TRENDING MICROBIOLOGICALS AND THEIR ROLE TO ENHANCE GROWTH AND ESSENTIAL OIL CONTENT OF DILL (ANETHUM GRAVEOLENS)HTML Full Text
TRENDING MICROBIOLOGICALS AND THEIR ROLE TO ENHANCE GROWTH AND ESSENTIAL OIL CONTENT OF DILL (ANETHUM GRAVEOLENS)
Kamal Jeet 1, 2 and Ashish Baldi * 2, 3
I. K. G. Punjab Technical University 1, Jalandhar - 144603, Punjab, India.
I. S. F. College of Pharmacy 2, Moga - 142001, Punjab, India.
Department of Pharmaceutical Sciences & Technology 3, Maharaja Ranjit Singh Punjab Technical University, Bathinda - 151001, Punjab, India.
ABSTRACT: A greenhouse and field experiment was conducted to investigate the effects of Azotobacter (Azotobacter chroococcum), Phosphate solubilizing bacteria (Pseudomonas fluorescens), and Arbuscular mycorrhiza-like fungi (Sebacinca vermifera) on seed germination, physiology, and essential oil production of dill (Anethum graveolens). The experimentation was comprised of a randomized complete block design with six replicates of each treatment. Evaluation of germination was done using parameters; germination percentage, mean germination time, germination index, T50 of germination, seedling vigour, and vigour index. Physiological responses include the parameters for total length, total fresh weight, and total dry weight of the plant. For physiological evaluation, harvesting of plants was done a total of four times at an interval of 30 days i.e. on 30, 60, 90, 120 days after transplantation. Essential oil analysis was done by hydrodistillation followed by Gas chromatography-Mass spectrometry. All the data collected were statistically analyzed using the GraphPad Prism v6 software package. Results showed that all treatments negatively affected the emergence behavior of seeds, whereas physiology of plants and essential oil production by Sebacina vermifera were significantly higher than other treatments. More specific to essential oil, treatments not only affected the total yield of essential oil but also affected the most components of essential oil. This study is potentially representing an alternative way of promoting the growth and biosynthesis of essential oils in dill.
Anethum graveolens, Dill, Essential oil, Carvone, Mycorrhiza, Sebacina vermifera
INTRODUCTION: Anethum graveolens L. (Dill) is an aromatic and herbaceous annual plant that belongs to the family Umbelliferae (Apiaceae). This plant is indigenous to the Mediterranean, central and southern Asia 1. This plant has been used in condiments and medicinal purposes since Egyptian times 2.
This plant has been used throughout Europe, Asia, and America in traditional medicine systems, including Ayurveda, Unani, and Chinese medicine system 2, 3.
This plant claims a wide range of ethnomedicinal uses like in stomachache, hemorrhoids, insomnia, flatulence, carminative, diuretic, soporific, galac-tagogue, cough, cold, flu, nosebleeds, abdominal pain, eye diseases, uterine pain, swelling of joints, and to heal drunkenness 2, 3. According to Jana and Shekha wat (2010), 2 more than 56 Ayurvedic preparations include dill as an ingredient. Dried leaves of dill are used as a condiment and herbal tea, whereas fresh leaves are used in meats, fishes sandwiches, and fish sauces. Dill seeds are used widely as spice and seasoning of various foods such as pickles, salads, and soups 4-6. Dill seeds contain about 3.5% of essential oil (EO). Monoterpenes are the major constituents of EO, including d-carvone, d-limonene, and apiol, and responsible for its aroma and medicinal effects 7-9. EO from dill used in food industries and perfumery 6. EO components are mainly responsible for the medical use of dill. Numerous scientific studies has been conducted using dill extracts, suggesting it as a potential medicinal candidate as antimicrobial, antihyperlipidemic, antihypercholesterolemic, mucosal protective, antisecretory, anti-ulcer, anti-oxidant, spasmolytic, anti-inflammatory, analgesic, anticancer, antidiabetic, insecticidal, diuretic, and menstrual cycle regulator 2, 10, 11. Worldwide cultivation wide array of medicinal active constituent and large scale perfumery utilization of dill make this plant as a suitable candidate for growth and EO enhancement studies whether it is genetically based or obligatory mutualistic symbiosis based. Azotobacter (Azotobacter chroococcum), Phosphate solubilizing bacteria (Pseudomonas fluorescens), and Arbuscular mycorrhizal (AM)-like fungi (Sebacinca vermifera) has been largely used to enhance the growth of a plant and alter the phytochemical productions. This microorganisms viz. A. chroococcum 12, 13, P. fluorescens 14, 15, and S. vermifera 16, 17 are well known for their beneficial effects on plants. Therefore, it is interesting to investigate the comparative effects of tested microorganisms on germination, growth, and EO production of dill.
MATERIALS AND METHODS:
Microorganisms and Plant: The culture of S. vermifera was kindly gifted by Prof. Virendra Swarup Bisaria, department of Biochemical Engineering and Biotechnology, Indian Institute of Technology-Delhi, India. The culture of S. vermifera was incubated on a modified Kaefer-agar medium for 10 days at 30 ± 1 °C and pH 6.5; after that, the slants we restored at 4 °C18. Further cultivation was done in 100 ml of modified Kaefer liquid medium in 500 ml Erlenmeyer flasks at 30 ± 1 °C on a gyratory shaker rotating at 200 rpm 19-20. Fungal culture (8 day old) was then mixed with 1 ml carboxy methylcellulose (CMC) followed by mixing of 75 g of sterilized talcum powder in 25 ml of CMC mixed culture 21. The formulation was then filled in airtight polythene bags and stored at normal room temperature until further experimentation. Azotobacter (A. chroococcum) and Phosphate Solubilizing Bacteria (P. fluorescens) were marketed biofertilizers, procured form Ganesh Agro Service Centre, and belongs to local market of Moga, Punjab, India. Seeds of dill (Anethum graveolens) were collected from Punjab Agriculture University, Ludhiana, India, during the rabi season. Seeds were surface sterilized using 70% v/v alcohol, followed by treatment with 0.01% Bavistin. Seeds were kept 24 h in sterilized water for soaking before experimentation.
Experimental Conditions: Experimentation was performed under greenhouse conditions (in pots) and field conditions. Soils used in both conditions were different, and a sample of soils was tested for chemical reserve prior to the experimentations. The physical properties and chemical reserves are given in Table 1. The soil used for greenhouse conditions was autoclaved for 1 h in cotton bags and cooled at room temperature. The sterilization was repeated for 3 times after 24 h on consecutive days. The experimentation under greenhouse condition was conducted in controlled environmental conditions maintained at 25 ± 2 °C, 16 h light / 8 h dark with light intensity 1,000 Lux and relative humidity 70%. The field study was conducted in the agricultural farms using Randomized Complete Block Design (RCBD). The soil was made porous by several ploughings and disking to facilitate healthy root development. Population size was 100 for each replicate of an observational group. All experimentation was done in six replicates, and the sample size was also six from each replicates 22. A complete topography of field experimentation and sowing scheme is given in Fig. 1, 2.
TABLE 1: PHYSICAL AND CHEMICAL PROPERTIES OF SOIL
|Sample||pH||Electrical Conductivity (mmho/cm)||C (%)||P
Note: C-Carbon, P-Phosphorus, K-Potash, Fe-Ferrous, Zn-Zinc, Cu-Copper, Mn- Manganese,N-Nitrogen
Treatments: There were four study groups viz. control (CON), Azotobacter (AZOTO), Phosphate solubilizing bacteria (PSB) and S. vermifera (SV). CON group received same treatment without any microbial strain, AZOTO, PSB, and SV groups received dual treatment with different schemes. Treatment of seeds with AZOTO, PSB, and SV was carried out using paste of 1 kg biomass in 1 L of water for seeds sufficient for 1 acre (approx. 10 Kg). The paste was applied uniformly on the surface of seeds and dried in the shade before sowing in pots/fields.
The treatment of plantlets (for physiological studies) was carried by root dipping in the paste of same composition used for seed treatment and sown immediately in pots/field. Soil treatment was carried by induction of 1 kg biomass in 19 kg of vermicompost and mixed with soil in the ratio of 60:40 (soil: treated vermicompost), whereas in the field, treated vermicompost was spread as 60 kg treated vermicompost per acre. For standing plants treatment was carried out by drilling/drenching method after 8 weeks using treated vermicompost 22.
Germination Studies: The pot and field studies were composed of 100 seeds per replicate of each treatment group. Seeds in pot were uniformly sown as 10 seeds per pot, in 2 kg capacity polythene pots, where first 3/4th part of treated soil was filled then the soil was moistened with water. After placing seeds uniformly 1/4th reaming part of soil was filled such that each seed were 2 cm below the soil surface. In field seeds were sown in plot containing 10 rows and 10 columns, and seeds were interspaced at 45 cm to next seed Fig. 2. There was a buffering zone surrounding the plots, which was a reservoir from contamination and a platform for handling and maintenance activities. All seeds of the field were covered 2 cm below the soil surface. The soil was moistened with a light spray of water. The soil was covered with straw to avoid certain dryness, and water was supplied daily to avoid drought stress. Germination behavior was observed regularly after 24 h and a seed was considered germinated when radical was visible on surface of soil. Germination study both under greenhouse and field conditions were observed until the germination was constant for 3 days and evaluation was comprised of following parameters:
- Germination percentage 23
- Mean germination time 24,25
- Germination index 26
- T50 of germination 27-29
- Seed vigour 30
- Vigour index 31
Physiological Studies: The young and healthy 30 days old plantlets of similar size and in the same development stage were taken for the physiological study. Under both green house and field studies the population of plants was maintained at 100 for each replicate of respective treatment groups. Under green house condition each pot of 10 kg capacity was containing single plantlet whereas under field conditions plantlets were sown in plot containing 10 rows and 10 columns and plantlets were interspaced at 45 cm to next plantlets Fig. 2. Soils of both conditions were irrigated regularly to avoid drought stress.
Plants were uprooted periodically at an interval of 30 days i.e. 30, 60, 90 and 120 DAT (Day after transplantation) for physiological evaluations. Evaluation was done using following parameters:
- Total plant length (root + shoot)
- Total fresh weight of plant (root + shoot)
- Total dry weight of the plant (root + shoot)
Colonization Studies: The plants were harvested, four time at and interval of 30 days. Collected roots were washed thoroughly under slow stream of water to remove the adhering soil particles. Small segments of roots (1.0 cm approximately) were heated in 10 % KOH for 15 min. After washing with water 3-5 times, the root segments were neutralized by treating with 1 N HCl for 2-3 min 32. After washing with water, root segments were then stained with 0.02 % Trypan blue overnight and were de-stained with 50 % lacto-glycerol for1-2 h prior to the observation under a light microscope. Root colonization was assessed using the following formula 33:
Percentage colonization = Number of root segments colonized / Number of total segments examined × 100
Oil extraction: Sample of seeds were collected from well-grown healthy plants of each group and dried at room temperature. Dried samples were grounded in a blender. The extractions of grounded seeds were done by hydrodistillation using a Clevenger apparatus for 4 h. The oil samples were collected in airtight container and stored at 4 °C until further analysis.
Gas Chromatography-Mass Spectrometry: GC-MS analyses were carried out on a gas chromatograph Thermo trace 1300 GC coupled to a Thermo TSQ 8000 mass spectrometer with electron impact ionization method. Ion source temperature was 230 °C. A TG-5MS capillary column (30 m × 0.25 mm, 0.25 μm film thickness) was used. The column temperature was programmed to rise from 50 °C (2 min) to 280 °C at the rate of 10 °C / min. The S/SL injector’s temperature was maintained at 250 °C, and the injection volume was 1.0 μL. The MS transfer line temperature was maintained at 280 °C. The carrier gas was helium with a flow rate 1 mL/min, and mass range was 50-500 m/z.
EO components were identified by comparison spectral data to those from mass spectra stored in the National Institute of Standards and Technology (NIST) spectral library. The percentage peak area of corresponding component was taken as content concentration without using correction factors 34.
Statistical Analysis: All experiments were performed in six replicates (Sample size was 6 from each replicate). The data were expressed as mean ± SD (standard deviation). Data from germination studies, a yield of EO and composition of various EO components, was analyzed using one-way - analysis of variance (ANOVA) followed by Tukey’s post hoc test to compare means at the significance level p<0.05. Data from physiological studies were analyzed using two-way - ANOVA, followed by Bonferroni post-test for multiple comparison of means at the significance level p<0.05. All statistical analysis was performed using the GraphPad Prism v6 software package.
Colonization Studies: The presence of fungal hyphae confirm the positive colonized association between the tested plant and S. vermifera under both conditions, i.e., pots under greenhouse and field conditions. Further, there was a variation in colonization percentage under pots and field conditions.
Colonization percentage was found lowest at 30DAT (Pot-25.65%; Field-15.25%), which gradually increased at 60 DAT (Pot-46.31%; Field-26.12%) and 90 DAT (Pot-70.32%; Field-40.38%). The highest colonization percentage was recorded at 120 DAT (Pot-85.40%; Field-78.31%) under both greenhouse and field conditions. Colonization responses are given as Table 2.
TABLE 2: COLONIZATION PERCENTAGE OF SEBACINA VERMIFERA WITH DILL ROOTS AT DIFFERENT TIME PERIODS IN POT AND FIELD TRIALS
Root colonization (%) of Sebacina vermifera treated plants: data expressed as mean ± SD of six replicates. CON- Normal control; SV- S. vermifera; DAT- Day after transplantation
Note: (-): not detected
Germination Studies Under Greenhouse Conditions: Emergence studies on dill seeds were observed for 25 days from the day of sowing of seeds. The statistical analysis revealed significant positive effects of all three treatments for all the germination traits on tested plant species, i.e., dill Table 3. It was observed that all three treatments enhanced the emergence trait and positively decreased mean germination time. Among all groups, the SV group showed better emergence performance with respect to all germination traits. In comparison to CON, SV here increased germination percentage, germination index, seedling vigour, and vigour index by 38.46%, 265%, 22.58%, and 69.73%, respectively. PSB enhanced the same traits by 28.85%, 258.86%, 16.13%, and 49.63%, respectively. Similarly, AZOTO enhanced these factors by 19.23%, 31%, 6.45%, and 26.92%, respectively. On the other hand, SV, PSB, and AZOTOpositivelydecreased mean germination time by19.40%, 18.35%, and 9.02%, respectively. Similarly, T50 germination was positively decreased by 14.29%, 12.63%, and 8% for SV, PSB, and AZOTO, respectively Table 3.
TABLE 3: EFFECTS OF VARIOUS TREATMENTS ON DILLSEEDS UNDER POT TRIALS
|Mean germination time||16.29±0.61||14.82±0.67a||13.30±0.50a,b||13.13±0.30a,b|
|Seedling vigour (mm)||62.00±2.00||66.00±1.00a||72.00±1.00a,b||76.00±2.00a,b,c|
|Vigour index (mm)||3224.00±228.01||4092.00±161.53a||4824.00±175.63a,,b||5472.00±257.79a,b,c|
Emergence response of seeds to various treatments in pots trials: data expressed as mean ± SD of six replicates. Superscripts with different letters (a-c) within the same row represent significance level as pa<0.05 v/s Con; pb<0.05 v/s AZOTO; pc<0.05 PSB; CON- Normal control; AZOTO- Azotobacter; PSB- Phosphate solubilizing bacteria; SV- S. vermifera formulation
Germination Studies Under Field Conditions: Similar, to pot trials, under the field, all treatment groups exerted a positive effect on the germination performance of dill seeds. Overall emergence of seeds under field conditions, including treated and non treated groups, were slightly changed Table 4. When compared to CON, SV increased the germination percentage, germination index, seedling vigour, and vigour index by 44.68%, 167.41%, 37.86%, and 99.46%, respectively. For PSB, the same factors were increased by 40.43%, 162.74%, 22.33%, and 71.78%, respectively. Similarly, AZOTO increased the same factors by 14.89%, 152.55%, 8.74%, and 24.93%, respectively. Simultaneously, SV, PSB, and AZOTO positively decreased the mean germination time by 20.10%, 14.92%, and 13.42%, respectively. Similarly, T50 germination was positively decreased by 11.69%, 6.68%, and 4.78% for SV, PSB, and AZOTO, respectively Table 4.
TABLE 4: EFFECTS OF VARIOUS TREATMENTS ON DILL SEEDS UNDER FIELD TRIALS
|Mean germination time||16.62±0.45||14.39±0.72a||14.14±0.40a||13.28±0.65a,b|
|Seedling vigour (mm)||51.50±1.00||56.00±1.53a||63.00±1.00a,b||71.00±1.53a,b,c|
|Vigour index (mm)||2420.50±124.72||3024.00±165.01a||4158.00±129.00a,b||4828.00±210.58a,b,c|
Emergence response of seeds to various treatments in field trials: data expressed as mean ± SD of six replicates. Superscripts with different letters (a-c) within the same row represent significance level as pa<0.05 v/s CON; pb<0.05 v/s AZOTO; pc<0.05 PSB; CON- Normal control; AZOTO- Azotobacter; PSB- Phosphate solubilizing bacteria; SV- S. vermifera formulation
Physiological Response Under Green House Conditions: Plants were evaluated four times during the experimentation, at an interval of 30 days i.e., 30, 60, 90, and 120 DAT to understand the effects of treatments on the physiological performance of plants. All treatments significantly enhanced the physiology of plants in terms of the total length of the plant, total fresh weight of the plant, total dry weight Fig. 3, 4. Of all three treatments, the SV performed extremely well and consistently with an increment in the total length of the plant (range from 29.19% to 159.20%), total fresh weight (range from 58.39% to 226.67%), and total dry weight (range from 62.79% to 357.89%). The enhancement was found significantly higher when compared to all other groups, including treated and non-treated. Here, PSB was recorded as the second performer to enhance the total length of plant (range from 16.02% to 105.79%), total fresh weight (range from 29.64% to 147.22%) and total dry weight (range from 33.69% to 231.58%) and enhancements by PSB were significantly higher when compared to CON and AZOTO groups.
AZOTO was recorded as the third performer, which significantly enhanced total length of a plant (range from 7.56% to 50.89%), total fresh weight (range from 16.01% to 58.89%), and total dry weight (range from 18.38%to 92.11%) Fig. 4.
FIG. 3: PLANTS UNDER POT TRIALS AT 120 DAT (A) CONTROL (B) AZOTOBACTER (C) PHOSPHATE SOLUBILIZING BACTERIA (D) S. VERMIFERA
FIG. 4: EFFECT OF TREATMENTS ON (A) TOTAL LENGTH OF PLANTS (B) TOTAL FRESH WEIGHT OF PLANTS (C) TOTAL DRY WEIGHT OF PLANTS UNDER POT CONDITIONS; DATA EXPRESSED AS MEAN ± SD OF SIX REPLICATES. SUPERSCRIPTS WITH DIFFERENT LETTERS (a-c) WITHIN THE SAME HARVESTING GROUP REPRESENT SIGNIFICANCE LEVEL ASpa<0.05 v/s CON; pb<0.05 v/s AZOTO; pc<0.05 v/s PSB; CON-NORMAL CONTROL; AZOTO- AZOTOBACTER; PSB- PHOSPHATE SOLUBILIZING BACTERIA; SV- S. VERMIFERA
Physiological Response Under Field Conditions: Overall physiology of plants including length, fresh weight, and dry weight of plant was found slightly higher under field conditions unlike plant grown under pot conditions Fig. 5, 6. Like pot trials under field trial, SV also performed extremely well and consistently with an increment in a total length of a plant (range from 24% to 153.86%), total fresh weight (range from 57.68% to 187.26%), and total dry weight (range from 62.22% to 326.67%).
The enhancement was found significantly higher when compared to all other groups, including treated and non-treated.
Here PSB was recorded as the second performer to enhance the total length of a plant (range from 14.39% to 101.30%), total fresh weight (range from 30.73% to 100.64%), and total dry weight (range from 31.77% to 176.67%) and enhancements by PSB were significantly higher when compared to CON and AZOTO groups.
AZOTO was recorded as the third performer, which significantly enhanced the total length of a plant (range from 6.32% to 46.98%), total fresh weight (range from 16.08% to 50.96%), and total dry weight (range from 15.23 to 83.33%) Fig. 6.
FIG. 5: PLANTS UNDER FIELD TRIALS AT 60 DAT (A) CONTROL (B) AZOTOBACTER (C) PHOSPHATE SOLUBILIZING BACTERIA (D) S. VERMIFERA
FIG. 6: EFFECT OF TREATMENTS ON (A) TOTAL LENGTH OF PLANTS (B) TOTAL FRESH WEIGHT OF PLANTS (C) TOTAL DRY WEIGHT OF PLANTS UNDER FIELD CONDITIONS; DATA EXPRESSED AS MEAN ± SD OF SIX REPLICATES. SUPERSCRIPTS WITH DIFFERENT LETTERS (A-C) WITHIN THE SAME HARVESTING GROUP REPRESENT SIGNIFICANCE LEVEL AS PA<0.05 V/S CON; PB<0.05 V/S AZOTO; PC<0.05 V/S PSB; CON- NORMAL CONTROL; AZOTO- AZOTOBACTER; PSB- PHOSPHATE SOLUBILIZING BACTERIA; SV- S. VERMIFERA
Yield of Essential Oils: EO yield was significantly influenced by treatments viz. AZOTO, PSB, and SV. Like physiological enhancements, SV also prominently enhanced the yield of EO efficiently under both conditions (pot & field). SV treated group significantly increased EO yield (pot 2.90%; field 2.30%) in comparison to CON, AZOTO, and PSB. Here PSB (pot 1.90%; field 1.80%) and AZOTO (pot 1.80%; field 1.40%) were also recorded with significantly enhanced yield, whereas, CON (pot 1.40%; field 1.20%) group was recorded with the lowest yield Fig. 7. Chemical composition of EO of dill: GC-MS analysis of EO of dill seed of greenhouse (in pots) condition resulted in the identification of 16 chemical constituents Table 5 adding up to99.99 to 100% of total area. The major constituents of EO were limonene (25.19-33.18%), carvone (20.57-30.95%), apiol (12.79-26.07%) followed by cis-dihydrocarvon (3.59-24.44%), trans- dihydro-carvone (8.17-12.94%). Different treatments exerted relatively different effects significantly. Limonene was the maximum elevated compound of EO in comparison to all other compounds and reached to highest in the AZOTO (33.18%) group, followed by PSB (30.55%) and SV (26.33) whereas, CON (25.19) group was recorded with the lowest percentage of limonene. Carvone was the second, elevated compound reached to its maximum (30.95%) with SV treatment followed by PSB (28.38%) and AZOTO (23.91%) while the CON group restricted the Carvone to 20.57% only. The third elevated compound has Apiol recorded maximum with SV again (26.07%) followed by PSB (13.07%) and CON (12.79%) while it was absent in the AZOTO group. It was observed that cis-dihydrocarbon and trans-dihydrocarvone, p-cymene, limonene oxide-cis were the compounds recorded highest in CON, whereas down-regulated by all treatments. α-pinene, o-cymene, limonene, ϒ-terpinene, linalool, carvone, anethole, carvacrol, myristicin, and apiol were upregulated by other treatments. In contrast to individual components, the effect of various treatments is summarized in Table 5.
FIG. 7: EFFECT OF TREATMENTS ON YIELD OF EO OF PLANT SEEDS UNDER POT AND FIELD CONDITIONS: DATA EXPRESSED AS MEAN ± SD OF SIX REPLICATES. SUPERSCRIPTS WITH DIFFERENT LETTERS (A-C) WITHIN THE SAME CONDITION GROUP REPRESENT SIGNIFICANCE LEVEL AS PA<0.05 V/S CON; PB<0.05 V/S AZOTO; PC<0.05 V/S PSB; CON- NORMAL CONTROL; AZOTO- AZOTOBACTER; PSB- PHOSPHATE SOLUBILIZING BACTERIA; SV- S. VERMIFERA
TABLE 5: EFFECT OF DIFFERENT TREATMENTS ON COMPOSITION OF VARIOUS EO COMPONENTS OF DILLSEEDS GROWN IN POTS UNDER GREENHOUSE CONDITIONS
Data expressed as mean ± SD of three replicates: Superscripts with different letters (a-c) within the same row represent significance level aspa<0.05 v/s CON; pb<0.05 v/s AZOTO; pc<0.05 v/s PSB; CON- Normal control; AZOTO- Azotobacter; PSB- Phosphate solubilizing bacteria; SV- S. vermifera formulation Note: (-): not detected
Overall field response in contrast to individual compounds was found slightly different, unlike pot responses. GC-MS analysis of EO of dill seed under field conditions also resulted in the identification of 16 chemical constituents Table 6 adding up to 99.99 to 100% of the total area. The major constituents of EO were limonene (23.40-32.12%), carvone (19.40-29.47%), apiol (10.49-25.21%) followed by cis-dihydrocarvone (3.57-23.36%), trans-dihydrocarvone (7.26-11.27%). Different treatments exerted relatively different effects significantly. Limonene was the maximum elevated compound of EO in comparison to all other compounds and reached to highest in AZOTO (32.12%) group, followed by PSB (28.90%) and SV (25.93), whereas, CON (23.40) group was recorded with the lowest percentage of limonene. Carvone was the second, elevated compound reached its maximum (29.47%) with SV treatment followed by PSB (26.57%) and AZOTO (21.52%) while CON group restricted carvone to 19.40% only. The third elevated compound was apiol recorded maximum with SV again (25.21%) followed by PSB (12.87%) and CON (10.49%) while it was absent in the AZOTO group. It was observed that cis- dihydrocarvone and trans- dihydrocarvone, p-cymene, limonene oxide-cis were the compound recorded highest in the CON group, whereas down-regulated by all treatments. α-pinene, o-cymene, limonene, ϒ-terpinene, linalool, carvone, anethole, carvacrol, myristicin, and apiol were upregulated by other treatments. In contrast to individual components, the effect of various treatments is summarized in Table 6.
TABLE 6: EFFECT OF DIFFERENT TREATMENTS ON COMPOSITION OF VARIOUS EO COMPONENTS OF DILLSEEDS GROWN UNDER FIELD CONDITIONS
Data expressed as mean ± SD of three replicates: Superscripts with different letters (a-c) within the same row represent significance level aspa<0.05 v/s CON; pb<0.05 v/s AZOTO; pc<0.05 v/s PSB; CON- Normal control; AZOTO- Azotobacter; PSB- Phosphate solubilizing bacteria; SV- S. vermifera formulation Note: (-): not detected
DISCUSSION: The evaluation of colonization percentage is the key indicator for the symbiotic association between AM fungi and tested plant34. The present work established the active symbiotic relation between S. vermifera and A. graveolens. These observations are in line with previous studies that demonstrated the successful establishment of an association between S. vermifera and a wide range of plant species like Trigonella Foenumgraecum 21, Coriandrum sativum 22, Foeniculum vulgare 35, Nicotiana attenuate 36, Thymus vulgaris 37, Brassicaceae plants38, Panicum virgatum 39, 40 and Oryza sativa 17. All tested microbes have positively influenced germination traits. Similar positive effects of A. chroococcum was observed on germination of Dodonaea viscoseseeds 41 similarly P. fluorescens was recorded with a positive effect on germination of Vicia faba 42; contrary to this, a negative effect of A. chroococcum was observed on germination of H. vulgareseed 43 also P. fluorescenswas recorded with a negative effect on germination of Triticum turgidum 44 and Ambrosia artemisiifolia seeds (weed plant) 45. Although the underlying mechanisms behind the stimulatory and inhibitory effects of selected microbes are still not exposed but it is hypothesized that enhanced germination is the due response of phytohormones and other complex mixture of biologically active compounds and growth-promoting metabolites that are modulated by A. chroococcum 46-48, P. fluorescens 49-50. Similarly, fungal inoculant (S. vermifera)was recorded with a positive influence on the germination of dill seeds. These observations are supported by previous studies on N. attenuate, P. virgatum, Cynorkis purpurea 16, 51. In context to S. vermifera, it is conceivable that the performance of S. vermifera dependent on planting species, application procedures, and experimental designs and conditions under which experiments are to be performed. The observation of Maighal et al. (2016) 52 also supports our observation and suggests that two factors, “Mycorrhiza” and “seed species,” are responsible for seed viability and hence germination. In the contrary, Lendzemo et al. (2007) 53 explain that inhibitory action of AMF may be the result of the formation of unwanted metabolites, inhibitions of required metabolites, and negative niche effects. The overall emergence responses in pot under greenhouse conditions were found better in comparison to the field because of controlled environmental conditions, while under field conditions, external unfavorable conditions largely inhibit the metabolic processes and proliferation of embryonic tissues and negatively altered the emergence. Morphological evaluation represents the growth-enhancing features of tested microbes. The same observation was also made previously for A. chroococcum 12, 13, P. fluorescens 14, 15 and S. vermifera 16, 17.
In addition, a prominently enhanced fresh weight and dry weight of fungi inoculated T. vulgaris was recorded by Dolatabadi et al. (2011b) 37. Similarly, S. vermifera inoculated plants have been recorded with enhanced Plant length, enhanced fresh weight, dry weight, enhanced root system, and number of nodes 38, 54. Previous works hypothesized that increased plant growth due to AMF inoculation could be attributed to ea earlier expression of developmentally regulated genes 55 and phytohormonal involvements 56. Eventually, A. chroococcum, Pseudomonas species, and AM-like fungi (P. indica- closely related to S. vermifera) has been demonstrated for phytohormonal modulator effects 56-60. Moreover, improved plant growth may be ascribed to higher nutrient uptakes, especially nitrogen and phosphorus. Nitrogen and phosphorus largely contribute to biomass allocation, accumulation, and prominent growth of plants, an excellent yield of seeds, and EO production 61.
It is well known that A. chroococcum specifically fixes nitrogen to soil 62, 63, and Pseudomonas genera are well known as phosphate solubilizing bacteria, which fixes non-utilizable phosphate to utilizable forms to plant 64 whereas, S. vermifera not restricted to a selected nutrient but has the potential to fix and efflux wide range of macro-and micro-nutrients in addition to Nitrogen and Phosphorus 16, 40. Indeed, S. vermifera has contributed to the exploration of large soil volume, enhanced nutrient uptake, and mass accumulation more than other treatments. In support, elemental analysis of CHN from a dry matter of plants confirms enhanced nutrient uptake has contributed to mass accumulation (Data is not shown here). The inoculation of microbes also altered the yield of EO and contributed to the better quantity and quality of components. A similar investigation has demonstrated that A. chroococcum stimulates the production of EO in Cymbopogon martini and F. vulgare 65, 66. Also, P. fluorescens has investigated to increase the EO in Ocimum basilicum and Origanum majorana 67, 68. Prior investigations demonstrated that S. vermifera significantly increased the yield of EO in Coriandrum Sativum 22, Foeniculum vulgare 35, T. vulgaris 37.
Although the underlying mechanism behind the increment in EO is still to disclose however it may attribute to defensive response 68, 69, morphological traits 70, 71, up-regulation of biosynthetic genes 71-73 and P availability 74-78. It is speculated that S. vermifera may have associated with aforesaid factors and indeed the higher efflux of N and P may have stimulated isopentenyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMAPP) synthesis better than other microbes resulted in better yield of EO in treated plants. In context to major constituent of EO already some studies demonstrated that A. chroococcum had increased the content of Anethole in F. vulgare66, A. chroococcum has increased the content of (+) pulegone and (-) menthone in Mentha piperita 79, Similarly S. vermifera increased the content of linalool, anethole and thymol in C. sativum, F. vulgare and T. vulgaris respectively 22, 35, 37.
Similarly, S. vermifera enhanced the production of podophyllotoxin and its 6-methoxy derivative in Linum album. Additionally, precursor and elicitor of fungal origins are also in prevalence to enhance secondary metabolites in plant cell culture 83-85. Enhancement in commercially important secondary metabolites i.e., artemisinin and withaferin-a, were already achieved efficiently in cell culture technique facilitated with elicitor of fungal origins 86-87.
Although the underlying mechanism(s) for enhancement in major components of EO is still hidden however it is hypothesized that upregulation of biosynthetic genes, modulation of phyto-hormones, enhanced physiology, enhanced defensive response higher influx of N and P may enhance the particular class of secondary metabolites. This hypothesis is well supported by Baldi et al. (2008) 80 stated that S. vermifera could enhance the secondary metabolite production by activating the defensive pathways. Baldi et al. (2010) 18 also demonstrated that elicitor of fungal origin could stimulate the biosynthetic pathway, which resulted in enhanced secondary metabolites in cell culture; further, it was supported by Ammonia-lyase (PAL) activity, which is a short limiting step to synthesize secondary metabolite of lignin origin (Farkya et al. 2010) 82. It is worth mentioning that the overall physiological and biochemical responses were slightly higher under field trials, whereas they were low in pots trials. It is tempting to speculate that the undisturbed core, higher fertility, and presence of indigenous microflora were responsible for better performance of plants under field conditions while the soil of pots was sterilized with disturbed core might be the reason for underperformance of plants.
CONCLUSION: Although AZOTO and PSB could extend their contribution towards better performance of dill plant but S. vermiferaimplied the greater magnitude for multifaceted benefits for the dill plant in all aspects (except germination) and support the growth of plants, stimulate the defensive mechanisms, maintain the health and vitality of plant, enhance the yield of EO and hence the secondary metabolites. By extrapolating the overall results and considering the efficacy, we promoteS. vermiferaas a potential alternate to achieving eco-friendly and sustainable agricultural practices in general and in particular to dill.
ACKNOWLEDGEMENT: Authors are thankful to Science and Engineering Board (SERB), Department of Science and Technology, Govt. of India, New Delhi, for providing financial assistance under the Fast Track Scheme (DST-SERB-FTYS) to Dr. Ashish Baldi. The authors are also thankful to Mr. Pankaj Samuel and Mr. Neeraj Jaswal (CIL, Panjab University, Chandigarh, India) for their help in GC-MS analysis and organic elemental analysis.
CONFLICTS OF INTEREST: The authors declare that they have no conflicts of interest.
- Bailer J, Aichinger T, Hackl G, Hueber KD and Dachler M: Essential oil content and composition in commercially available dill cultivars in comparison to caraway. Industrial crops and products 2001; 14: 229-39.
- Jana S and Shekhawat GS: Anethum graveolens: An Indian traditional medicinal herb and spice. Pharmacognosy Reviews 2010; 4: 179-84.
- Sharopov FS, Wink M, Gulmurodov IS, Isupov SJ, Zhang H and Setzer WN: Composition and bioactivity of the essential oil of Anethum graveolens from Tajikistan. International Journal of Medicinal and Aromatic Plants 2013; 3: 125-30.
- Huopalathi R and Linko RR: Composition and content of aroma compounds in dill, Anethum graveolens at three different growth stages. Journal of Agricultural and Food Chemistry 1983; 31: 331-33.
- Blank I and Grosch W: Evaluation of potent odorants in dill seed and dill herb (Anethum graveolens) by aroma extract dilution analysis. Journal of Food Science 1991; 56: 63-7.
- Lawless J: The illustrated encyclopedia of essential oils. Shaftesbury Dorset Element 1995.
- Jirovetz L, Buchbauer G and Nikiforov A: Comparative analysis of different dill herb and dill seed oils constituents by means of GC/FID and GC/MS. Ernahrung / Nutrition 1994; 18: 534-36.
- Lis-Balchin M, Deans SG and Eaglesham E: Relationship between bioactivity and chemical composition of commercial essential oils. Flavour and Fragrance Journal 1998; 13: 98-04.
- Santos PAG, Figueiredo AC, Lourenco PML, Barrosa JG, Pedro LG, Oliverira MM, Schripsema J, Deans SG and Scheffer JCC: Hairy root cultures of Anethum graveolens(dill): Establishment, growth, time-course study of their essential oil and its comparison with parent plant oils. Biotechnology letters 2002; 24: 1031-36.
- Al-Snafi AE: The pharmacological importance of Anethum graveolens-a review. International Journal of Pharmacy and Pharmaceutical Sciences 2014; 6: 11-3.
- Saini N, Singh GK and Nagori BP: Spasmolytic potential of some medicinal plants belonging to family umbelliferae: a eview. International Journal of Research in Ayurveda and Pharmacy 2014; 5: 74-83.
- Ananthanaik T, Earanna N and Suresh CK: Influence of Azotobacter chroococcum strains on growth and biomass of Adathoda vasica Karnataka Journal of Agricultural Sciences 2007; 20: 613-5.
- Chaudhary D, Narula N, Sindhu SS and Behl RK: Plant growth stimulation of wheat (Triticum aestivum) by inoculation of salinity tolerant Azotobacter strains. Physiology and Molecular Biology of Plants 2013; 19: 515-9.
- Alemu F and Alemu T: Pseudomonas fluorescens isolates used as a plant growth promoter of Faba Bean (Vicia faba) in-vitro as well as in-vivo study in Ethiopia. American Journal Life Sciences 2015; 3: 100-8.
- Otieno N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ and Dowling DN: Plant growth promotion induced by phosphate solubilizing endophytic PseudomonasFrontiers in Microbiology 2015; 6: 745.
- Ghimire SR, Charlton ND and Craven KD: The mycorrhizal fungus, Sebacina vermifera, enhances seed germination and biomass production in switchgrass (Panicum virgatum L) BioEnergy Research 2009; 2: 51-8.
- Pirdashti H, Yaghoubian Y, Goltapeh E and Hosseini S: Effect of mycorrhiza-like endophyte (Sebacina vermifera) on growth, yield and nutrition of rice (Oryza sativa) under salt stress. Journal of Agricultural Technology 2012; 8: 1651-61.
- Baldi A, Farkya S, Jain A, Gupta N, Mehra R, Datta V, Srivastava AK and Bisaria VS: Enhanced production of podophyllotoxins by co-culture of transformed Linum album cells with plant growth-promoting fungi. Pure and Applied Chemistry 2010; 82: 227-41.
- Prasad R, Pham HG, Kumari R, Singh A, Yadav V, Sachdev M, Garg AP, Peskan T, Hehl S, Sherameti I, Oelmuller R and Varma A: Sebacinaceae: culturable mycorrhiza-like endosymbiotic fungi and their interaction with non-transformed and transformed roots. In Declerck S, Strullu DG, Fortin JA Ed In-vitro Culture of Mycorrhizas, Soil Biology Springer Berlin Heidelberg 2005: 291-12.
- Kumar V, Sahai V and Bisaria VS: High-density spore production of Piriformospora indica, a plant growth-promoting endophyte, by optimization of nutritional and cultural parameters. Bioresource Technology 2011; 102: 3169-75.
- Jeet K and Baldi A: Development of inorganic carrier based bioformulation of Sebacina vermifera and its evaluation on Trigonella foenumgraecum. International Journal of Pharma and Bio Sciences 2020; 11: 69-82.
- Jeet K, Malaviya A and Baldi A: Productivity enhancementof Coriandrum sativum using plant biologicals. International Journal of Pharmacy and Pharmaceutical Sciences 2020; 12: 60-72.
- ISTA: International rules for seed testing. Seed Science and Technology 1985; 13: 299-13.
- Ellis RH and Roberts EH: The quantification of ageing and survival in orthodox seeds. Seed Science and Technology Netherlands 1981; 9: 373-09.
- Dezfuli PM, Sharif-Zadeh F and Janmohammadi M: Influence of priming techniques on seed germination behavior of maize inbred lines (Zea mays ) ARPN Journal of Agricultural and Biological Science 2008; 3: 22-5.
- AOSA: Seed vigor testing handbook. contribution no. 32 to the handbook on Seed Testing. 1983.
- Coolbear P, Francis A and Grierson D: The effect of low temperature pre-sowing treatment under the germination performance and membrane integrity of artificially aged tomato seeds. Journal of Experimental Botany 1984; 35: 1609-17.
- Farooq M, Basra SMA, Ahmad N and Hafeez K: Thermal hardening: a new seed vigor enhancement tool in rice. Journal of Integrative Plant Biology 2005; 47: 187-93.
- Farooq M, Basra SMA, Hafeez-ue-Rehman and Mehmood T: Germination and early seedling growth as affected by pre-sowing ethanol seed treatments in fine rice. International Journal of Agriculture and Biology 2006; 8: 19-22.
- Srinivasan K and Saxena S: Effect of dormancy breaking treatments on seed quality during storage of four acacia species. Indian Journal of Forestry 2007; 30: 233-40.
- Abdul-Baki AA and Anderson JD: Vigour determination in soybean seed by multiple criteria. Crop Science 1973; 13: 630-3.
- Phillip JM and Hayman DS: Improved procedures for clearing roots and staining parasitic and VAM fungi for rapid assessment of infection. Transactions of the British Mycological Society 1970; 55: 158-61.
- Giovannetti M and Mosse B: An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 1980; 84: 489-500.
- Tarraf W, Ruta C, Tagarelli A, De Cillis F and De Mastro G: Influence of arbuscular mycorrhizae on plant growth, essential oil production and phosphorus uptake of Salvia officinalis Industrial Crops and Products 2017; 102: 144-53.
- Jeet K and Baldi A: Potential of microbes containing formulations to alter growth and phytochemicals of medicinal aromatic plant Foeniculum vulgare. International Journal of Lifescience and Pharma Research 2021; 11: 34-51.
- Barazani O, Benderoth M, Groten K, Kuhlemeier C and Baldwin IT: Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia2005; 146: 234-43.
- Dolatabadi HK, Goltapeh EM, Moieni A, Jaimand K, Sardrood BP and Varma A: Effect of Piriformospora indica and Sebacina vermifera on plant growth and essential oil yield in Thymus vulgaris in-vitro and in-vivoSymbiosis 2011: 53: 29-35.
- Dolatabadi HK and Goltapeh EM: Effect of inoculation with Piriformospora indica and Sebacina vermifera on growth of selected brassicaceae plants under greenhouse conditions. Journal of Horticultural Research 2013; 21: 115-24.
- Ghimire SR and Craven KD: Enhancement of switchgrass (Panicum virgatum) biomass production under drought conditions by the ectomycorrhizal fungus Sebacina vermifera. Applied Environmental Microbiology 2011; 77: 7063-67.
- Ray P, Ishiga T, Decker SR, Turner GB and Craven KD: A novel delivery system for the root symbiotic fungus, Sebacina vermifera and consequent biomass enhancement of low lignin COMT switchgrass lines. BioEnergy Research2015; 8: 922-33.
- Yousefi S, Kartoolinejad D, Bahmani M and Naghdi R: Effect of Azospirillum lipoferum and Azotobacter chroococcum on germination and early growth of hopbush shrub (Dodonaea viscosa) under salinity stress. Journal of Sustainable Forestry 2017; 36: 107-20.
- Demissie S, Muleta D and Berecha G: Effect of phosphate solubilizing bacteria on seed germination and seedling growth of faba bean (Vicia faba). International Journal of Agricultural Research 2013; 8: 123-36.
- Harper SHT and Lynch JM: Effects of Azotobacter chroococcum on barley seed germination and seedling development. Microbiology 1979; 112: 45-51.
- Tabatabaei S, Ehsanzadeh P, Etesami H, Alikhani HA and Glick BR: Indole-3-acetic acid (IAA) producing Pseudomonas isolates inhibit seed germination and α-amylase activity in durum wheat (Triticum turgidum) Spanish Journal of Agricultural Research 2016; 14: 0802.
- Vrbničanin S, Božić D, Sarić M, Pavlović D and Raičević V: Effect of plant growth promoting rhizobacteria on Ambrosia rtemisiifolia seed germination. Pesticides & Phytomedicine 2011; 26: 141-6.
- Rubenchik IL and Starkey RL: Azotobacter and its use in agriculture. Soil Science 1964; 98: 280.
- Mishustine N: The importance of non-symbiotic nitrogen-fixing micro-organisms in agriculture. Plant Soil 1970; 32: 545-54.
- Brown ME: Seed and root bacterization. Annual Review of Phytopatholgy 1974; 12: 181-97.
- Gholami A, Shahsavani S and Nezarat S: The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of Maize. International Journal of Biological, Biomolecular, Agricultural, Food and Biotechnological Engineering 2009; 3: 9-14.
- Ardebili ZO, Ardebili NO and Hamdi SMM: Physiological effects of Pseudomonas fluorescens CHA0 on tomato (Lycopersicon esculentum) plants and its possible impact on Fusarium oxysporum F. sp. lycopersici. Australian Journal of Crop Science 2011; 5: 1631-8.
- Rafter M, Yokoya K, Schofield EJ, Zettler LW and Sarasan V: Non-specific symbiotic germination of Cynorkis purpurea (Thouars) Kraezl a habitat-specific terrestrial orchid from the Central Highlands of Madagascar. Mycorrhiza 2016; 26: 541-52.
- Maighal M, Salem M, Kohler J and Rillig MC: Arbuscular mycorrhizal fungi negatively affect soil seed bank viability. Ecology and Evolution 2016; 6: 7683-9.
- Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ and Ast AV: Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signaling Behavior 2007; 2: 58-62.
- Dolatabadi HK, Goltapeh EM, Moieni A and Varma A: Evaluation of different densities of auxin and endophytic fungi (Piriformospora indica and Sebacina vermifera) on Mentha piperita and Thymus vulgarisAfrican Journal of Biotechnology 2012; 11: 1644-50.
- Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P and Kogel KH: Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. Journal of Plant Physiology 2008; 165: 60-70.
- Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J and Oelmüller R: The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Molecular Plant-Microbe Interactions 2008; 21: 1371-83.
- Xie H, Pastrnak JJ and Gilck BR: Isolation and characterization of mutants of plant growth promoting rhizobacteria Pseudomonas putida, GR12-2 that over produced indole acetic acid. Current Micr 1996; 32: 67-71.
- Lee YC, Johnson JM, Chien CT, Sun C, Cai DG, Lou BG, Oelmüller R and Yeh KW: Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indicais not stimulated by mycelium-synthesized auxin. Molecular Plant-Microbe Interactions 2011; 24: 421-31.
- Karthikeyan A and Sakthivel KM: Efficacy of Azotobacter chroococcum in rooting and growth of Eucalyptus camaldulensis stem cuttings. Research Journal of Microbiology 2011; 6: 618-24.
- Dong SQ, Tian ZH, Chen PJ, Kumar RS, Shen CH, Cai DG, Oelmüller R and Yeh KW: The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J of Experimen Botany 2013; 64: 4529-40.
- Li Y, Hou L, Song B, Yang L and Li L: Effects of increased nitrogen and phosphorus deposition on offspring performance of two dominant species in a temperate steppe ecosystem. Scientific Reports 2017; 7: 40951.
- Lakshminarayana K: Influence of Azotobacter on nitrogen nutrition of plants and crop productivity. Proceedings of the Indian National Science Academy B 1993; 59: 303-8.
- Kizilkaya R: Nitrogen fixation capacity of Azotobacter strains isolated from soils in different ecosystems and relationship between them and the microbiological properties of soils. J of Enviro Biology 2009; 30: 73-82.
- Rodrı́guez H and Fraga R: Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances 1999; 17: 319-39.
- Maheshwari SK, Gangrade SK and Trivedi KC: Comparative response of palmarosa to Azotobacter and nitrogen under rainfall and irrigated swards. Indian Perfume 1991; 35: 308-11.
- Mahfouz SA and Sharaf-Eldin MA: Effect of mineral vs. biofertilizer on growth, yield, and essential oil content of fennel (Foeniculum vulgare ). International Agrophysics 2007; 21: 361-6.
- Hemavathi, Navi V, Sivakumr BS, Suresh CK and Earanna N: Effect of Glomus fasciculatum and plant growth promoting rhizobacteria on growth and yield of Ocimum basilicum. Karnatak J of Ag Sci 2006; 19: 17-20.
- Banchio E, Bogino PC, Zygadlo J and Giordano W: Plant growth promoting rhizobacteria improve growth and essential oil yield in Origanum majorana Biochemical Systematics and Ecology 2008; 36: 766-71.
- Copetta A, Lingua G and Berta G: Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum var. Genovese.Mycorrhiza 2006; 16: 485-94.
- Kapoor R, Chaudhary V and Bhatnagar AK: Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua Mycorrhiza 2007; 17: 581-7.
- Mandal S, Upadhyay S, Wajid S, Ram M, Jain DC, Singh VP, Abdin MZ and Kapoor R: Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels. Mycorrhiza 2014; 25: 345-57.
- Floß DS, Hause B, Lange PR, Kuester H, Strack D and Walter MH: Knock-down of the MEP pathway isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids and abolishes normal expression of mycorrhiza-specific plant marker genes. The Plant Journal 2008; 56: 86-100.
- Mandal S, Upadhyay S, Singh VP and Kapoor R: Enhanced production of steviol glycosides in mycorrhizal plants: a concerted effect of arbuscular mycorrhizal symbiosis on transcription of biosynthetic genes. Plant Physiology and Biochemistry 2015; 89: 100-6.
- Torelli A, Trotta A, Acerbi L, Arcidiacono G, Berta G, Branca C: IAA and ZR content in leek (Allium porrum), as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant Soil 2000; 226: 29-35.
- Kapoor R, Giri B and Mukerji KG: Glomus macrocarpum: A potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens) and Carum (Trachyspermum ammi (Linn.) Sprague). World J of Microbiology and Biotechnology 2002; 18: 459-63.
- Strack D, Fester T, Hause B, Schliemann W and Walter MH: Review Paper: arbuscular mycorrhiza: biological, chemical, and molecular aspects. Journal of Chemical Ecology 2003; 29: 1955-79.
- Krishna H, Singh SK, Sharma RR, Khawale RN, Grover M and Patel VB: Biochemical changes in micropropagated grape (Vitis vinifera) plantlets due to arbuscular-mycorrhizal fungi (AMF) inoculation during ex vitro acclimatization. Scientia Horticulturae 2005; 106: 554-67.
- Sailo GL and Bagyaraj DJ: Influence of different AM-fungi on the growth, nutrition and forskolin content of Coleus forskohlii. Mycological Research 2005; 109: 795-8.
- Santoro MV, Zygadlo J, Giordano W and Banchio E: Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol Biochem 2011; 49: 1177-82.
- Baldi A: Production of anticancer drug, podophyllotoxin, by plant cell cultivation of Linum album. Dissertation Indian Institute of Technology Delhi New Delhi India 2008.
- Baldi A, Jain A, Gupta N, Srivastava AK and Bisaria VS: Co-culture of arbuscular mycorrhiza-like fungi (Piriformospora indica and Sebacina vermifera) with plant cells of Linum album for enhanced production of podophyllotoxins: A first report. Biotechnology Letters 2008; 30: 1671-7.
- Farkya S, Baldi A, Kumar V, Datta V, Mehra R, Gupta N, Jain A, Srivastava AK and Bisaria VS: Impact of symbiotic fungi on production of secondary metabolites by plant cell culture. Asia-Pacific Journal of Molecular Biology and Biotechnology 2010; 18: 51-3.
- Bisaria VS, Baldi A, Kumar V, Gupta N, Jain A, Farkya S and Srivastava AK: Interaction of phytopromotional fungi and plant cells on synthesis of plant-derived metabolites. Journal of Biotechnology 2008; 136:
- Baldi A, Jain A, Gupta N, Srivastava AK and Bisaria VS: Co-culture of Linum album cells and Piriformospora indica for improved production of phytopharmaceuticals. In: Varma A, Kharkwal AC (ed) Symbiotic fungi. Springer Berlin Heidelberg 2009: 361-72
- Baldi A, Srivastava AK and Bisaria VS: Fungal elicitors for enhanced production of secondary metabolites in plant cell suspension cultures. In Varma A, Kharkwal AC (Ed) Symbiotic Fungi Springer Berlin Heidelberg 2009: 373-80.
- Baldi A and Dixit VK: Yield enhancement strategies for artemisinin production by suspension cultures of Artemisia annua. Bioresource Technology 2008; 99: 4609-14.
- Baldi A, Singh D and Dixit VK: Dual elicitation for improved production of withaferin A by cell suspension cultures of Withania somnifera. Applied biochemistry and biotechnology 2008; 151: 556-64.
How to cite this article:
Jeet K and Baldi A: Trending microbiologicals and their role to enhance growth and essential oil content of dill (Anethum graveolens). Int J Pharm Sci & Res 2021; 12(2): 875-88. doi: 10.13040/IJPSR.0975-8232.12(2).875-88.
All © 2013 are reserved by the International Journal of Pharmaceutical Sciences and Research. This Journal licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.
K. Jeet and A. Baldi *
Department of Pharmaceutical Sciences & Technology, Maharaja Ranjit Singh Punjab Technical University, Bathinda, Punjab, India.
03 February 2020
15 June 2020
30 June 2020
01 February 2021