Research Article

Split Viewer

J Plant Biotechnol (2023) 50:239-247

Published online December 11, 2023

https://doi.org/10.5010/JPB.2023.50.030.239

© The Korean Society of Plant Biotechnology

Effects of arbuscular mycorrhizal fungi on enhancing growth, fruit quality, and functional substances in tomato fruits (Lycopersicon esculentum Mill.)

Thanapat Suebrasri・Wasan Seemakram・Chanon Lapjit・Wiyada Mongkolthanaruk・Sophon Boonlue

Faculty of Allied Health Sciences, Nakhon Ratchasima College, Nakhon Ratchasima, 30000, Thailand
Department of Microbiology, Faculty of Science, Khon Kaen University, Khon Kaen, 40002, Thailand
Department of Horticulture, Faculty of Agriculture, Khon Kaen University, Khon Kaen, 40002, Thailand

Correspondence to : e-mail: bsopho@kku.ac.th

Received: 4 October 2023; Revised: 21 October 2023; Accepted: 21 October 2023

This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

This study aimed to investigate the efficiency of arbuscular mycorrhizal fungi (AMF) in enhancing plant performance and bioactive compound concentrations in tomatoes (Lycopersicon esculentum Mill.). This factorial pot experiment included nine replications over 120 days of cultivation. Three AMF species (Rhizophagus prolifer, Claroideoglomus etunicatum, and Acaulospora mellea) were utilized as inoculum, while non-mycorrhizal controls with or without synthetic NPK fertilizer were compared. Interestingly, C. etunicatum KS-02 inoculations effectuated the best fruit growth and weight, which were statistically higher than those of the control without AMF. However, only fruit fresh weight was higher in plants inoculated with C. etunicatum KS-02 than those treated with the synthetic NPK fertilizer. In addition, C. etunicatum KS-02 inoculations induced a ≥ 11% increase in DDPH (1,1-diphenyl-2-picrylhydrazyl) activity, lycopene content, and carotenoid content compared to the control. This study is the first to report Claroideoglomus species’ effectiveness in promoting growth, fruit yield, and bioactive compound production in L. esculentum Mill. These findings substantiate the significant potential of C. etunicatum KS-02 for tomato cultivation without the adverse effects of excessive synthetic fertilizer use.

Keywords Antioxidants, Carotenoids, Lycopene, Phytochemical, Tomato production

Tomato (Lycopersicon esculentum Mill.) is the second most important fruits and vegetable crop in the world, next to the potatoes. Ripe fruits are small, sweet and crispy in taste. They are commonly consumed as fresh fruit or can be eaten with salads. The fruits are rich in antioxidants such as carotenoids and vitamin C, with lycopene representing the main carotenoid, accounting for 80% of all carotenoids (Nguyen and Schwartz 1999). The fruits can be processed in a variety of industries to create products such as ketchup and tomato juice or used as an ingredient in some food condiments. This has resulted in a high demand value of up to 16 million tons per year. There is 6,328.8 hectare of tomato cultivation area in Thailand, most of this area being located in northeastern Thailand. The total yield in 2020 was 132,650 tons. However, tomato production in this area experiences many problems, including disease, insects or unacceptable weather conditions such as high temperatures, drought and low nutrient content in the soil. These factors result in lower yield and a poorer fruit quality of tomatoes (Lahoz et al. 2016). In light of this, a great deal of focus has fallen on new approaches to improve plant growth and increase specific substance content. At present synthetic fertilizer is commonly utilized to boost plant production (Seemakram et al. 2022). However, over long-term use, these synthetic fertilizers have been found to decrease soil quality with a notable reduction in beneficial soil microbes and evidence of toxic residues (Chandini et al. 2019). One way to lessen agriculture’s dependency on synthetic fertilizers is through the use of plant-growth-promoting microorganisms (PGPM), which are a focus of interest and study because of their environmentally friendly nature (Andre et al. 2016; Seemakram et al. 2022).

Soil fertility has been declining as a result of cultivation for a long time. Thus, there is an evident need for cultivation management by other means, particularly with the soil biota, which facilitates improved growth performance of tomato fruit. Arbuscular mycorrhizal fungi (AMF), a soil biota belonging to the Division Glomeromycota, offers great potential. It involves a process of fungal symbiosis that colonizes the roots of over 80% of land plants (Boonlue et al. 2012) AMF symbiosis can be observed in nearly all ecosystems and occurs naturally in most plant species. One of the effects of this symbiotic relationship is to increase nutrient uptake from the soil for nutrients such as phosphorus (P), nitrogen (N) and potassium (K), and micronutrients that help for enhancing plant growth (Jeffries 1987). AMF also aids plant growth under adverse environmental conditions, such as aridity, and help prevent diseases in the root system (Seemakram et al. 2021). Moreover, AMF serves to help plants adjust the osmotic balance within their cells (Nacoon et al. 2021), and strengthen plant tolerance to stresses, such as salinity and heavy-metal pollution (Salam et al. 2017). Owing to the above benefits, some species of arbuscular mycorrhizal are of interest for utilization in bio-fertilizers to replace chemical fertilizers, etc.

Therefore, our principle objective was to investigate the role various species of AMF played on the growth performance, and the lycopene, carotenoid, and 1,1-diphenyl-2-picryl-hydrazyl (DPPH) content of the fruit of Lycopersicon esculentum Mill. varieties T72011. AMF treatment of the species was compared with two controls (without AMF inoculation and with chemical fertilizer treatment); a treatment with existing fertile soil and one with the addition of mineral fertilizer. However, there are currently no reports investigating the effects of AMF on the growth and combined production of secondary metabolites in tomatoes. The results obtained in this research could provide a framework for an in-situ application of AMF to increase tomato cultivation in Thailand. Mycorrhizal management offers economic benefits as an alternative to purchasing mineral fertilizer; therefore, this study offers potential options for the agricultural sector to decrease expenses and boost income.

AMF preparation

The AMF species, Rhizophagus prolifer PC2-2 (Seemakram et al. 2021, 2022), Claroideoglomus etunicatum KS-02 (Nacoon et al. 2023) and Acaulospora mellea KKU-NBP-SB-2 (Khaekhum et al. 2017), were obtained from Mycorrhiza and Mycotechnology Laboratory and used as the fungal inoculum. The maize was used as the host plant for production of AMF spore following the methods of Boonlue et al. (2012). Soil was sterilized twice then placed in 8-inch-diameter plastic pots for use as a plant substrate. Surface sterilization of maize seed was performed by soaking in 6% sodium hypochlorite solution for 30 min. Around 200 AMF spores were added to the pots containing sterile maize seeds, before the maize was cultivated in a greenhouse at a temperature of 30-35°C with daily irrigation until 90 days, when watering ceased and the plants began to dry. The plants were cut just above the soil surface. Finally, soil samples were first dried and then crushed into finely ground particles. The purity of the spores and the total spore number were determined using the sucrose centrifugation method (Daniels and Skipper 1982). These dried soils containing AMF spores, mycelia and infected roots were then used as the inoculum in the experiments.

Soil preparation

The sandy loam soil properties include pH, electrical conductivity (EC), organic matter (OM), nitrogen (N), phosphorus (P), potassium (K), available phosphorus, exchangeable potassium, calcium (Ca), and sodium (Na) were analyzed according to the method described by Seemakram et al (2021). The soil samples were sterilized and stored overnight at room temperature, before being sterilized again under the same conditions, then packed in 6-inch diameter plastic pots; each pot contained 3 kg.

Tomato seed preparation

Tomato cultivars of Lycopersicon esculentum Mill. varieties T72011 were obtained by Asist. Prof. Dr. Chanon Lapjit, Faculty of Agriculture, Khon Kaen University, Thailand from the Horticultural station, Khon Kaen University, which develops and distributes them. The tomato seeds were sterilized with 6% sodium hypochlorite for 5 min, before being rinsed with sterile distilled water for 3 min. The sterilized seeds were placed in sterilized Petri dishes for 5 to 7 days, where root germination was observed. The seedlings were cultivated in peatmoss-filled trays for 2 weeks, after which the mature seedlings (of around 10cm in height) were transferred to plastic pots.

Experimental design and treatment

The pot experiment was carried out in a greenhouse at the Faculty of Science, Khon Kaen University, Thailand. The experimental design was conducted with a factorial completely randomized design (CRD) with 5 treatments in 6 replications as follows: (T1) control, sterilized soil without AMF; (T2) control with mineral fertilizer, sterilized soil without AMF with the addition of mineral nutrients (N,P,K: 15-15-15) at 0.32 g per pot; (T3) inoculation with R. prolifer PC2-2; (T4) inoculation with A. mellea KKU-NBP-SB-2; and (T5) inoculation with C. etunicatum KS-02. The AMF inoculum was applied adjacent to the plant root at a rate of approximately 200 spores/pot. After 3 months the plants were harvested.

Mycorrhizal root colonization

Mycorrhizal root colonization intensity was determined according to the method described by Koske and Gemma (1989). Roots were washed with 10% KOH for 3 min at 95°C, and then soaked in 2% HCl overnight. Trypan blue solution (0.05%) was used to stain root samples, which were then cut into 1 cm long pieces. The cellular structures of AMF, including vesicles, arbuscules, and hyphae, were observed using a microscope at 40 × magnification (SMZ745T Nikon, Japan) (Seemakram et al. 2022).

Determination of plant growth parameters

After 90 days of transplantation, the parameters of plant growth including plant height, stem diameter, SPAD and leaf area (Arnon 1949) were evaluated. The number and fresh weight of fruit were analyzed at harvest. Leaves, stem and roots were dried in an oven at 80°C for 3 days prior to analysis, and the dry weight measured to record plant biomass. The nutrient uptake concentration (N, P and K) of the samples was next determined. The parameters determining the quality of the plant roots, including the diameter, specific root length (SRL) and root tissue density (RTD), were measured by scanning the root samples using an Epson scanner V800 PHOTO, and the data were analyzed using WINRHIZO Pro2004a software (REGENT Instruments Inc., Quebec, QC, Canada).

Lycopene and Carotenoid content measurement

Fruit samples were cut and blended using a blender. Then, the samples were kept on ice in dark conditions. The sample of 0.2 g was transferred to a 50 mL covered test tube. A total of 20 mL of hexane: acetone: ethanol (HAE) of 2:1:1 (v/v/v) was added to the sample tubes. After that, the samples were mixed for 10 min and 3 mL of distilled water was added to each sample tube. The samples were agitated for several minutes. Then, the samples were kept at room temperature. The supernatant of the hexane layer that contained lycopene and carotenoid was measured using a spectrophotometer at the wavelengths of 503 and 449 nm, respectively. The lycopene and carotenoid contents were calculated according to the formula described by Biswas et al. (2011) and Fester et al. (2002)

Antioxidant content measurement

Free-radical-scavenging activity of 1,1-diphenyl-2-picryl-hydrazyl (DPPH) was detected modifying to the method described by Leong and Shui (2002). A freshly 0.1 mM solution of DPPH in methanol was prepared. A 100 µL of each sample (with appropriate dilution) was first mixed with 4.0 mL of DPPH solution, before holding at room temperature for 30 min prior to measurement. The mixture solution was measured at 517 nm and detected by spectrophotometer. Methanol (0.5 mL), replacing the sample, was used as the blank. The percentage of radical-scavenging ability was analyzed by using the following formula:

Scavenging ability (%) = (Absorbance 517 nm of control - Absorbance 517 nm of sample) / Absorbance 517 nm of control × 100

Statistical analysis

All data from this work were evaluated by analysis of variance (ANOVA) for data from the factorial CRD. Fisher’s least significant difference (LSD) was significant at p ≤ 0.05. The correlation between data was analyzed using Statistix 10 software.

Mycorrhizal colonization

The quantity of AMF spores and root colonization in Lycopersicon esculentum Mill. was measured and is reported in Table 1. In addition, AMF was found in the plant roots, such as hyphae, vesicles and arbuscules, in various structures. In the treatment without AMF (treatments T1 and T2), spores in the soils and tomato root colonization were not detected.

Table 1 AMF spores in soil and AMF colonization in tomato roots

TreatmentSpore/gram soilRoot colonization (%)
T10.00c0.00c
T20.00c0.00c
T32.68b20.19ab
T410.29ab28.23a
T521.14a29.01a
% cv.11.3628.09
F-test*n.s.

Numbers followed by the same letters in each column indicate values that were not significantly different according to the LSD test. * significant difference at p ≤ 0.05, ** significant difference at p ≤ 0.01. T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s, not significant.



Effects of AMF on plant growth parameters

The ability of AMF to enhance plant growth was detected with respect to plant height, leaf greenness, diameter, leaf area, stem dry weight, leaf dry weight and root dry weight. In addition, the plant yield, including the number of fruits and the fruit fresh weight, was also evaluated (Table 2). The presence of AMF was found to increase all of the plant growth parameters in comparison to the control plant (T1). All of the plant growth parameters and yields in these treatments were significantly increased when compared to the control plant treatment. In the case of tomato inoculated with C. etunicatum KS-02 treatment, all plant growth parameters were found to be statistically higher than those of the control without AMF. Moreover, the highest yield or fruit fresh weight was also found in the C. etunicatum KS-02 treatment (T5). Therefore, the best AMF treatment for enhancing the growth of tomato was demonstrated to be C. etunicatum KS-02 (T5).

Table 2 Effects of AMF on tomato growth

TreatmentSPADHeight (cm)Diameter (cm)Leaf area (cm2)Total number of fruitsFruit fresh weight (g)Stem dry weight (g)Leaf dry weight (g)
T130.25b68.80b13.01b15.09c5b10.16c3.92b1.96a
T245.32a76.50ab16.90a30.78a10a18.38b7.62a2.18a
T340.18a68.50b15.10ab25.75ab8ab24.16ab5.56b2.32a
T438.06a74.50ab13.70b20.02b11a25.17ab6.61ab2.18a
T539.27a78.60a16.70a29.35a10a40.70a7.64a2.67a
% cv.20.1825.0124.5027.5224.3129.0727.0925.67
F-test**********n.s.

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant.



Table 3 shows the plant root growth performance of the tomato plants grown under different conditions. The results indicate that most of the root traits were significantly improved by inoculation with either AMF compared to control plant (T1). Nevertheless, the root dry weight and specific root length of the plants inoculated with A. mellea KKU-NBP-SB-2 (T4) and with C. etunicatum KS-02 (T5) were significantly higher than those of the control plant (T1).

Table 3 Effects of AMF on tomato root growth

TreatmentRoot dry weight (g)Average diameter (mm)Specific root length (m g-1)Root tissue density (g cm-3)
T10.91ab0.28a107.95b94.02a
T21.23a0.30a113.31ab78.03ab
T30.88b0.29a113.18ab83.60ab
T41.09ab0.28a124.11ab81.78ab
T51.24a0.28a149.93a67.69b
% cv.21.3628.0925.7124.02
F-test*n.s.**

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant.



Effects of AMF on N, P and K contents

The effects of AMF on NPK concentration in tomato plants are indicated in Table 4. The tomato plants to which chemical fertilizer had been applied showed the maximum value of N,P. Among the AMF-inoculated treatments, N accumulation in the plants was increased but no significant difference was found with the non-inoculated control. The concentration of P in tomato plant inoculated with AMF was not statistically higher than that of the control treatment. However, the highest phosphorus content was detected in the tomato inoculation with R. prolifer PC2-2. The concentration of potassium (K) was found to be statistically higher in all treatments inoculated with AMF than in the control. In the tomato plants inoculated with C. etunicatum KS-02, the highest K concentration was found. These results reveal that AMF enhanced mineral (N, P and K) contents in tomato plants, and particularly K, compared with the non-inoculated control.

Table 4 Effects of AMF on nitrogen, phosphorus, and potassium concentrations in tomatoes

TreatmentN concentration (mg g-1)P concentration (mg g-1)K concentration (mg g-1)
T116.6b10.2b10.9b
T221.2a23.3a13.7ab
T317.5ab15.1ab15.7a
T416.9b10.1b14.4ab
T519.9ab13.8b15.9a
% cv.29.0925.8327.42
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; N, Nitrogen; P, Phosphorus; K, Potassium.



Effects of AMF on antioxidant activity, lycopene content and carotenoid content

Fruit lycopene content, carotenoid content and antioxidant activity increased with all of the AMF treatments compared to the control treatment without fertilizer, and no significant difference was found with chemical fertilizer treatment. The maximum antioxidant activity (97.29%), lycopene content (0.62 µg/g) and carotenoid content (3.22 µg/g) were found in the C. etunicatum KS-02 treatment, which showed a significant difference from the non-inoculated control (Table 5). In addition, this finding was not significantly different to chemical fertilizer treatment. Therefore, the best performance in terms of fruit lycopene content, carotenoid content and antioxidant activity was found in the treatment of the plant inoculated with C. etunicatum KS-02, which might be used instead of chemical fertilizer.

Table 5 Effect of AMF on antioxidant activity, lycopene content, and carotenoid content in tomatoes

TreatmentDPPH (%)Lycopene (µg/g)Carotenoid (µg/g)
T187.14b0.42b2.37b
T296.26a0.52ab3.38a
T396.23a0.49b3.26a
T495.61a0.59ab3.16a
T597.29a0.62a3.22a
% cv.27.0925.7125.32
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi.



Correlations between AMF, % colonization, nutrient uptake and the concentration of secondary compounds and the plant growth parameters of tomato at the harvest stage are shown in Table 6. Mycorrhizal colonization and root dry weight significantly positively correlated with the number of fruit, fruit fresh weight, antioxidant activity, lycopene content and K concentration of the plant. Among the AMF treatments, C. etunicatum KS-02 was significantly positively correlated with fruit fresh weight, antioxidant activity, lycopene content and the K concentration of the plant. The number of fruit and fruit fresh weight were significantly positively correlated with DPPH activity, lycopene content and carotenoid content, and the K concentration of the plant. Additionally, DPPH activity, lycopene content and carotenoid content were significantly positively correlated with the K concentration of the plant.

Table 6 Correlation between AMF, nutrient uptake, antioxidants, lycopene, and carotenoids in tomatoes

CorrelationCFAMF1AMF2AMF3Root colonizationNo. of sporesRoot dry weightNo. of fruitFruit fresh weightDPPHLycopeneCarotenoidsNP
Root colonization-0.59**0.18 ns0.48*0.51*
No. of spores-0.42 ns-0.25 ns0.21 ns0.88**0.81**
Root dry weight0.52*-0.62**0.06 ns0.55*0.16 ns0.53*
No. of fruit0.28 ns-0.18 ns0.51*0.28 ns0.58*0.53*0.73**
Fruit fresh weight-0.26 ns0.02 ns0.07 ns0.84**0.83**0.92**0.54*0.63**
DPPH0.23 ns0.23 ns0.14 ns0.37 ns0.60**0.49*0.57*0.86**0.75**
Lycopene0.10 ns-0.01 ns0.36 ns0.47*0.73**0.68**0.67**0.94**0.82**0.94**
Carotenoids0.41 ns0.25 ns0.11 ns0.19 ns0.43 ns0.29 ns0.55*0.84**0.58*0.97**0.87**
N0.76**-0.25 ns-0.41ns0.40 ns-0.15 ns0.18 ns0.81**0.48 ns0.35 ns0.56*0.47*0.62**
P0.91**0.06 ns-0.45**-0.07 ns-0.42 ns-0.29 ns0.48 ns0.30 ns-0.02 ns0.46 ns0.24 ns0.61**0.85**
K-0.11 ns0.43 ns0.07 ns0.49*0.77**0.61**0.33 ns0.68**0.85**0.92**0.86**0.83**0.33 ns0.19 ns

**, significant difference at p ≤ 0.01; *, significant difference at p ≤ 0.05; ns, not significant. R. prolifer PC2-2 (AMF1), A. mellea KKU-NBP-SB-2 (AMF2); and C. etunicatum KS-02 (AMF3)


According to our previous studies, the species of AMF showed high efficiency in enhancing plant growth and biomass in perennial plants belonging to the legume family (Siamese rosewood and Burma padauk) (Seemakram et al. 2021) and cannabis (Seemakram et al. 2022). Therefore, we expected inoculation with AMF to play a key role in boosting the growth and production of secondary metabolites in tomato. The efficiency of three AMF species, namely R. prolifer PC2-2, C. etunicatum KS-02 and A. mellea KKU-NBP-SB-2, was investigated for its capacity to promote the growth and production of secondary metabolites of tomato (L. esculentum Mill.), compared with the effect of the application of synthetic NPK fertilizer under greenhouse conditions. Claroideoglomus etunicatum KS-02 showed a higher root colonization than that of A. mellea KKU-NBP-SB-2 (28.23%) and R. prolifer PC2-2 (20.19%). A study using concentrations of C. etunicatum up to 51% (Ziane et al. 2017) observed higher root colonization in tomato roots compared with our findings. The data from our study is similar to the value of the mycorrhizal colonization of black rice (Maled Phai and Niew Dam Hmong) of 25, and the value of 9% reported by Nacoon et al. (2023).

This study identified that colonization with AMF affected growth performance of tomato cultivars and the production of secondary metabolites of tomato fruits beneficially under greenhouse conditions. Treatment with C. etunicatum KS-02 significantly affected the SPAD value, height, diameter, leaf area and biomass of the tomato plant. Our data show similar results to those of Ziane et al. (2017), who reported that the overall height and biomass of tomato inoculated with the commercial AMF inoculum were significantly increased. Mutumba et al. (2018) documented the effect of mycorrhizal fungi on improving the plant growth parameters and chlorophyll index of the host plant. In addition, our results concur with those in previous literature using other plant species. Inoculation with R. prolifer PC2-2 in Siamese rosewood, Burma padauk and cannabis resulted in an increase in the leaf area and biomass (Seemakram et al. 2021). Moreover, black rice inoculated with C. etunicatum outperformed non-inoculated plants in the absence of mineral fertilizer in terms of biomass (Nacoon et al. 2023). Mineral fertilizer boosted plant performance when applied, but the effect was non-significant in terms of biomass. The symbiotic relationship between AMF and host plants enhances plant growth and biomass, and enables the plant to resist abiotic stress conditions (Alam et al. 2023). Furthermore, AMF inoculation significantly affected the number of tomato fruits yielded and fruit fresh weight. Consistent with previous studies, the incorporation of inoculated Funneliformis mosseae into the continuous cropping substrate remarkably improved the growth and yield of tomatoes, and resulted in a slender rise in fruit size in tomato production (Wang et al. 2021). The above results affirm that AMF inoculation resulted in greater fruit numbers regardless of the fertilization criterion in tomato.

As may be expected, for the roots of tomato plants colonized by AMF in all treatments, the root qualities were affected. However, the root dry weight and specific root length after treatment with C. etunicatum KS-02 were significantly higher than those of non-inoculated plants. This may have resulted from the introduction of AMF, leading to more effective root colonization, which affected the root qualities, especially root dry weights, which were significantly greater in inoculated plants compared to non-inoculated plants (Ziane et al. 2017). These results suggest that the inoculation of AMF had an effect on specific root traits, but not all of them (Seemakram et al., 2022). Furthermore, plants inoculated with C. etunicatum KS-02 exhibited slightly higher N, P and K concentrations. This is perhaps due to mycorrhizal plants exploring a greater volume of soil for available nutrients and water than uninoculated ones, leading to the recorded increase in N, P and K (Evelin et al. 2012). However, considering nutrient concentration among the tomato plants, all plants inoculated with AMF demonstrated a value of K which was significantly higher than that of the uninoculated plant.

Both inoculation with AMF and synthetic fertilizer served to increase the performance of tomato and increased the capacity of the DPPH, lycopene content and carotenoid content compared to the unfertilized control. The maximum DDPH activity and lycopene and carotenoid contents for the C. etunicatum KS-02 treatment were found to be higher than those seen in the non-inoculated control treatment. A positive correlation was found between K uptake and an increase in DPPH activity, in addition to lycopene and carotenoid content. Moreover, inoculation with C. etunicatum KS-02 in tomato cultivation showed a positive correlation between lycopene and K uptake. Lycopene is one of the precursors of carotenoid synthesis, formed through the cyclization of lycopene, which has a positive correlation with K (Heldt 2003; Taber 2006). In addition, root colonization and root dry weight exhibited positive correlations with the number of fruit and fruit fresh weight, resulting in increased lycopene and carotenoid accumulation in the fruit. Our data are similar to those of Ordookhani et al. (2010), who reported that a positive correlation between lycopene and shoot potassium was found in plants treated with PGPR. Stimulation of the carotenoid metabolism was correlated with the root colonization of AMF (Fester et al. 2002). AMF colonization activated plant defense mechanisms producing of phenolics and flavonoids (Zhao et al. 2022). Avio et al. (2017) reported that R. irregulare IMA6 increased the phenolics concentration and antioxidant activity in tomato plants. In general, tomato cultivation with AMF led to increased carotenoid and total phenolic contents, while AMF inoculation also increased lycopene content in cultivated tomatoes (Ulrichs et al. 2008). In previous work reported that the increase in functional substances in plants was correlated with increases in phosphorus acquisition (Seemakram et al. 2022). Our results contradict those from previous studies, which partly supported the nutritional mechanism of tomato, indicated by the correlations between AMF and K concentration with an increase in antioxidant activity, lycopene content and carotenoid content.

Our study shows that using AMF obtained a similar result in terms of plant growth performance, tomato yield and functional compounds in tomato fruit compared with the application of chemical fertilizer; inoculation with C. etunicatum KS-02 was particularly successful. Further, high levels of antioxidant compounds, such as lycopene and carotenoids, in tomato fruit may boost market price, especially where the tomato plant is cultivated organically (Pataro et al., 2020). Nevertheless, the use of AMF alone had substantial benefits regarding plant growth and quality and functional compounds in tomato fruit. As highlighted above, the use of chemical fertilizers enhanced some physical plant characteristics more rapidly than with the use of AMF. Best practice for agribusiness would be utilizing chemical fertilizers in combination with biological techniques in order to achieve the highest efficiency in the production of tomato yield and to maximize the quality of fruit with a high content of functional compounds, while minimizing environmental damage. In this regard, the inoculation of C. etunicatum KS-02 could, with careful management, help farmers to reduce the production costs of tomato cultivation by providing a partial or complete alternative to chemical fertilizer. The combined use of AMF and fertilizer application, including organic soil management, is the main target that warrants further investigation.

Our study demonstrates the effect of AMF inoculation on the growth promotion, yield and bioactive compound production of tomato (L. esculentum Mill.), showing no significant difference from chemical fertilizer application. AMF treatment also led to significant correlations between mycorrhizal colonization, fruit weight, fruit number, concentration of K and bioactive compound content. We found that Claroideoglomus etunicatum KS-02 was the best plant growth promoter, being able to promote growth, fruit yield, antioxidant capacity, lycopene and carotenoids in tomato compared with non-inoculated plants under unfertilized conditions. This species warrants further analysis as a means to developing an AMF inoculum alternative for the industrial production of tomato, replacing the immoderate application of synthetic fertilizer which characterizes current conventional practices.

This work was supported by the Fundamental Fund of Khon Kaen University in FY 2022, grant no. FRB650032/0161, which received funding support from the National Science, Research and Innovation Fund (NSRF).

This research was supported by the Fundamental Fund of Khon Kaen University in FY 2022, grant no. FRB650032/0161, through the research on growth enhancement and carotenoid accumulation in tomato fruit by arbuscular mycorrhizal fungi by Khon Kaen University, Department of Microbiology, Faculty of Science, which received funding support from the National Science, Research and Innovation Fund (NSRF).

  1. Alam MZ, Choudhury TR, Mridha MAU (2023) Arbuscular mycorrhizal fungi enhance biomass growth, mineral content, and antioxidant activity in tomato plants under drought stress. J Food Qual 2023:2581608. https://doi.org/10.1155/2023/2581608
    CrossRef
  2. Andre CM, Hausman JF, Guerriero G (2016) Cannabis sativa: The plant of the thousand and one molecules. Front Plant Sci 7:19. https://doi.org/10.3389/fpls.2016.00019
    Pubmed KoreaMed CrossRef
  3. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1-15. http://doi.org/10.1104/pp.24.1.1
    Pubmed KoreaMed CrossRef
  4. Avio L, Sbrana C, Giovannetti M, Frassinetti S (2017) Arbuscular mycorrhizal fungi affect total phenolics content and antioxidant activity in leaves of oak leaf lettuce varieties. Sci Hortic 224:265-271. https://doi.org/10.1016/j.scienta.2017.06.022
    CrossRef
  5. Biswas AK, Sahoo J, Chatli MK (2011) A simple UV-Vis spectrophotometric method for determination of β-carotene content in raw carrot, sweet potato and supplemented chicken meat nuggets. LWT - Food Sci Technol 44: 1809-1813
    CrossRef
  6. Boonlue S, Surapat W, Pukahuta C, Suwanarit P, Suwanarit A, Morinaga T (2012) Diversity and efficiency arbuscular mycorrhizal fungi in soils from organic chili (Capsicum frutescens L.) farms. Mycoscience 53:10-16
    CrossRef
  7. Chandini, Kumar R, Kumar R, Prakash O (2019) The impact of chemical fertilizers on our environment and ecosystem. In: Research Trends in Environmental Sciences (2nd ed.). New Delhi, India (pp 71-86)
  8. Daniels BA, Skipper HD (1982) Method for the recovery and quantitative estimation of propagules from soil. In: Schenck, N.C. (Ed.), Method and Principle of Mycorrhizal Research. Am. Phytopathol. Soc., St. Paul Minnesota, USA (pp 29-36)
  9. Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203-217
    Pubmed CrossRef
  10. Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216(1):148-54
    Pubmed CrossRef
  11. Heldt HW (2003) Pflanzenbiochemie. 3. Auflage. Spektrum Akademischer Verlag, Heidelberg. p 622
  12. Khaekhum S, Lumyong S, Kuyper TW, Boonlue S (2017) Species richness and composition of arbuscular mycorrhizal fungi occurring on eucalypt trees (Eucalyptus camaldulensis Dehnh.) in rainy and dry season. Curr Res Environ Appl Mycol 7(4): 282-292. https://doi.org/10.5943/cream/7/4/5
    CrossRef
  13. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486-505. https://doi.org/10.1016/S0953-7562(89)80195-9
    CrossRef
  14. Lahoz I, Pérez-de-Castro A, Valcárcel M, Macua JI, Beltrán J, Roselló S, Cebolla-Cornejo J (2016) Effect of water deficit on the agronomical performance and quality of processing tomato. Scientia Horticulturae 200:55-65. https://doi.org/10.1016/j.scienta.2015.12.051
    CrossRef
  15. Leong LP, Shui G (2002) An Investigation of antioxidant capacity of fruits in Singapore markets. Food Chem 76:69-75. https://doi.org/10.1016/S0308-8146(01)00251-5
    CrossRef
  16. Mutumba FA, Zagal E, Gerding M, Castillo-Rosales D, Paulino L, Schoebitz M (2018) Plant growth promoting rhizobacteria for improved water stress tolerance in wheat genotypes. J Soil Sci Plant Nutr 18(4):1080-1096. https://doi.org/10.4067/S0718-95162018005003003
    CrossRef
  17. Nacoon S, Ekprasert J, Riddech N, Mongkolthanaruk W, Jogloy S, Vorasoot N, Cooper J, Boonlue S (2021) Growth enhancement of sunchoke by arbuscular mycorrhizal fungi under drought condition. Rhizosphere 17:100308. https://doi.org/10.1016/j.rhisph.2021.100308
    CrossRef
  18. Nacoon S, Seemakram W, Ekprasert J, Theerakulpisut P, Sanitchon J, Kuyper TW, Boonlue S (2023) Arbuscular mycorrhizal fungi enhance growth and increase concentrations of anthocyanin, phenolic compounds, and antioxidant activity of Black Rice (Oryza sativa L.). Soil Syst 7:44. https://doi.org/10.3390/soilsystems7020044
    CrossRef
  19. Nguyen ML, Schwartz SJ (1999) Lycopene: chemical and biological properties. Food Technol 53:38-45
  20. Ordookhani K, Khavazi K, Moezzi A, Rejali F (2010) Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr J Agric Res 5(10):1108- 1116
  21. Pataro G, Carullo D, Falcone M, Ferrari G (2020) Recovery of lycopene from industrially derived tomato processing by-products by pulsed electric fields-assisted extraction. Innov Food Sci Emerg Technol 63. https://doi.org/10.1016/j.ifset.2020.102369
    CrossRef
  22. Salam EA, Alatar A, El-Sheikh MA (2017) Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J Biol Sci 25:1772-1780. https://doi.org/10.1016/j.sjbs.2017.10.015
    Pubmed KoreaMed CrossRef
  23. Seemakram W, Paluka J, Suebrasri T, Lapjit C, Kanokmedhakul S, Kuyper TW, Ekprasert J, Boonlue S (2022) Enhancement of growth and Cannabinoids content of hemp (Cannabis sativa) using arbuscular mycorrhizal fungi. Front Plant Sci 13: 845794.https://doi.org/10.3389/fpls.2022.845794
    Pubmed KoreaMed CrossRef
  24. Seemakram W, Suebrasri T, Khaekhum S, Ekprasert J, Aimi A, Boonlue S (2021) Growth enhancement of the highly prized tropical trees siamese rosewood and burma padauk. Rhizosphere 19:100363. https://doi.org/10.1016/j.rhisph.2021.100363
    CrossRef
  25. Taber HG (2006) Potassium application and leaf sufficiency level for fresh-market tomatoes on a Midwestern United States fine-textured soil. HortTechnology 16:247-252
    CrossRef
  26. Ulrichs C, Fischer G, Büttner C, Mewis I (2008) Comparison of lycopene, b-carotene and phenolic contents of tomato using conventional and ecological horticultural practices, and arbuscular mycorrhizal fungi (AMF). Agron Colomb 26(1): 40-46
  27. Wang Y, Zhang W, Liu W, Ahammed GJ, Wen W, Guo S, Sun J (2021) Auxin is involved in arbuscular mycorrhizal fungi- promoted tomato growth and NADP-malic enzymes expression in continuous cropping substrates. BMC Plant Biology 21(1): doi:10.1186/s12870-020-02817-2
    Pubmed KoreaMed CrossRef
  28. Zhao YY, Cartabia A, Lalaymia I, Declerck S (2022) Arbuscular mycorrhizal fungi and production of secondary metabolites in medicinal plants. Mycorrhiza 32:221-256
    Pubmed KoreaMed CrossRef
  29. Ziane H, Meddad-Hamza A, Beddiar A, Gianinazzi S (2017) Effects of arbuscular mycorrhizal fungi and fertilization levels on industrial tomato growth and production. Int J Agric Biol 19:341-347. https://doi.org/10.17957/IJAB/15.0287
    CrossRef

Article

Research Article

J Plant Biotechnol 2023; 50(1): 239-247

Published online December 11, 2023 https://doi.org/10.5010/JPB.2023.50.030.239

Copyright © The Korean Society of Plant Biotechnology.

Effects of arbuscular mycorrhizal fungi on enhancing growth, fruit quality, and functional substances in tomato fruits (Lycopersicon esculentum Mill.)

Thanapat Suebrasri・Wasan Seemakram・Chanon Lapjit・Wiyada Mongkolthanaruk・Sophon Boonlue

Faculty of Allied Health Sciences, Nakhon Ratchasima College, Nakhon Ratchasima, 30000, Thailand
Department of Microbiology, Faculty of Science, Khon Kaen University, Khon Kaen, 40002, Thailand
Department of Horticulture, Faculty of Agriculture, Khon Kaen University, Khon Kaen, 40002, Thailand

Correspondence to:e-mail: bsopho@kku.ac.th

Received: 4 October 2023; Revised: 21 October 2023; Accepted: 21 October 2023

This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

This study aimed to investigate the efficiency of arbuscular mycorrhizal fungi (AMF) in enhancing plant performance and bioactive compound concentrations in tomatoes (Lycopersicon esculentum Mill.). This factorial pot experiment included nine replications over 120 days of cultivation. Three AMF species (Rhizophagus prolifer, Claroideoglomus etunicatum, and Acaulospora mellea) were utilized as inoculum, while non-mycorrhizal controls with or without synthetic NPK fertilizer were compared. Interestingly, C. etunicatum KS-02 inoculations effectuated the best fruit growth and weight, which were statistically higher than those of the control without AMF. However, only fruit fresh weight was higher in plants inoculated with C. etunicatum KS-02 than those treated with the synthetic NPK fertilizer. In addition, C. etunicatum KS-02 inoculations induced a ≥ 11% increase in DDPH (1,1-diphenyl-2-picrylhydrazyl) activity, lycopene content, and carotenoid content compared to the control. This study is the first to report Claroideoglomus species’ effectiveness in promoting growth, fruit yield, and bioactive compound production in L. esculentum Mill. These findings substantiate the significant potential of C. etunicatum KS-02 for tomato cultivation without the adverse effects of excessive synthetic fertilizer use.

Keywords: Antioxidants, Carotenoids, Lycopene, Phytochemical, Tomato production

Introduction

Tomato (Lycopersicon esculentum Mill.) is the second most important fruits and vegetable crop in the world, next to the potatoes. Ripe fruits are small, sweet and crispy in taste. They are commonly consumed as fresh fruit or can be eaten with salads. The fruits are rich in antioxidants such as carotenoids and vitamin C, with lycopene representing the main carotenoid, accounting for 80% of all carotenoids (Nguyen and Schwartz 1999). The fruits can be processed in a variety of industries to create products such as ketchup and tomato juice or used as an ingredient in some food condiments. This has resulted in a high demand value of up to 16 million tons per year. There is 6,328.8 hectare of tomato cultivation area in Thailand, most of this area being located in northeastern Thailand. The total yield in 2020 was 132,650 tons. However, tomato production in this area experiences many problems, including disease, insects or unacceptable weather conditions such as high temperatures, drought and low nutrient content in the soil. These factors result in lower yield and a poorer fruit quality of tomatoes (Lahoz et al. 2016). In light of this, a great deal of focus has fallen on new approaches to improve plant growth and increase specific substance content. At present synthetic fertilizer is commonly utilized to boost plant production (Seemakram et al. 2022). However, over long-term use, these synthetic fertilizers have been found to decrease soil quality with a notable reduction in beneficial soil microbes and evidence of toxic residues (Chandini et al. 2019). One way to lessen agriculture’s dependency on synthetic fertilizers is through the use of plant-growth-promoting microorganisms (PGPM), which are a focus of interest and study because of their environmentally friendly nature (Andre et al. 2016; Seemakram et al. 2022).

Soil fertility has been declining as a result of cultivation for a long time. Thus, there is an evident need for cultivation management by other means, particularly with the soil biota, which facilitates improved growth performance of tomato fruit. Arbuscular mycorrhizal fungi (AMF), a soil biota belonging to the Division Glomeromycota, offers great potential. It involves a process of fungal symbiosis that colonizes the roots of over 80% of land plants (Boonlue et al. 2012) AMF symbiosis can be observed in nearly all ecosystems and occurs naturally in most plant species. One of the effects of this symbiotic relationship is to increase nutrient uptake from the soil for nutrients such as phosphorus (P), nitrogen (N) and potassium (K), and micronutrients that help for enhancing plant growth (Jeffries 1987). AMF also aids plant growth under adverse environmental conditions, such as aridity, and help prevent diseases in the root system (Seemakram et al. 2021). Moreover, AMF serves to help plants adjust the osmotic balance within their cells (Nacoon et al. 2021), and strengthen plant tolerance to stresses, such as salinity and heavy-metal pollution (Salam et al. 2017). Owing to the above benefits, some species of arbuscular mycorrhizal are of interest for utilization in bio-fertilizers to replace chemical fertilizers, etc.

Therefore, our principle objective was to investigate the role various species of AMF played on the growth performance, and the lycopene, carotenoid, and 1,1-diphenyl-2-picryl-hydrazyl (DPPH) content of the fruit of Lycopersicon esculentum Mill. varieties T72011. AMF treatment of the species was compared with two controls (without AMF inoculation and with chemical fertilizer treatment); a treatment with existing fertile soil and one with the addition of mineral fertilizer. However, there are currently no reports investigating the effects of AMF on the growth and combined production of secondary metabolites in tomatoes. The results obtained in this research could provide a framework for an in-situ application of AMF to increase tomato cultivation in Thailand. Mycorrhizal management offers economic benefits as an alternative to purchasing mineral fertilizer; therefore, this study offers potential options for the agricultural sector to decrease expenses and boost income.

Materials and Methods

AMF preparation

The AMF species, Rhizophagus prolifer PC2-2 (Seemakram et al. 2021, 2022), Claroideoglomus etunicatum KS-02 (Nacoon et al. 2023) and Acaulospora mellea KKU-NBP-SB-2 (Khaekhum et al. 2017), were obtained from Mycorrhiza and Mycotechnology Laboratory and used as the fungal inoculum. The maize was used as the host plant for production of AMF spore following the methods of Boonlue et al. (2012). Soil was sterilized twice then placed in 8-inch-diameter plastic pots for use as a plant substrate. Surface sterilization of maize seed was performed by soaking in 6% sodium hypochlorite solution for 30 min. Around 200 AMF spores were added to the pots containing sterile maize seeds, before the maize was cultivated in a greenhouse at a temperature of 30-35°C with daily irrigation until 90 days, when watering ceased and the plants began to dry. The plants were cut just above the soil surface. Finally, soil samples were first dried and then crushed into finely ground particles. The purity of the spores and the total spore number were determined using the sucrose centrifugation method (Daniels and Skipper 1982). These dried soils containing AMF spores, mycelia and infected roots were then used as the inoculum in the experiments.

Soil preparation

The sandy loam soil properties include pH, electrical conductivity (EC), organic matter (OM), nitrogen (N), phosphorus (P), potassium (K), available phosphorus, exchangeable potassium, calcium (Ca), and sodium (Na) were analyzed according to the method described by Seemakram et al (2021). The soil samples were sterilized and stored overnight at room temperature, before being sterilized again under the same conditions, then packed in 6-inch diameter plastic pots; each pot contained 3 kg.

Tomato seed preparation

Tomato cultivars of Lycopersicon esculentum Mill. varieties T72011 were obtained by Asist. Prof. Dr. Chanon Lapjit, Faculty of Agriculture, Khon Kaen University, Thailand from the Horticultural station, Khon Kaen University, which develops and distributes them. The tomato seeds were sterilized with 6% sodium hypochlorite for 5 min, before being rinsed with sterile distilled water for 3 min. The sterilized seeds were placed in sterilized Petri dishes for 5 to 7 days, where root germination was observed. The seedlings were cultivated in peatmoss-filled trays for 2 weeks, after which the mature seedlings (of around 10cm in height) were transferred to plastic pots.

Experimental design and treatment

The pot experiment was carried out in a greenhouse at the Faculty of Science, Khon Kaen University, Thailand. The experimental design was conducted with a factorial completely randomized design (CRD) with 5 treatments in 6 replications as follows: (T1) control, sterilized soil without AMF; (T2) control with mineral fertilizer, sterilized soil without AMF with the addition of mineral nutrients (N,P,K: 15-15-15) at 0.32 g per pot; (T3) inoculation with R. prolifer PC2-2; (T4) inoculation with A. mellea KKU-NBP-SB-2; and (T5) inoculation with C. etunicatum KS-02. The AMF inoculum was applied adjacent to the plant root at a rate of approximately 200 spores/pot. After 3 months the plants were harvested.

Mycorrhizal root colonization

Mycorrhizal root colonization intensity was determined according to the method described by Koske and Gemma (1989). Roots were washed with 10% KOH for 3 min at 95°C, and then soaked in 2% HCl overnight. Trypan blue solution (0.05%) was used to stain root samples, which were then cut into 1 cm long pieces. The cellular structures of AMF, including vesicles, arbuscules, and hyphae, were observed using a microscope at 40 × magnification (SMZ745T Nikon, Japan) (Seemakram et al. 2022).

Determination of plant growth parameters

After 90 days of transplantation, the parameters of plant growth including plant height, stem diameter, SPAD and leaf area (Arnon 1949) were evaluated. The number and fresh weight of fruit were analyzed at harvest. Leaves, stem and roots were dried in an oven at 80°C for 3 days prior to analysis, and the dry weight measured to record plant biomass. The nutrient uptake concentration (N, P and K) of the samples was next determined. The parameters determining the quality of the plant roots, including the diameter, specific root length (SRL) and root tissue density (RTD), were measured by scanning the root samples using an Epson scanner V800 PHOTO, and the data were analyzed using WINRHIZO Pro2004a software (REGENT Instruments Inc., Quebec, QC, Canada).

Lycopene and Carotenoid content measurement

Fruit samples were cut and blended using a blender. Then, the samples were kept on ice in dark conditions. The sample of 0.2 g was transferred to a 50 mL covered test tube. A total of 20 mL of hexane: acetone: ethanol (HAE) of 2:1:1 (v/v/v) was added to the sample tubes. After that, the samples were mixed for 10 min and 3 mL of distilled water was added to each sample tube. The samples were agitated for several minutes. Then, the samples were kept at room temperature. The supernatant of the hexane layer that contained lycopene and carotenoid was measured using a spectrophotometer at the wavelengths of 503 and 449 nm, respectively. The lycopene and carotenoid contents were calculated according to the formula described by Biswas et al. (2011) and Fester et al. (2002)

Antioxidant content measurement

Free-radical-scavenging activity of 1,1-diphenyl-2-picryl-hydrazyl (DPPH) was detected modifying to the method described by Leong and Shui (2002). A freshly 0.1 mM solution of DPPH in methanol was prepared. A 100 µL of each sample (with appropriate dilution) was first mixed with 4.0 mL of DPPH solution, before holding at room temperature for 30 min prior to measurement. The mixture solution was measured at 517 nm and detected by spectrophotometer. Methanol (0.5 mL), replacing the sample, was used as the blank. The percentage of radical-scavenging ability was analyzed by using the following formula:

Scavenging ability (%) = (Absorbance 517 nm of control - Absorbance 517 nm of sample) / Absorbance 517 nm of control × 100

Statistical analysis

All data from this work were evaluated by analysis of variance (ANOVA) for data from the factorial CRD. Fisher’s least significant difference (LSD) was significant at p ≤ 0.05. The correlation between data was analyzed using Statistix 10 software.

Results

Mycorrhizal colonization

The quantity of AMF spores and root colonization in Lycopersicon esculentum Mill. was measured and is reported in Table 1. In addition, AMF was found in the plant roots, such as hyphae, vesicles and arbuscules, in various structures. In the treatment without AMF (treatments T1 and T2), spores in the soils and tomato root colonization were not detected.

Table 1 . AMF spores in soil and AMF colonization in tomato roots.

TreatmentSpore/gram soilRoot colonization (%)
T10.00c0.00c
T20.00c0.00c
T32.68b20.19ab
T410.29ab28.23a
T521.14a29.01a
% cv.11.3628.09
F-test*n.s.

Numbers followed by the same letters in each column indicate values that were not significantly different according to the LSD test. * significant difference at p ≤ 0.05, ** significant difference at p ≤ 0.01. T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s, not significant..



Effects of AMF on plant growth parameters

The ability of AMF to enhance plant growth was detected with respect to plant height, leaf greenness, diameter, leaf area, stem dry weight, leaf dry weight and root dry weight. In addition, the plant yield, including the number of fruits and the fruit fresh weight, was also evaluated (Table 2). The presence of AMF was found to increase all of the plant growth parameters in comparison to the control plant (T1). All of the plant growth parameters and yields in these treatments were significantly increased when compared to the control plant treatment. In the case of tomato inoculated with C. etunicatum KS-02 treatment, all plant growth parameters were found to be statistically higher than those of the control without AMF. Moreover, the highest yield or fruit fresh weight was also found in the C. etunicatum KS-02 treatment (T5). Therefore, the best AMF treatment for enhancing the growth of tomato was demonstrated to be C. etunicatum KS-02 (T5).

Table 2 . Effects of AMF on tomato growth.

TreatmentSPADHeight (cm)Diameter (cm)Leaf area (cm2)Total number of fruitsFruit fresh weight (g)Stem dry weight (g)Leaf dry weight (g)
T130.25b68.80b13.01b15.09c5b10.16c3.92b1.96a
T245.32a76.50ab16.90a30.78a10a18.38b7.62a2.18a
T340.18a68.50b15.10ab25.75ab8ab24.16ab5.56b2.32a
T438.06a74.50ab13.70b20.02b11a25.17ab6.61ab2.18a
T539.27a78.60a16.70a29.35a10a40.70a7.64a2.67a
% cv.20.1825.0124.5027.5224.3129.0727.0925.67
F-test**********n.s.

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant..



Table 3 shows the plant root growth performance of the tomato plants grown under different conditions. The results indicate that most of the root traits were significantly improved by inoculation with either AMF compared to control plant (T1). Nevertheless, the root dry weight and specific root length of the plants inoculated with A. mellea KKU-NBP-SB-2 (T4) and with C. etunicatum KS-02 (T5) were significantly higher than those of the control plant (T1).

Table 3 . Effects of AMF on tomato root growth.

TreatmentRoot dry weight (g)Average diameter (mm)Specific root length (m g-1)Root tissue density (g cm-3)
T10.91ab0.28a107.95b94.02a
T21.23a0.30a113.31ab78.03ab
T30.88b0.29a113.18ab83.60ab
T41.09ab0.28a124.11ab81.78ab
T51.24a0.28a149.93a67.69b
% cv.21.3628.0925.7124.02
F-test*n.s.**

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant..



Effects of AMF on N, P and K contents

The effects of AMF on NPK concentration in tomato plants are indicated in Table 4. The tomato plants to which chemical fertilizer had been applied showed the maximum value of N,P. Among the AMF-inoculated treatments, N accumulation in the plants was increased but no significant difference was found with the non-inoculated control. The concentration of P in tomato plant inoculated with AMF was not statistically higher than that of the control treatment. However, the highest phosphorus content was detected in the tomato inoculation with R. prolifer PC2-2. The concentration of potassium (K) was found to be statistically higher in all treatments inoculated with AMF than in the control. In the tomato plants inoculated with C. etunicatum KS-02, the highest K concentration was found. These results reveal that AMF enhanced mineral (N, P and K) contents in tomato plants, and particularly K, compared with the non-inoculated control.

Table 4 . Effects of AMF on nitrogen, phosphorus, and potassium concentrations in tomatoes.

TreatmentN concentration (mg g-1)P concentration (mg g-1)K concentration (mg g-1)
T116.6b10.2b10.9b
T221.2a23.3a13.7ab
T317.5ab15.1ab15.7a
T416.9b10.1b14.4ab
T519.9ab13.8b15.9a
% cv.29.0925.8327.42
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; N, Nitrogen; P, Phosphorus; K, Potassium..



Effects of AMF on antioxidant activity, lycopene content and carotenoid content

Fruit lycopene content, carotenoid content and antioxidant activity increased with all of the AMF treatments compared to the control treatment without fertilizer, and no significant difference was found with chemical fertilizer treatment. The maximum antioxidant activity (97.29%), lycopene content (0.62 µg/g) and carotenoid content (3.22 µg/g) were found in the C. etunicatum KS-02 treatment, which showed a significant difference from the non-inoculated control (Table 5). In addition, this finding was not significantly different to chemical fertilizer treatment. Therefore, the best performance in terms of fruit lycopene content, carotenoid content and antioxidant activity was found in the treatment of the plant inoculated with C. etunicatum KS-02, which might be used instead of chemical fertilizer.

Table 5 . Effect of AMF on antioxidant activity, lycopene content, and carotenoid content in tomatoes.

TreatmentDPPH (%)Lycopene (µg/g)Carotenoid (µg/g)
T187.14b0.42b2.37b
T296.26a0.52ab3.38a
T396.23a0.49b3.26a
T495.61a0.59ab3.16a
T597.29a0.62a3.22a
% cv.27.0925.7125.32
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi..



Correlations between AMF, % colonization, nutrient uptake and the concentration of secondary compounds and the plant growth parameters of tomato at the harvest stage are shown in Table 6. Mycorrhizal colonization and root dry weight significantly positively correlated with the number of fruit, fruit fresh weight, antioxidant activity, lycopene content and K concentration of the plant. Among the AMF treatments, C. etunicatum KS-02 was significantly positively correlated with fruit fresh weight, antioxidant activity, lycopene content and the K concentration of the plant. The number of fruit and fruit fresh weight were significantly positively correlated with DPPH activity, lycopene content and carotenoid content, and the K concentration of the plant. Additionally, DPPH activity, lycopene content and carotenoid content were significantly positively correlated with the K concentration of the plant.

Table 6 . Correlation between AMF, nutrient uptake, antioxidants, lycopene, and carotenoids in tomatoes.

CorrelationCFAMF1AMF2AMF3Root colonizationNo. of sporesRoot dry weightNo. of fruitFruit fresh weightDPPHLycopeneCarotenoidsNP
Root colonization-0.59**0.18 ns0.48*0.51*
No. of spores-0.42 ns-0.25 ns0.21 ns0.88**0.81**
Root dry weight0.52*-0.62**0.06 ns0.55*0.16 ns0.53*
No. of fruit0.28 ns-0.18 ns0.51*0.28 ns0.58*0.53*0.73**
Fruit fresh weight-0.26 ns0.02 ns0.07 ns0.84**0.83**0.92**0.54*0.63**
DPPH0.23 ns0.23 ns0.14 ns0.37 ns0.60**0.49*0.57*0.86**0.75**
Lycopene0.10 ns-0.01 ns0.36 ns0.47*0.73**0.68**0.67**0.94**0.82**0.94**
Carotenoids0.41 ns0.25 ns0.11 ns0.19 ns0.43 ns0.29 ns0.55*0.84**0.58*0.97**0.87**
N0.76**-0.25 ns-0.41ns0.40 ns-0.15 ns0.18 ns0.81**0.48 ns0.35 ns0.56*0.47*0.62**
P0.91**0.06 ns-0.45**-0.07 ns-0.42 ns-0.29 ns0.48 ns0.30 ns-0.02 ns0.46 ns0.24 ns0.61**0.85**
K-0.11 ns0.43 ns0.07 ns0.49*0.77**0.61**0.33 ns0.68**0.85**0.92**0.86**0.83**0.33 ns0.19 ns

**, significant difference at p ≤ 0.01; *, significant difference at p ≤ 0.05; ns, not significant. R. prolifer PC2-2 (AMF1), A. mellea KKU-NBP-SB-2 (AMF2); and C. etunicatum KS-02 (AMF3).


Discussion

According to our previous studies, the species of AMF showed high efficiency in enhancing plant growth and biomass in perennial plants belonging to the legume family (Siamese rosewood and Burma padauk) (Seemakram et al. 2021) and cannabis (Seemakram et al. 2022). Therefore, we expected inoculation with AMF to play a key role in boosting the growth and production of secondary metabolites in tomato. The efficiency of three AMF species, namely R. prolifer PC2-2, C. etunicatum KS-02 and A. mellea KKU-NBP-SB-2, was investigated for its capacity to promote the growth and production of secondary metabolites of tomato (L. esculentum Mill.), compared with the effect of the application of synthetic NPK fertilizer under greenhouse conditions. Claroideoglomus etunicatum KS-02 showed a higher root colonization than that of A. mellea KKU-NBP-SB-2 (28.23%) and R. prolifer PC2-2 (20.19%). A study using concentrations of C. etunicatum up to 51% (Ziane et al. 2017) observed higher root colonization in tomato roots compared with our findings. The data from our study is similar to the value of the mycorrhizal colonization of black rice (Maled Phai and Niew Dam Hmong) of 25, and the value of 9% reported by Nacoon et al. (2023).

This study identified that colonization with AMF affected growth performance of tomato cultivars and the production of secondary metabolites of tomato fruits beneficially under greenhouse conditions. Treatment with C. etunicatum KS-02 significantly affected the SPAD value, height, diameter, leaf area and biomass of the tomato plant. Our data show similar results to those of Ziane et al. (2017), who reported that the overall height and biomass of tomato inoculated with the commercial AMF inoculum were significantly increased. Mutumba et al. (2018) documented the effect of mycorrhizal fungi on improving the plant growth parameters and chlorophyll index of the host plant. In addition, our results concur with those in previous literature using other plant species. Inoculation with R. prolifer PC2-2 in Siamese rosewood, Burma padauk and cannabis resulted in an increase in the leaf area and biomass (Seemakram et al. 2021). Moreover, black rice inoculated with C. etunicatum outperformed non-inoculated plants in the absence of mineral fertilizer in terms of biomass (Nacoon et al. 2023). Mineral fertilizer boosted plant performance when applied, but the effect was non-significant in terms of biomass. The symbiotic relationship between AMF and host plants enhances plant growth and biomass, and enables the plant to resist abiotic stress conditions (Alam et al. 2023). Furthermore, AMF inoculation significantly affected the number of tomato fruits yielded and fruit fresh weight. Consistent with previous studies, the incorporation of inoculated Funneliformis mosseae into the continuous cropping substrate remarkably improved the growth and yield of tomatoes, and resulted in a slender rise in fruit size in tomato production (Wang et al. 2021). The above results affirm that AMF inoculation resulted in greater fruit numbers regardless of the fertilization criterion in tomato.

As may be expected, for the roots of tomato plants colonized by AMF in all treatments, the root qualities were affected. However, the root dry weight and specific root length after treatment with C. etunicatum KS-02 were significantly higher than those of non-inoculated plants. This may have resulted from the introduction of AMF, leading to more effective root colonization, which affected the root qualities, especially root dry weights, which were significantly greater in inoculated plants compared to non-inoculated plants (Ziane et al. 2017). These results suggest that the inoculation of AMF had an effect on specific root traits, but not all of them (Seemakram et al., 2022). Furthermore, plants inoculated with C. etunicatum KS-02 exhibited slightly higher N, P and K concentrations. This is perhaps due to mycorrhizal plants exploring a greater volume of soil for available nutrients and water than uninoculated ones, leading to the recorded increase in N, P and K (Evelin et al. 2012). However, considering nutrient concentration among the tomato plants, all plants inoculated with AMF demonstrated a value of K which was significantly higher than that of the uninoculated plant.

Both inoculation with AMF and synthetic fertilizer served to increase the performance of tomato and increased the capacity of the DPPH, lycopene content and carotenoid content compared to the unfertilized control. The maximum DDPH activity and lycopene and carotenoid contents for the C. etunicatum KS-02 treatment were found to be higher than those seen in the non-inoculated control treatment. A positive correlation was found between K uptake and an increase in DPPH activity, in addition to lycopene and carotenoid content. Moreover, inoculation with C. etunicatum KS-02 in tomato cultivation showed a positive correlation between lycopene and K uptake. Lycopene is one of the precursors of carotenoid synthesis, formed through the cyclization of lycopene, which has a positive correlation with K (Heldt 2003; Taber 2006). In addition, root colonization and root dry weight exhibited positive correlations with the number of fruit and fruit fresh weight, resulting in increased lycopene and carotenoid accumulation in the fruit. Our data are similar to those of Ordookhani et al. (2010), who reported that a positive correlation between lycopene and shoot potassium was found in plants treated with PGPR. Stimulation of the carotenoid metabolism was correlated with the root colonization of AMF (Fester et al. 2002). AMF colonization activated plant defense mechanisms producing of phenolics and flavonoids (Zhao et al. 2022). Avio et al. (2017) reported that R. irregulare IMA6 increased the phenolics concentration and antioxidant activity in tomato plants. In general, tomato cultivation with AMF led to increased carotenoid and total phenolic contents, while AMF inoculation also increased lycopene content in cultivated tomatoes (Ulrichs et al. 2008). In previous work reported that the increase in functional substances in plants was correlated with increases in phosphorus acquisition (Seemakram et al. 2022). Our results contradict those from previous studies, which partly supported the nutritional mechanism of tomato, indicated by the correlations between AMF and K concentration with an increase in antioxidant activity, lycopene content and carotenoid content.

Our study shows that using AMF obtained a similar result in terms of plant growth performance, tomato yield and functional compounds in tomato fruit compared with the application of chemical fertilizer; inoculation with C. etunicatum KS-02 was particularly successful. Further, high levels of antioxidant compounds, such as lycopene and carotenoids, in tomato fruit may boost market price, especially where the tomato plant is cultivated organically (Pataro et al., 2020). Nevertheless, the use of AMF alone had substantial benefits regarding plant growth and quality and functional compounds in tomato fruit. As highlighted above, the use of chemical fertilizers enhanced some physical plant characteristics more rapidly than with the use of AMF. Best practice for agribusiness would be utilizing chemical fertilizers in combination with biological techniques in order to achieve the highest efficiency in the production of tomato yield and to maximize the quality of fruit with a high content of functional compounds, while minimizing environmental damage. In this regard, the inoculation of C. etunicatum KS-02 could, with careful management, help farmers to reduce the production costs of tomato cultivation by providing a partial or complete alternative to chemical fertilizer. The combined use of AMF and fertilizer application, including organic soil management, is the main target that warrants further investigation.

Conclusions

Our study demonstrates the effect of AMF inoculation on the growth promotion, yield and bioactive compound production of tomato (L. esculentum Mill.), showing no significant difference from chemical fertilizer application. AMF treatment also led to significant correlations between mycorrhizal colonization, fruit weight, fruit number, concentration of K and bioactive compound content. We found that Claroideoglomus etunicatum KS-02 was the best plant growth promoter, being able to promote growth, fruit yield, antioxidant capacity, lycopene and carotenoids in tomato compared with non-inoculated plants under unfertilized conditions. This species warrants further analysis as a means to developing an AMF inoculum alternative for the industrial production of tomato, replacing the immoderate application of synthetic fertilizer which characterizes current conventional practices.

Funding

This work was supported by the Fundamental Fund of Khon Kaen University in FY 2022, grant no. FRB650032/0161, which received funding support from the National Science, Research and Innovation Fund (NSRF).

Acknowledgement

This research was supported by the Fundamental Fund of Khon Kaen University in FY 2022, grant no. FRB650032/0161, through the research on growth enhancement and carotenoid accumulation in tomato fruit by arbuscular mycorrhizal fungi by Khon Kaen University, Department of Microbiology, Faculty of Science, which received funding support from the National Science, Research and Innovation Fund (NSRF).

Table 1 . AMF spores in soil and AMF colonization in tomato roots.

TreatmentSpore/gram soilRoot colonization (%)
T10.00c0.00c
T20.00c0.00c
T32.68b20.19ab
T410.29ab28.23a
T521.14a29.01a
% cv.11.3628.09
F-test*n.s.

Numbers followed by the same letters in each column indicate values that were not significantly different according to the LSD test. * significant difference at p ≤ 0.05, ** significant difference at p ≤ 0.01. T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s, not significant..


Table 2 . Effects of AMF on tomato growth.

TreatmentSPADHeight (cm)Diameter (cm)Leaf area (cm2)Total number of fruitsFruit fresh weight (g)Stem dry weight (g)Leaf dry weight (g)
T130.25b68.80b13.01b15.09c5b10.16c3.92b1.96a
T245.32a76.50ab16.90a30.78a10a18.38b7.62a2.18a
T340.18a68.50b15.10ab25.75ab8ab24.16ab5.56b2.32a
T438.06a74.50ab13.70b20.02b11a25.17ab6.61ab2.18a
T539.27a78.60a16.70a29.35a10a40.70a7.64a2.67a
% cv.20.1825.0124.5027.5224.3129.0727.0925.67
F-test**********n.s.

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant..


Table 3 . Effects of AMF on tomato root growth.

TreatmentRoot dry weight (g)Average diameter (mm)Specific root length (m g-1)Root tissue density (g cm-3)
T10.91ab0.28a107.95b94.02a
T21.23a0.30a113.31ab78.03ab
T30.88b0.29a113.18ab83.60ab
T41.09ab0.28a124.11ab81.78ab
T51.24a0.28a149.93a67.69b
% cv.21.3628.0925.7124.02
F-test*n.s.**

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; n.s., not significant..


Table 4 . Effects of AMF on nitrogen, phosphorus, and potassium concentrations in tomatoes.

TreatmentN concentration (mg g-1)P concentration (mg g-1)K concentration (mg g-1)
T116.6b10.2b10.9b
T221.2a23.3a13.7ab
T317.5ab15.1ab15.7a
T416.9b10.1b14.4ab
T519.9ab13.8b15.9a
% cv.29.0925.8327.42
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi; N, Nitrogen; P, Phosphorus; K, Potassium..


Table 5 . Effect of AMF on antioxidant activity, lycopene content, and carotenoid content in tomatoes.

TreatmentDPPH (%)Lycopene (µg/g)Carotenoid (µg/g)
T187.14b0.42b2.37b
T296.26a0.52ab3.38a
T396.23a0.49b3.26a
T495.61a0.59ab3.16a
T597.29a0.62a3.22a
% cv.27.0925.7125.32
F-test***

T1: control without AMF inoculum; T2: chemical fertilizer; T3: Rhizophagus prolifer PC2-2; T4: Acaulospora mellea KKU-NBP-SB-2; T5: Claroideoglomus etunicatum KS-02. AMF, Arbuscular mycorrhizal fungi..


Table 6 . Correlation between AMF, nutrient uptake, antioxidants, lycopene, and carotenoids in tomatoes.

CorrelationCFAMF1AMF2AMF3Root colonizationNo. of sporesRoot dry weightNo. of fruitFruit fresh weightDPPHLycopeneCarotenoidsNP
Root colonization-0.59**0.18 ns0.48*0.51*
No. of spores-0.42 ns-0.25 ns0.21 ns0.88**0.81**
Root dry weight0.52*-0.62**0.06 ns0.55*0.16 ns0.53*
No. of fruit0.28 ns-0.18 ns0.51*0.28 ns0.58*0.53*0.73**
Fruit fresh weight-0.26 ns0.02 ns0.07 ns0.84**0.83**0.92**0.54*0.63**
DPPH0.23 ns0.23 ns0.14 ns0.37 ns0.60**0.49*0.57*0.86**0.75**
Lycopene0.10 ns-0.01 ns0.36 ns0.47*0.73**0.68**0.67**0.94**0.82**0.94**
Carotenoids0.41 ns0.25 ns0.11 ns0.19 ns0.43 ns0.29 ns0.55*0.84**0.58*0.97**0.87**
N0.76**-0.25 ns-0.41ns0.40 ns-0.15 ns0.18 ns0.81**0.48 ns0.35 ns0.56*0.47*0.62**
P0.91**0.06 ns-0.45**-0.07 ns-0.42 ns-0.29 ns0.48 ns0.30 ns-0.02 ns0.46 ns0.24 ns0.61**0.85**
K-0.11 ns0.43 ns0.07 ns0.49*0.77**0.61**0.33 ns0.68**0.85**0.92**0.86**0.83**0.33 ns0.19 ns

**, significant difference at p ≤ 0.01; *, significant difference at p ≤ 0.05; ns, not significant. R. prolifer PC2-2 (AMF1), A. mellea KKU-NBP-SB-2 (AMF2); and C. etunicatum KS-02 (AMF3).


References

  1. Alam MZ, Choudhury TR, Mridha MAU (2023) Arbuscular mycorrhizal fungi enhance biomass growth, mineral content, and antioxidant activity in tomato plants under drought stress. J Food Qual 2023:2581608. https://doi.org/10.1155/2023/2581608
    CrossRef
  2. Andre CM, Hausman JF, Guerriero G (2016) Cannabis sativa: The plant of the thousand and one molecules. Front Plant Sci 7:19. https://doi.org/10.3389/fpls.2016.00019
    Pubmed KoreaMed CrossRef
  3. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1-15. http://doi.org/10.1104/pp.24.1.1
    Pubmed KoreaMed CrossRef
  4. Avio L, Sbrana C, Giovannetti M, Frassinetti S (2017) Arbuscular mycorrhizal fungi affect total phenolics content and antioxidant activity in leaves of oak leaf lettuce varieties. Sci Hortic 224:265-271. https://doi.org/10.1016/j.scienta.2017.06.022
    CrossRef
  5. Biswas AK, Sahoo J, Chatli MK (2011) A simple UV-Vis spectrophotometric method for determination of β-carotene content in raw carrot, sweet potato and supplemented chicken meat nuggets. LWT - Food Sci Technol 44: 1809-1813
    CrossRef
  6. Boonlue S, Surapat W, Pukahuta C, Suwanarit P, Suwanarit A, Morinaga T (2012) Diversity and efficiency arbuscular mycorrhizal fungi in soils from organic chili (Capsicum frutescens L.) farms. Mycoscience 53:10-16
    CrossRef
  7. Chandini, Kumar R, Kumar R, Prakash O (2019) The impact of chemical fertilizers on our environment and ecosystem. In: Research Trends in Environmental Sciences (2nd ed.). New Delhi, India (pp 71-86)
  8. Daniels BA, Skipper HD (1982) Method for the recovery and quantitative estimation of propagules from soil. In: Schenck, N.C. (Ed.), Method and Principle of Mycorrhizal Research. Am. Phytopathol. Soc., St. Paul Minnesota, USA (pp 29-36)
  9. Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203-217
    Pubmed CrossRef
  10. Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216(1):148-54
    Pubmed CrossRef
  11. Heldt HW (2003) Pflanzenbiochemie. 3. Auflage. Spektrum Akademischer Verlag, Heidelberg. p 622
  12. Khaekhum S, Lumyong S, Kuyper TW, Boonlue S (2017) Species richness and composition of arbuscular mycorrhizal fungi occurring on eucalypt trees (Eucalyptus camaldulensis Dehnh.) in rainy and dry season. Curr Res Environ Appl Mycol 7(4): 282-292. https://doi.org/10.5943/cream/7/4/5
    CrossRef
  13. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486-505. https://doi.org/10.1016/S0953-7562(89)80195-9
    CrossRef
  14. Lahoz I, Pérez-de-Castro A, Valcárcel M, Macua JI, Beltrán J, Roselló S, Cebolla-Cornejo J (2016) Effect of water deficit on the agronomical performance and quality of processing tomato. Scientia Horticulturae 200:55-65. https://doi.org/10.1016/j.scienta.2015.12.051
    CrossRef
  15. Leong LP, Shui G (2002) An Investigation of antioxidant capacity of fruits in Singapore markets. Food Chem 76:69-75. https://doi.org/10.1016/S0308-8146(01)00251-5
    CrossRef
  16. Mutumba FA, Zagal E, Gerding M, Castillo-Rosales D, Paulino L, Schoebitz M (2018) Plant growth promoting rhizobacteria for improved water stress tolerance in wheat genotypes. J Soil Sci Plant Nutr 18(4):1080-1096. https://doi.org/10.4067/S0718-95162018005003003
    CrossRef
  17. Nacoon S, Ekprasert J, Riddech N, Mongkolthanaruk W, Jogloy S, Vorasoot N, Cooper J, Boonlue S (2021) Growth enhancement of sunchoke by arbuscular mycorrhizal fungi under drought condition. Rhizosphere 17:100308. https://doi.org/10.1016/j.rhisph.2021.100308
    CrossRef
  18. Nacoon S, Seemakram W, Ekprasert J, Theerakulpisut P, Sanitchon J, Kuyper TW, Boonlue S (2023) Arbuscular mycorrhizal fungi enhance growth and increase concentrations of anthocyanin, phenolic compounds, and antioxidant activity of Black Rice (Oryza sativa L.). Soil Syst 7:44. https://doi.org/10.3390/soilsystems7020044
    CrossRef
  19. Nguyen ML, Schwartz SJ (1999) Lycopene: chemical and biological properties. Food Technol 53:38-45
  20. Ordookhani K, Khavazi K, Moezzi A, Rejali F (2010) Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr J Agric Res 5(10):1108- 1116
  21. Pataro G, Carullo D, Falcone M, Ferrari G (2020) Recovery of lycopene from industrially derived tomato processing by-products by pulsed electric fields-assisted extraction. Innov Food Sci Emerg Technol 63. https://doi.org/10.1016/j.ifset.2020.102369
    CrossRef
  22. Salam EA, Alatar A, El-Sheikh MA (2017) Inoculation with arbuscular mycorrhizal fungi alleviates harmful effects of drought stress on damask rose. Saudi J Biol Sci 25:1772-1780. https://doi.org/10.1016/j.sjbs.2017.10.015
    Pubmed KoreaMed CrossRef
  23. Seemakram W, Paluka J, Suebrasri T, Lapjit C, Kanokmedhakul S, Kuyper TW, Ekprasert J, Boonlue S (2022) Enhancement of growth and Cannabinoids content of hemp (Cannabis sativa) using arbuscular mycorrhizal fungi. Front Plant Sci 13: 845794.https://doi.org/10.3389/fpls.2022.845794
    Pubmed KoreaMed CrossRef
  24. Seemakram W, Suebrasri T, Khaekhum S, Ekprasert J, Aimi A, Boonlue S (2021) Growth enhancement of the highly prized tropical trees siamese rosewood and burma padauk. Rhizosphere 19:100363. https://doi.org/10.1016/j.rhisph.2021.100363
    CrossRef
  25. Taber HG (2006) Potassium application and leaf sufficiency level for fresh-market tomatoes on a Midwestern United States fine-textured soil. HortTechnology 16:247-252
    CrossRef
  26. Ulrichs C, Fischer G, Büttner C, Mewis I (2008) Comparison of lycopene, b-carotene and phenolic contents of tomato using conventional and ecological horticultural practices, and arbuscular mycorrhizal fungi (AMF). Agron Colomb 26(1): 40-46
  27. Wang Y, Zhang W, Liu W, Ahammed GJ, Wen W, Guo S, Sun J (2021) Auxin is involved in arbuscular mycorrhizal fungi- promoted tomato growth and NADP-malic enzymes expression in continuous cropping substrates. BMC Plant Biology 21(1): doi:10.1186/s12870-020-02817-2
    Pubmed KoreaMed CrossRef
  28. Zhao YY, Cartabia A, Lalaymia I, Declerck S (2022) Arbuscular mycorrhizal fungi and production of secondary metabolites in medicinal plants. Mycorrhiza 32:221-256
    Pubmed KoreaMed CrossRef
  29. Ziane H, Meddad-Hamza A, Beddiar A, Gianinazzi S (2017) Effects of arbuscular mycorrhizal fungi and fertilization levels on industrial tomato growth and production. Int J Agric Biol 19:341-347. https://doi.org/10.17957/IJAB/15.0287
    CrossRef
JPB
Vol 51. 2024

Stats or Metrics

Share this article on

  • line

Related articles in JPB

Journal of

Plant Biotechnology

pISSN 1229-2818
eISSN 2384-1397
qr-code Download