense mechanism activated by plants to perceive environmental stimuli and minimize damage from challenging conditions [2, 13].

Under unfavourable environmental conditions, such as heat stress, plants experience reduced productivity and shortened life cycles due to diminished photosynthetic efficiency and compromised photochemical reactions [14]. Additionally, secondary metabolite accumulation contributes to environmental adaptation and acts as a defense mechanism against external stimuli [15]. Temperature stress can also lead to the accumulation of reactive oxygen species (ROS) in plant cells, resulting in lipid peroxidation, enzyme inactivation, nucleic acid and protein degradation [Full size image

Status of VOCs under elevated temperature and light

We detected 44 VOCs that included 5 phenylpropenes, 16 monoterpenes, 15 sesquiterpenes, 5 aldehydes, and 3 other compound groups (Table 2). Linalool (monoterpene) and eugenol (phenylpropene) were identified as the major constituents of VOCs in basil, as displayed in Additional file 1: Fig. S2. Among the other components, relatively major compounds accounting for more than 1% on average were (E)-α-bergamotene (4.4%), eucalyptol (6.5%), α-terpineol (3.1%), and epi-α-cadinol (2.5%) and their quantification results were presented in Fig. 4. However, the distribution of total VOCs content, ranging from 163.8 µg/20 mg to 394.3 µg/20 mg, was determined by two main constituents (linalool and eugenol), which accounted for 26.2% and 48.1% on average. Under the lowest temperature condition (T30), a high DLI had a positive effect on phenolic compounds (TPC and RAC) as shown in Fig. 1, however had a negative effect on VOCs, as indicated in Table 3. Meanwhile, temperature stress-induced conditions (T35 and T40) and the lowest DLI (D11) stimulated VOCs production (Fig. 4). The highest content was observed in T35/D11 (361.9 ± 33.7 µg/20 mg), followed by T35/D23 (305.3 ± 25.7 µg/20 mg) and T40/D11 (293.4 ± 27.9 µg/20 mg). These opposite trends resulted in a negative correlation between the main VOCs, including linalool, eugenol, eucalyptol, (E)-α-bergamotene, α-terpineol, and epi-α-cadinol, with TPC (r = 0.1860, − 0.4271, − 0.6910, − 0.5997, − 0.7479, and − 0.3415, respectively) and RAC (r = 0.2366, − 0.4271, − 0.7481, − 0.6196, − 0.8166, and − 0.4138, respectively), as presented in Fig. 2.

Table 2 HS-SPME-GC-TOF–MS analysis for VOCs profiling and dynamic changes of basil

Full size table

Table 3 Summary table of two-way (factorial) ANOVA

Full size table

Analysis of antioxidant activities

DPPH and ABTS radical assays have been developed to spectrophotometrically monitor antioxidant activities as such assays are considered effective for screening and identifying the natural bioactivity of complex mixtures. We recorded higher activity in the ABTS assay (RC50 = 65.7 ± 15.8 μg/mL) compared to the DPPH assay (RC50 = 133.2 ± 3.2 μg/mL) as shown in Fig. 3. Notably, temperature was found a significant factor in antioxidant activity. Based on the temperature grou** (Fig. 3C, D), the T30 treatment exhibited stronger DPPH (RC50 = 107.1 ± 19.4 μg/mL) and ABTS radical scavenging activities (RC50 = 55.2 ± 5.7 μg/mL) compared to T35 (DPPH RC50 = 141.6 ± 29.7 μg/mL; ABTS RC50 = 66.3 ± 16.3 μg/mL) and T40 (DPPH RC50 = 150.9 ± 29.3 μg/mL; ABTS RC50 = 75.5 ± 16.3 μg/mL).

Under the same DLI conditions, higher activity was observed at lower temperatures, and this temperature-dependent trend became more pronounced at lower DLI levels, regardless of the experimental method. Therefore, strong correlations (p < 0.0001) were observed between phenolic contents and antioxidant activities (Fig. 2), as follows: TPC-DPPH: r = 0.6666; TPC-ABTS: r = 0.6632; RAC-DPPH: r = 0.5960; and RAC-ABTS: r = 0.5803. Considering the results categorized by temperature conditions, the highest functional value, as judged by TPC, RAC, and antioxidant activities of basil grown under T30 conditions, was clearly demonstrated.

ANOVA analysis

A two-way ANOVA analysis was performed to evaluate the effects of variables (temperature and DLI) on growth patterns, secondary metabolites (TPC, RAC, and VOCs), and antioxidant activities. While the production based on shoot weight was significantly influenced by the combination of temperature and DLI, not by single factors, a significant effect of temperature was observed in most cases (p < 0.05). In particular, a highly significant effect of temperature on TPC, RAC, and total VOCs was determined (p < 0.005). TPC and RAC showed a p value of less than 0.005 only with temperature as a factor, but total VOCs significantly changed with temperature alone and when combined with DLI.

Profiling of primary metabolites

Based on the secondary metabolite analysis and two-way ANOVA, it was elucidated that temperature primarily regulates the secondary metabolism of basil. We also conducted an analysis of primary metabolites in this study. The variables within the same category (such as organic acids, amino acids, sugars, and fatty acids) displayed positive correlations with one another, as indicated in Fig. 2. Furthermore, the results revealed that primary metabolites exhibited variations based on temperature, as illustrated in Fig. 5. Consequently, we averaged the results by temperature to facilitate interpretation. The total organic content and total sugar content decreased with rising temperatures, while the trend for total amino acids was the opposite. Notably, the highest total organic acids content was observed in the T30 condition (128.5 ± 21.3 μg/10 mg), which was approximately 1.17- and 1.29- times higher than the T35 (110.2 ± 16.2 μg/10 mg) and T40 (55.2 ± 16.4 μg/10 mg) conditions. The content of all observed organic acids (fumaric acid, malic acid, shikimic acid, and citric acid) related to the TCA cycle contributed significantly to the total organic acids content, with positive correlations (r = 0.7180, 0.8260, 0.8860, and 0.5643, respectively). In the T30 condition, it was observed that as DLI increased, the content of these organic acids and sugars also increased. Similarly, the total sugar content followed the same trend. T30 (90.5 ± 32.8 μg/10 mg) exhibited 1.64- and 3.64- times higher content compared to T35 (55.2 ± 16.4 μg/10 mg) and T40 (24.9 ± 3.5 μg/10 mg), respectively. Most sugar components, except for sucrose, displayed significantly positive correlations with total sugar content. In particular, glucose, which represented over 50% of the total sugar content, exhibited a very strong correlation with total sugar content (r value of 0.999). This is why the highest total sugar content was determined in T30/D23 (120.6 ± 8.0 μg/10 mg), where the glucose content was the highest (99.0 ± 6.9 μg/10 mg). Conversely, the total amino acids content exhibited a significant correlation within the total amino acids content. All detected amino acids, except for 5-oxoproline, showed positive correlations. The content of total amino acids was found to be 1.33 times higher in T40 (27.5 ± 2.2 μg/10 mg) compared to T30 (20.6 ± 2.7 μg/10 mg) and 1.32 times higher compared to T35 (20.8 ± 7.0 μg/10 mg).

Discussions

It is widely known that the preferred temperature range for most plant species typically falls within the range of 20 to 30 °C [38]. However, when plants are exposed to temperatures exceeding their optimal growth range by more than 5 °C, they experience stress, which triggers a variety of metabolic defense mechanisms and leads to the accumulation of secondary metabolites [39]. It's important to note that prolonged exposure to stressful conditions can lead to an acclimation process in plants. This acclimation results in increased stress tolerance, which is characterized by higher survival rates and enhanced production [3]. Therefore, there have been ongoing efforts to improve both production and functionality by modulating these factors. In this study, basil plants were subjected to elevated temperatures and light intensities (D11 and D23), and their responses were comprehensively analyzed through the evaluation of various metabolites, including both primary and secondary metabolites.

Plants within the Lamiaceae family, especially those with high levels of phenolic compounds, are considered valuable sources of natural substances for healthcare [40]. Basil, a member of the Lamiaceae family, contains various phenolic compounds such as caffeic acid, chicoric acid, caftaric acid, p-coumaric acid, and RA. The distribution of these phenolic compounds varies among basil species and cultivars [41, 42]. Among these compounds, RA has been identified as the most prevalent phenolic compound in sweet basil, as well as in other Lamiaceae species like thyme, marjoram, sage, rosemary, and lemon balm [43, 44]. RA content significantly influences the antioxidant properties of these plants, and a strong correlation has been found between phenolic content and antioxidant activities in various plant species [45, 46]. RA has also been reported to have various health-related properties, such as inducing melanogenesis, photoprotective effects, and anti-staphylococcus aureus and anti-inflammatory activities. These properties make RA valuable for industrial applications, such as in anti-acne products [47, 48]. Therefore, enhancing the content of RA in basil is crucial to make it more valuable with higher economic returns. Researchers have conducted various experiments to enhance the content of these substances in basil, including modifying cultivation conditions like drought stress, silver treatment, heat stress, and phytohormone treatments [49,50,51,52]. Basil exposed to temperature stress activates the accumulation of RA, which serves as a main component of the plant’s defense mechanism [53]. These findings are consistent with the previous results, where the highest TPC and RAC were observed under specific temperature conditions (T30). According to factorial ANOVA analysis, temperature alone showed a significant effect on TPC and RAC, while the combination of temperature and DLI did not have a significant effect. For the metabolomics aspect, prior research has also suggested that light intensity does not significantly affect the content of certain compounds in basil [54, 55]. This is in line with previous results where DLI alone or combined with temperature did not have a significant impact on TPC and RAC. Additionally, the non-significant combined effect was consistent with the previously mentioned decreased complex influence in tomatoes [56]. Furthermore, the elevated temperature induced significant changes in the VOCs contents. VOCs have numerous functions, such as mediating plant-plant interactions, facilitating plant-pathogen communication, repelling insects through chemotaxis, and attracting pollinators by releasing pheromones [57]. The production of VOCs in plants is a metabolic activity that varies in composition and quantity depending on the function, developmental stage, genotypes, species, site of biosynthesis, and environmental conditions [58]. A similar previous conducted on the effect of drought stress severity on the biosynthesis of phenylpropanoids and essential oils in basil reported a decreased gene expression (C4H, cinnamate 4-hydroxylase) in the upstream biosynthesis pathway and an increased gene expression (EOMT, eugenol O-methyltransferase; CVOMT, chavicol O-methyltransferase) [59]. Additionally, Rezaie, Abdollahi Mandoulakani [60] described that prolonged cold stress (over 48 h) did not show any difference in their expression compared to untreated plants. These previous studies highlighted the effect of certain plant VOCs that can be released in response to various abiotic and biotic stresses. For basil, two phenylpropanoids (eugenol and methyl chavicol) and two terpenoids (1,8-cineole and linalool) have been reported as the major compounds determining its flavor [61]. In this study, the main VOCs emitted by basil plants were linalool (monoterpene) and eugenol (phenylpropene), and significantly higher VOCs content was observed at the specific temperature of T35 conditions.

Primary metabolism is involved in a complex defense system by interacting with secondary metabolites and participating in reactions against environmental stressors. This involvement occurs through the regulation of carbohydrates, proteins, and lipids in plants [62]. Due to differences in secondary metabolism responses to light and temperature treatments, an attempt was made to confirm the mechanism differences through primary metabolite analysis. Temperature stress has been reported to alter respiration and photosynthesis in plants, resulting in a shortened life cycle and decreased plant productivity [63]. It also affects the activity of enzymes involved in the carbon flux of the chloroplast stroma [64]. However, it should be noted that the impact of stress can vary depending on the type, intensity, duration, and developmental stage of the plant [65]. In unstressed plants, normal photosynthetic processes occur, and glucose produced serves as an energy source through glycolysis [66]. However, when plants are exposed to photosynthetic stress, such as temperature stress, drought stress, or excessive light, the equilibrium between the production and scavenging of ROS is disrupted, leading to excessive ROS accumulation. Consequently, this is considered the initial stress response and can result in oxidative stress and damage to cell components [67]. This primarily occurs in chloroplasts, mitochondria, and peroxisomes in plants. To prevent excess ROS accumulation, the process of photorespiration is activated, dissipating excess reducing equivalents and energy through both direct and indirect mechanisms [68]. As part of these mechanisms, alternative metabolic pathways are engaged to restore cellular homeostasis. Malic acid, through the malate valve shuttle, plays a significant role in reducing excess equivalents in the chloroplasts [69, 70]. Moreover, under stress conditions, plants accumulate amino acids. The TCA cycle in plants becomes suppressed under stress, and the previously generated energy is redirected to accumulate amino acids, enhancing stress tolerance [71,72,73]. Shikimate, a core compound in the biosynthesis of aromatic amino acids like phenylalanine, tyrosine, and tryptophan, is particularly important [74]. Thus, metabolites related to the TCA cycle are crucial for interpreting the stress response and synthesizing secondary metabolites in plants, owing to their role in producing ATP and providing carbon skeletons for secondary metabolites [75]. In our current study, a significant increase in shikimate production was observed in basil plants that were grown under two conditions: T30 (T30/D11: 5.1 ± 6.9 μg/10 mg; T30/D23: 10.5 ± 0.8 μg/10 mg) and RA (T30/D11: 38.9 ± 6.9 mg/g; T30/D23: 35.1 ± 5.7 mg/g). Shikimate, which is the final product of the shikimate pathway, was also found highly quantified under the T30 condition. This observation is supported by a correlation coefficient (R-value) of 0.6906. These results suggest that photosynthesis under the T30 condition was functioning effectively and generating carbon skeletons that contributed to the production of the RA precursor. The superior photosynthetic efficiency under T30 conditions compared to other conditions can also be explained through identifiable growth patterns. Photosynthesis serves as a crucial determinant of plant biomass, yield, and metabolism. It enables the capture of solar energy, subsequently converting it into chemical molecules [76]. Carbohydrates produced through photosynthesis play dual roles, acting as signals and providing carbon for various plant metabolic processes and growth, including leaf development [77]. As shown in Table 4, carbohydrate (glucose) content was highly observed in T30 and T35 samples (27.7–99.0 µg/10 mg) but the T40 condition, which was extreme temperature stress, exhibited below 20 µg/10 mg content of glucose. Carbohydrate content provides insight into the potential impact of temperature variations on glucose production. Not only growth parameters linked to photosynthesis but also showed high in T30 conditions. In T30 conditions, both leaf length and leaf width, relative to lateral area, exhibited an expansion as light intensity decreased, and under consistent light conditions, with decreasing temperature. Furthermore, shoot length and internode length were markedly higher under T30 conditions, following a discernible trend of increase with decreasing temperature (Table 4).

Table 4 Primary metabolites of basil cultivated under different temperature and DLI

Full size table

The gradual reduction in leaf area and shoot length observed from T30 was considered to be a plant acclimatization strategy against temperature stress at T35 and T40. Various plant species have been documented to initiate acclimation responses during prolonged exposure to high temperatures, involving changes in morphological, physiological, and biochemical characteristics [78]. These morpho-physiological alterations, including diminished leaf area and photosynthesis, subsequently have a negative effect on vegetative stress and productivity [78]. In our study, the T35/D11 condition was identified as being under stress, as indicated by significantly elevated levels of various primary metabolites, including fumaric acid and malic acid. These changes can be attributed to the increased occurrence of photorespiration and the glyoxylate cycle, as documented in previous studies [69, 70]. It is important to note that secondary compounds, such as terpenes, can be synthesized to facilitate photorespiration, which serves as a protective mechanism for plants against oxidative stress and photodamage [79]. This observation aligns with our current findings.

As the stress intensity increased, particularly under the T40 extreme temperature stress condition, plants exhibited a notable accumulation of amino acids, which can act as a means of temperature stress resistance [80, 81]. Amino acids, being constituents of proteins, play diverse regulatory roles in abiotic stress responses. They can serve as signaling molecules, precursors for secondary metabolites, protein chaperones, and osmotic protectants [71]. Under temperature stress, plants accumulate specific amino acids, which can function as osmoprotectants to help maintain optimal balance, preserve redox homeostasis, and support metabolic processes [53, 71]. Aromatic amino acids, including phenylalanine, tyrosine, and tryptophan, are crucial precursors in protein synthesis and the synthesis of various natural products [82]. These amino acids are synthesized using the carbon skeleton provided by the shikimate pathway [83, 84]. Consequently, phenylalanine and tyrosine, as products of the shikimate pathway and intermediates in the RA (rosmarinic acid) and VOCs biosynthesis pathway, were found highly quantified in both the T40 condition (both in D11 and D23). This resulted in a negative correlation between amino acids and RAC (phenylalanine, r = − 0.4073; tyrosine, r = − 0.6695) and shikimate (phenylalanine, r = − 0.4249; tyrosine, r = − 0.5928). Furthermore, glutamine and glutamic acid, which contribute to balance homeostasis in plants by exporting into the cytoplasm and converting to GABA (gamma-aminobutyric acid) [85], also exhibited a significant increase under the T40 condition.

In plants, continuous stress treatments lasting for days or weeks lead to an acclimation process [86]. In this study, both the maintenance/enhancement of growth and the enhancement of functional components were achieved by inducing adaptive mechanisms in basil through long-term treatments. The responses to temperature and light intensity were interpreted based on metabolic changes.

Conclusion

In plants, continuous stress treatments lasting for days or weeks lead to an acclimation process that enhances stress tolerance, resulting in higher survival rates and increased production. Therefore, long-term cultivation conditions with different temperatures (T30, T35, and T40) and DLI (D11 and D23) were applied to basil cultivation and morphological and biochemical (primary and secondary metabolites) investigations in plants were performed to obtain a comprehensive understanding. As growth progressed, the growth parameters gradually displayed differences, indicating that treatment conditions induced morphological changes in basil plants, and it was interpreted as associated with metabolites. The larger leaf area, longer shoot length, and internode length of T30 were attributed to effective photosynthesis, resulting in a higher amount of carbohydrates and these served as generating carbon skeletons for the TCA cycle. Consequently, higher organic acids, in particular shikimate, are attributed to RA precursor. Meanwhile, along with the temperature increase, reduced leaf area was observed and as the assimilation process, plants stimulated a balance in homeostasis against the accumulated reactive oxygen species (ROS). As a part of this response, plants stimulate transpiration, consequently, fumaric acid and malic acid, which are involved in the glyoxylate pathway, and emission of VOCs were increased under T35/T11. Furthermore, under the more intense heat stress conditions of T40, an extreme accumulation of amino acids was observed, suggesting an adaptation mechanism for survival.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ANOVA:: Analysis of variance
DLI:: Daily light integral
GC-TOF–MS:: Gas chromatogram-time of flight-mass
HPLC:: High performance liquid chromatogram
HS:: Head space
PPFD:: Photosynthetic photon flux density
RA:: Rosmarinic acid
RAC:: Rosmarinic acid content
ROS:: Reactive oxygen species
SPME:: Solid-phase microextraction
TCA:: Tricarboxylic acid
TPC:: Total phenolics content
VOCs:: Volatile organic compounds

References

** H, Zhu Z. Dark, light, and temperature: key players in plant morphogenesis. Plant Physiol. 2019;180(4):1793–802.
Article CAS PubMed PubMed Central Google Scholar
Franklin KA. Light and temperature signal crosstalk in plant development. Curr Opin Plant Biol. 2009;12(1):63–8.
Article CAS PubMed Google Scholar
Janda T, Prerostová S, Vanková R, Darkó É. Crosstalk between light-and temperature-mediated processes under cold and heat stress conditions in plants. Int J Mol Sci. 2021;22(16):8602.
Article CAS PubMed PubMed Central Google Scholar
Cheng M-C, Kathare PK, Paik I, Huq E. Phytochrome signaling networks. Annual Rev Plant Biol. 2021;72(1):217–44.
Article CAS Google Scholar
Ding Y, Shi Y, Yang S. Molecular regulation of plant responses to environmental temperatures. Mol Plant. 2020;13(4):544–64.
Article CAS PubMed Google Scholar
Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, Van Zanten M. Molecular and genetic control of plant thermomorphogenesis. Nature plants. 2016;2(1):1–9.
Article Google Scholar
Sun J, Qi L, Li Y, Chu J, Li C. PIF4–mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet. 2012;8(3): e1002594.
Article CAS PubMed PubMed Central Google Scholar
Xu Y, Zhu Z. PIF4 and PIF4-interacting proteins: at the nexus of plant light, temperature and hormone signal integrations. Int J Mol Sci. 2021;22(19):10304.
Article CAS PubMed PubMed Central Google Scholar
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol. 2009;19(5):408–13.
Article CAS PubMed Google Scholar
Ma D, Li X, Guo Y, Chu J, Fang S, Yan C, et al. Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light. Proc Natl Acad Sci. 2016;113(1):224–9.
Article CAS PubMed Google Scholar
Guo H, Yang H, Mockler TC, Lin C. Regulation of flowering time by Arabidopsis photoreceptors. Science. 1998;279(5355):1360–3.
Article CAS PubMed Google Scholar
Karayekov E, Sellaro R, Legris M, Yanovsky MJ, Casal JJ. Heat shock–induced fluctuations in clock and light signaling enhance phytochrome B–mediated arabidopsis deetiolation. Plant Cell. 2013;25(8):2892–906.
Article CAS PubMed PubMed Central Google Scholar
Legris M, Nieto C, Sellaro R, Prat S, Casal JJ. Perception and signalling of light and temperature cues in plants. Plant J. 2017;90(4):683–97.
Article CAS PubMed Google Scholar
Qin L, Li C, Li D, Wang J, Yang L, Qu A, et al. Physiological, Metabolic and transcriptional responses of Basil (Ocimum basilicum Linn. var. pilosum (Willd.) Benth.) to Heat Stress. Agronomy. 2022;12(6):1434.
Article CAS Google Scholar
Akula R, Ravishankar GA. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav. 2011;6(11):1720–31.
Article Google Scholar
Geng X-M, Liu X, Ji M, Hoffmann WA, Grunden A, **ang Q-YJ. Enhancing heat tolerance of the little dogwood Cornus canadensis L. f. with introduction of a superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus. Front Plant Sci. 2016;7:26.
PubMed PubMed Central Google Scholar
Irato P, Santovito G. Enzymatic and non-enzymatic molecules with antioxidant function. MDPI. 2021;10:579.
CAS Google Scholar
Erb M, Kliebenstein DJ. Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy. Plant Physiol. 2020;184(1):39–52.
Article CAS PubMed PubMed Central Google Scholar
Anulika NP, Ignatius EO, Raymond ES, Osasere O-I, Abiola AH. The chemistry of natural product: plant secondary metabolites. Int J Technol Enhancem Emerg Eng Res. 2016;4(8):1–9.
Google Scholar
Nadeem M, Imran M, Aslam Gondal T, Imran A, Shahbaz M, Muhammad Amir R, et al. Therapeutic potential of rosmarinic acid: a comprehensive review. Appl Sci. 2019;9(15):3139.
Article CAS Google Scholar
Salar E, Khavari-Nejad R, Mandoulakani BA, Najafi F. Effects of TiO2 Nanoparticles on Activity of Antioxidant Enzymes, the Expression of Genes Involved in Rosmarinic Acid Biosynthesis and Rosmarinic Acid Content in Dracocephalum kotschyi Boiss. Russ J Plant Physiol. 2021;68(1):118–25.
Article CAS Google Scholar
Pirooz P, Amooaghaie R, Ahadi A, Sharififar F, Torkzadeh-Mahani M. Silicon and nitric oxide synergistically modulate the production of essential oil and rosmarinic acid in Salvia officinalis under Cu stress. Protoplasma. 2022;259(4):905–16.
Article CAS PubMed Google Scholar
Benedec D, Hanganu D, Oniga I, Tiperciuc B, Olah N-K, Raita O, et al. Assessment of rosmarinic acid content in six Lamiaceae species extracts and their antioxidant and antimicrobial potential. Pak J Pharm Sci. 2015;28(6):2297–303.
CAS PubMed Google Scholar
Bahcesular B, Yildirim ED, Karaçocuk M, Kulak M, Karaman S. Seed priming with melatonin effects on growth, essential oil compounds and antioxidant activity of basil (Ocimum basilicum L.) under salinity stress. Ind Crops Prod. 2020;146: 112165.
Article CAS Google Scholar
Sakkas H, Papadopoulou C. Antimicrobial activity of basil, oregano, and thyme essential oils. J Microbiol Biotechnol. 2017;27(3):429–38.
Article CAS PubMed Google Scholar
Juliani H, Simon J. Antioxidant activity of basil. Trends New Crops New Uses. 2002;575(9):575–9.
Google Scholar
Oxenham S, Svoboda K, Walters D. Antifungal activity of the essential oil of basil (Ocimum basilicum). J Phytopathol. 2005;153(3):174–80.
Article CAS Google Scholar
Blande JD, Glinwood R. Deciphering chemical language of plant communication: Springer; 2016.
Widhalm JR, Jaini R, Morgan JA, Dudareva N. Rethinking how volatiles are released from plant cells. Trends Plant Sci. 2015;20(9):545–50.
Article CAS PubMed Google Scholar
Baldwin IT. Plant volatiles. Curr Biol. 2010;20(9):R392–7.
Article CAS PubMed Google Scholar
Lu N, Bernardo EL, Tippayadarapanich C, Takagaki M, Kagawa N, Yamori W. Growth and accumulation of secondary metabolites in perilla as affected by photosynthetic photon flux density and electrical conductivity of the nutrient solution. Front Plant Sci. 2017;8:708.
Article PubMed PubMed Central Google Scholar
Shabani L, Razavizadeh R. Chitosan enhances rosmarinic acid production in shoot cultures of Melissa officinalis L. through the induction of methyl jasmonate. Bot Stud. 2019;60(1):1–10.
Google Scholar
Walters KJ, Currey CJ. Growth and development of basil species in response to temperature. HortScience. 2019;54(11):1915–20.
Article CAS Google Scholar
Shen Y, ** L, **ao P, Lu Y, Bao J. Total phenolics, flavonoids, antioxidant capacity in rice grain and their relations to grain color, size and weight. J Cereal Sci. 2009;49(1):106–11.
Article CAS Google Scholar
Park MJ, Cho JY, Ha IJ, Moon JS, Kang Y-H. Comparison of the antioxidant properties and flavonols in various parts of Korean red onions by multivariate data analysis. Horticult Environ Biotechnol. 2018;59(6):919–27.
Article CAS Google Scholar
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Bio Med. 1999;26(9–10):1231–7.
Article CAS Google Scholar
Xu JL, Kim TJ, Kim J-K, Choi Y. Simultaneous roasting and extraction of green coffee beans by pressurized liquid extraction. Food Chem. 2019;281:261–8.
Article CAS PubMed Google Scholar
Jorge TF, Duro N, Da Costa M, Florian A, Ramalho JC, Ribeiro-Barros AI, et al. GC-TOF-MS analysis reveals salt stress-responsive primary metabolites in Casuarina glauca tissues. Metabolomics. 2017;13:1–13.
Article CAS Google Scholar
Copolovici L, Copolovici DM, Moisa C, Lupitu A. Antagonist temperature variation affects the photosynthetic parameters and secondary metabolites of Ocimum basilicum L. and Salvia officinalis L. Plants. 2022;11(14):1806.
Article CAS PubMed PubMed Central Google Scholar
Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273.
Article PubMed PubMed Central Google Scholar
Mosadegh H, Trivellini A, Ferrante A, Lucchesini M, Vernieri P, Mensuali A. Applications of UV-B lighting to enhance phenolic accumulation of sweet basil. Sci Hortic. 2018;229:107–16.
Article CAS Google Scholar
Kwee EM, Niemeyer ED. Variations in phenolic composition and antioxidant properties among 15 basil (Ocimum basilicum L.) cultivars. Food Chem. 2011;128(4):1044–50.
Article CAS Google Scholar
Złotek U, Szymanowska U, Karaś M, Świeca M. Antioxidative and anti-inflammatory potential of phenolics from purple basil (Ocimum basilicum L.) leaves induced by jasmonic, arachidonic and β-aminobutyric acid elicitation. Int J Food Sci Technol. 2016;51(1):163–70.
Article Google Scholar
Shiga T, Shoji K, Shimada H, Hashida S, Goto F, Yoshihara T. Effect of light quality on rosmarinic acid content and antioxidant activity of sweet basil, Ocimum basilicum L. Plant Biotechnol. 2009;26(2):255–9.
Article CAS Google Scholar
Shekarchi M, Hajimehdipoor H, Saeidnia S, Gohari AR, Hamedani MP. Comparative study of rosmarinic acid content in some plants of Labiatae family. Pharmacogn Mag. 2012;8(29):37.
Article CAS PubMed PubMed Central Google Scholar
Meng L, Lozano YF, Gaydou EM, Li B. Antioxidant activities of polyphenols extracted from Perilla frutescens varieties. Molecules. 2009;14(1):133–40.
Article CAS Google Scholar
Canadanovic-Brunet J, Cetkovic G, Djilas S, Tumbas V, Bogdanović G, Mandic A, et al. Radical scavenging, antibacterial, and antiproliferative activities of Melissa officinalis L. extracts. J Med Food. 2008;11(1):133–43.
Article PubMed Google Scholar
Trivellini A, Lucchesini M, Maggini R, Mosadegh H, Villamarin TSS, Vernieri P, et al. Lamiaceae phenols as multifaceted compounds: bioactivity, industrial prospects and role of “positive-stress.” Ind Crops Prod. 2016;83:241–54.
Article CAS Google Scholar
Lee C-J, Chen L-G, Chang T-L, Ke W-M, Lo Y-F, Wang C-C. The correlation between skin-care effects and phytochemical contents in Lamiaceae plants. Food Chem. 2011;124(3):833–41.
Article CAS Google Scholar
Zare M, Ganjeali A, Lahouti M. Rosmarinic and caffeic acids contents in Basil (Ocimum basilicum L.) are altered by different levels of phosphorus and mycorrhiza inoculation under drought stress. Acta Physiol Plant. 2021;43:1–10.
Article Google Scholar
Moazzami Farida SH, Karamian R, Albrectsen BR. Silver nanoparticle pollutants activate oxidative stress responses and rosmarinic acid accumulation in sage. Physiol Plant. 2020;170(3):415–32.
Article CAS PubMed Google Scholar
Fletcher RS, Slimmon T, McAuley CY, Kott LS. Heat stress reduces the accumulation of rosmarinic acid and the total antioxidant capacity in spearmint (Mentha spicata L). J Sci Food Agric. 2005;85(14):2429–36.
Article CAS Google Scholar
Sahu R, Gangopadhyay M, Dewanjee S. Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Solenostemon scutellarioides. Acta Physiol Plant. 2013;35:1473–81.
Article CAS Google Scholar
Jakovljević D, Momčilović J, Bojović B, Stanković M. The short-term metabolic modulation of basil (Ocimum basilicum L. cv.‘Genovese’) after exposure to cold or heat. Plants. 2021;10(3):590.
Article PubMed PubMed Central Google Scholar
Castronuovo D, Russo D, Libonati R, Faraone I, Candido V, Picuno P, et al. Influence of shading treatment on yield, morphological traits and phenolic profile of sweet basil (Ocimum basilicum L.). Sci Horticultur. 2019;254:91–8.
Article CAS Google Scholar
Pennisi G, Pistillo A, Orsini F, Cellini A, Spinelli F, Nicola S, et al. Optimal light intensity for sustainable water and energy use in indoor cultivation of lettuce and basil under red and blue LEDs. Sci Hortic. 2020;272: 109508.
Article CAS Google Scholar
Zhou R, Yu X, Li X, Mendanha dos Santos T, Rosenqvist E, Ottosen C-O. Combined high light and heat stress induced complex response in tomato with better leaf cooling after heat priming. Plant Physiol Biochem. 2020;151:1–9.
Article CAS PubMed Google Scholar
Tiwari S, Kate A, Mohapatra D, Tripathi MK, Ray H, Akuli A, et al. Volatile organic compounds (VOCs): Biomarkers for quality management of horticultural commodities during storage through e-sensing. Trends Food Sci Technol. 2020;106:417–33.
Article CAS Google Scholar
Niederbacher B, Winkler J, Schnitzler J. Volatile organic compounds as non-invasive markers for plant phenoty**. J Exp Bot. 2015;66(18):5403–16.
Article CAS PubMed Google Scholar
Abdollahi Mandoulakani B, Eyvazpour E, Ghadimzadeh M. The effect of drought stress on the expression of key genes involved in the biosynthesis of phenylpropanoids and essential oil components in basil (Ocimum basilicum L.). Phytochemistry. 2017;139:1–7.
Article CAS PubMed Google Scholar
Rezaie R, Abdollahi Mandoulakani B, Fattahi M. Cold stress changes antioxidant defense system, phenylpropanoid contents and expression of genes involved in their biosynthesis in Ocimum basilicum L. Sci Rep. 2020;10(1):5290.
Article CAS PubMed PubMed Central Google Scholar
Walters KJ, Lopez RG. Hydroponic Basil production: temperature influences volatile organic compound profile, but not overall consumer preference. Horticulturae. 2022;8(1):76.
Article Google Scholar
Zaynab M, Fatima M, Sharif Y, Zafar MH, Ali H, Khan KA. Role of primary metabolites in plant defense against pathogens. Microb Pathog. 2019;137: 103728.
Article CAS PubMed Google Scholar
Barnabás B, Jäger K, Fehér A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 2008;31(1):11–38.
Article PubMed Google Scholar
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci. 2013;14(5):9643–84.
Article PubMed PubMed Central Google Scholar
Król A, Amarowicz R, Weidner S. Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiol Plant. 2014;36:1491–9.
Article Google Scholar
Paul MJ, Pellny TK. Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot. 2003;54(382):539–47.
Article CAS PubMed Google Scholar
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–99.
Article CAS PubMed Google Scholar
Voss I, Sunil B, Scheibe R, Raghavendra A. Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol. 2013;15(4):713–22.
Article CAS PubMed Google Scholar
Dao O, Kuhnert F, Weber APM, Peltier G, Li-Beisson Y. Physiological functions of malate shuttles in plants and algae. Trends Plant Sci. 2022;27(5):488–501.
Article CAS PubMed Google Scholar
Crecelius F, Streb P, Feierabend J. Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. J Exper Botany. 2003;54(384):1075–83.
Article CAS Google Scholar
Wang J, Yuan B, Xu Y, Huang B. Differential responses of amino acids and soluble proteins to heat stress associated with genetic variations in heat tolerance for hard fescue. J Am Soc Hortic Sci. 2018;143(1):45–55.
Article CAS Google Scholar
You J, Zhang Y, Liu A, Li D, Wang X, Dossa K, et al. Transcriptomic and metabolomic profiling of drought-tolerant and susceptible sesame genotypes in response to drought stress. BMC Plant Biol. 2019;19(1):1–16.
Article Google Scholar
Trovato M, Funck D, Forlani G, Okumoto S, Amir R. Amino acids in plants: regulation and functions in development and stress defense. Front Media SA. 2021;12:772810.
Google Scholar
Zabalza A, Orcaray L, Fernández-Escalada M, Zulet-González A, Royuela M. The pattern of shikimate pathway and phenylpropanoids after inhibition by glyphosate or quinate feeding in pea roots. Pestic Biochem Physiol. 2017;141:96–102.
Article CAS PubMed Google Scholar
Daloso DM, Müller K, Obata T, Florian A, Tohge T, Bottcher A, et al. Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Natl Acad Sci. 2015;112(11):E1392–400.
Article CAS PubMed PubMed Central Google Scholar
Muhie SH. Optimization of photosynthesis for sustainable crop production. CABI Agric Biosci. 2022;3(1):1–8.
Article Google Scholar
Vasseur F, Pantin F, Vile D. Changes in light intensity reveal a major role for carbon balance in Arabidopsis responses to high temperature. Plant Cell Environ. 2011;34(9):1563–76.
Article CAS PubMed Google Scholar
Kaur N, Snider JL, Parkash V, Paterson AH, Grey TL, Tishchenko V. Genotypic variation in growth, single leaf physiology, and acclimation potential of thylakoid processes in cotton exposed to high temperature extremes. Environ Exp Bot. 2023;215: 105512.
Article CAS Google Scholar
Kopaczyk JM, Warguła J, Jelonek T. The variability of terpenes in conifers under developmental and environmental stimuli. Environ Exp Bot. 2020;180: 104197.
Article CAS Google Scholar
Kosová K, Vítámvás P, Prášil IT, Renaut J. Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics. 2011;74(8):1301–22.
Article PubMed Google Scholar
Zhang L, Garneau MG, Majumdar R, Grant J, Tegeder M. Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids. Plant J. 2015;81(1):134–46.
Article CAS PubMed Google Scholar
Kisa D, İmamoğlu R, Genç N, Şahin S, Qayyum MA, Elmastaş M. The interactive effect of aromatic amino acid composition on the accumulation of phenolic compounds and the expression of biosynthesis-related genes in Ocimum basilicum. Physiol Mol Biol Plants. 2021;27(9):2057–69.
Article CAS PubMed PubMed Central Google Scholar
Tohge T, Watanabe M, Hoefgen R, Fernie AR. Shikimate and phenylalanine biosynthesis in the green lineage. Front Plant Sci. 2013;4:62.
Article PubMed PubMed Central Google Scholar
Weaver LM, Herrmann KM. Dynamics of the shikimate pathway in plants. Trends Plant Sci. 1997;2(9):346–51.
Article Google Scholar
Qiu X-M, Sun Y-Y, Ye X-Y, Li Z-G. Signaling role of glutamate in plants. Front Plant Sci. 2020;10:1743.
Article PubMed PubMed Central Google Scholar

Download references

Acknowledgements

This research was funded by an Intramural Grant (2Z06831) from the Korea Institute of Science and Technology (KIST); This research was supported by the National Research Council of Science & Technology (NST) grant by the Korea government (MSIT) (No. CPS22041-110).

Funding

Korea Institute of Science and Technology, South Korea, 2Z06831

Author information

Da Hye Ryu, Jwa Yeong Cho contributed equally to this work.

Authors and Affiliations

Smart Farm Research Center, Korea Institute of Science and Technology (KIST), Gangneung, Gangwon, 25451, Republic of Korea
Da Hye Ryu, Jwa Yeong Cho, Dong Gyu Lee & Ho-Youn Kim
Division of Bio-Medical Science and Technology, KIST School, Korea University of Science and Technology (UST), Daejeon, 34113, Republic of Korea
Jwa Yeong Cho & Ho-Youn Kim
Department of Botany, Garden Campus, Abdul Wali Khan University Mardan, Nowshera Mardan Rd, Mardan, 23200, Pakistan
Muhammad Hamayun

Authors

Da Hye Ryu
View author publications
You can also search for this author in PubMed Google Scholar
Jwa Yeong Cho
View author publications
You can also search for this author in PubMed Google Scholar
Muhammad Hamayun
View author publications
You can also search for this author in PubMed Google Scholar
Dong Gyu Lee
View author publications
You can also search for this author in PubMed Google Scholar
Ho-Youn Kim
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

DHR: Conceptualization, Investigation, Writing-original draft. JYC: Investigation. Methodology, Writing-review & editing. MH: Writing-review & editing. DGL: Investigation. HYK: Project administration, Supervision, Writing-review & editing.

Corresponding author

Correspondence to Ho-Youn Kim.

Ethics declarations

Ethics approval and consent to participate

The study did not use any animal or human subjects; hence, ethical approval or volunteer consent was not required.

Consent for publication

The authors give consent for the publication and its relevant data.

Competing interests

No conflict of interest exists among the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Fig. S1.

Typical HPLC chromatogram of basil (2 mg/mL) detected at 330 nm. RA was observed at 11.94 min as the major compound and the calibration curves were constructed by plotting the peak area of RA against diverse concentrations ranging from 5 μg/ml to 200 μg/mL.

Additional file 2: Fig. S2.

HS-SPME-GC-ToF–MS total ion chromatogram (TIC) of basil sample. Main compounds of volatiles were composed with linalool and eugenol.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Cite this article

Ryu, D.H., Cho, J.Y., Hamayun, M. et al. Metabolic modulation of Basil (Ocimum basilicum L.): an insight into growth, metabolomics and antioxidant activity under varying temperature and light conditions. Chem. Biol. Technol. Agric. 11, 10 (2024). https://doi.org/10.1186/s40538-023-00532-2

Download citation

Received: 12 November 2023
Accepted: 28 December 2023
Published: 15 January 2024
DOI: https://doi.org/10.1186/s40538-023-00532-2

Metabolic modulation of Basil (Ocimum basilicum L.): an insight into growth, metabolomics and antioxidant activity under varying temperature and light conditions