Since the studies were conducted in a climate chamber, the differences between years were not statistically significant. Therefore, analyses were performed by combining the data from both years.
Tubercule Density in Tomato Roots Caused by Branched Broomrape
The differences in the number of broomrape tubercles in the roots of tomatoes treated with or without the biological control agent were statistically significant (p < 0.05, Table 2, Fig. 2). The data analysis revealed that MIX had at least one tubercle overall (3.75 pots/piece), followed by M1 (5.25 pots/piece), M2P2 (5.37 pots/piece), and TH (5.50 pots/piece). All treatments, except for the THP1 and P1 treatments, decreased broomrape attachment compared to that in the control group; the most effective treatments were MIX, M1, TH, and M2P2. Compared to the control group, MIX, M1, M2P2, and TH prevented tubercle formation by 72.72%, 61.82%, 60.95% and 60.0%, respectively.
Table 2
Effect of Biological Control Agents on the Number of Branched Broomrape Tubercles in Tomato Roots (Average over Two Years, Number of Tubercles per Pot)
Treatments | Number of tubercules (Mean ± SE) | Rate of change compared to control (%) |
K | 13.75 ± 0.65 ab | |
M1 | 5.25 ± 0.65 e | -61.82 |
M2 | 9.37 ± 0.84 cd | -31.85 |
P1 | 13.75 ± 1.19 ab | 0.00 |
P2 | 9.12 ± 0.48 cd | -33.67 |
TH | 5.50 ± 0.71 e | -60.00 |
MIX | 3.75 ± 0.41 e | -72.73 |
M1P1 | 9.87 ± 0.72 bcd | -28.22 |
M1P2 | 11.37 ± 1.21 abc | -17.31 |
M2P1 | 10.00 ± 0.63 bcd | -27.27 |
M2P2 | 5.37 ± 0.71 e | -60.95 |
THM1 | 6.87 ± 0.79 de | -50.04 |
THM2 | 9.12 ± 0.77 cd | -33.67 |
THP1 | 15.25 ± 0.70 a | 10.91 |
THP2 | 11.62 ± 0.94 abc | -15.49 |
Mean | 9.33 ± 0.76 | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2). SE: Standart error.
The results of this study were in parallel with those of several previous studies, and it was observed that all the microorganisms and biological preparations used, except P1 and THP1, prevented the formation of broomrape tubercles. It is thought that the fact that P1 and THP1 application did not prevent the decrease in tubercle number may be due to an antagonistic effect. Recently, many biological control agents, especially microorganisms such as fungi and bacteria, have become the focus of interest for inhibiting broomrape germination (Dor et al. 2007; Sauerborn et al. 2007). Studies have shown that AMF have the potential to reduce P. ramosa infection and partially mitigate its negative effects on tomato plant growth ( Gworgwor and Weber 2003; Lendzemo et al. 2007; Fernández et al. 2010). In studies conducted in faba beans, it was reported that the use of AMF, T. harzanium, and some bacterial isolates reduced O. crenata germination (Hassan and Abakeer 2013). The application of G. intraradices, G. mosseae, and Glomus Sprint® to tomato plants reduced the percentage of P. ramosa tubercles by 22.2%, 42% and 56.8%, respectively (Musa 2012).
Several potential mechanisms are thought to explain the negative effects of biological control agents on weeds. One of them can be considered a direct effect, such as the reaction of the plant's defense system depending on the fungus used and the production of toxic compounds that can inhibit seed germination (Boari and Vurro 2004; Campos et al. 2012). Other researchers (Yoneyama et al. 2007; Fernández et al. 2010) have reported that AMF increase plant nutrient uptake, especially phosphorus, which may be due to a decrease in the amount of germination stimulants such as strigolactone present in root secretions. Therefore, it has been reported that nutrients as well as organic matter applied from the soil may cause serious physiological disorders in the germination of P. ramosa seeds with a decrease in weed infestation (Lops et al. 2017). It is also thought that some microorganisms thicken the cell wall of the host plant through enzymes and consequently affect the penetration between the host and the parasite by affecting the vascular connection, making it difficult for the broomrape to attach to the roots of the host plant (Pérez et al. 2005; Brahmi et al. 2016).
Effects of Branched Broomrape Infection and Biological Control Agents on Some Antioxidative Enzymes and MDA Activity in Tomato
Effect on Catalase (CAT) Enzyme Activity
For the antioxidant activity of CAT, as shown in Table 3, the differences between the means of the treatments infected and not infected with broomrape were statistically significant. Compared with that in the noninfected treatment group, the CAT content in the broomrape-infected treatment group increased. Specifically, the CAT activity was 80.95% greater in the plants infected with the branched broomrape than in the control plants.
Table 3
The effect of branched broomrape infestation and biological control agents on the CAT enzyme activity (mmol g− 1 FW)
Treatments | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 0.0021 ± 0.0002 abc B | | 0.0038 ± 0.0004 bc A | |
M1 | 0.0024 ± 0.0004 abc | 14.77 | 0.0032 ± 0.0004 bc | -13.89 |
M2 | 0.0018 ± 0.0003 abcd B | -13.92 | 0.0035 ± 0.0002 bc A | -5.56 |
P1 | 0.0022 ± 0.0002 abc B | 7.23 | 0.0053 ± 0.0006 a A | 41.67 |
P2 | 0.0021 ± 0.0003 abc B | -0.20 | 0.0056 ± 0.0005 a A | 50.00 |
TH | 0.0010 ± 0.0001 d B | -50.10 | 0.0026 ± 0.0003 c A | -30.56 |
MIX | 0.0015 ± 0.0003 cd B | -30.14 | 0.0025 ± 0.0002 c A | -33.33 |
M1P1 | 0.0021 ± 0.0002 abc | 1.05 | 0.0029 ± 0.0003 c | -22.92 |
M1P2 | 0.0015 ± 0.0003 cd B | -30.14 | 0.0035 ± 0.0003 bc A | -5.56 |
M2P1 | 0.0026 ± 0.0005 a | 22.26 | 0.0030 ± 0.0007 c | -19.44 |
M2P2 | 0.0024 ± 0.0003 ab | 17.27 | 0.0035 ± 0.0006 bc | -6.94 |
THM1 | 0.0025 ± 0.0002 a B | 19.76 | 0.0047 ± 0.0005 ab A | 25.00 |
THM2 | 0.0021 ± 0.0003 abc B | -0.20 | 0.0040 ± 0.0005 bc A | 5.56 |
THP1 | 0.0027 ± 0.0003 a | 29.12 | 0.0029 ± 0.0004 c | -23.71 |
THP2 | 0.0015 ± 0.0001 bcd B | -27.64 | 0.0027 ± 0.0005 c A | -27.78 |
Mean | 0.0020 B | | 0.0036 A | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
Effect on superoxide dismutase (SOD) enzyme activity
For the antioxidative stress enzyme SOD, as shown in Table 4, the differences between the means of the treatments infected and not infected with broomrape were statistically significant. When comparing the treatments with and without broomrape infection, statistically significant differences were observed only for the K, M2, P1, M1P1, M2P1, and THP2 treatments. The highest SOD activity was detected in the P1 and M2P1 treatments, while the lowest SOD activity was detected in the M2 and THP2 treatments. Among the broomrape treatment groups, the highest SOD activity was detected in the M2 and M2P2 treatment groups, while the lowest SOD activity was detected in the M1P1 and THP2 treatment groups.
Table 4
The effect of branched broomrape infestation and biological control agents on the SOD enzyme activity (U mg− 1 FW)
Treatment | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 137.99 ± 13.27 abc A | | 93.17 ± 6.51 bcd B | |
M1 | 93.89 ± 11.48 de | -31.96 | 105.40 ± 12.98 bc | 13.13 |
M2 | 64.93 ± 8.31 e B | -52.94 | 168.91 ± 13.33 a A | 81.29 |
P1 | 157.66 ± 9.33 a A | 14.25 | 103.86 ± 8.75 bc B | 11.47 |
P2 | 109.01 ± 16.09 bcd | -21.00 | 97.17 ± 4.81 bcd | 4.29 |
TH | 88.32 ± 13.28 de | -36.00 | 63.48 ± 9.19 de | -31.87 |
MIX | 112.42 ± 14.57 bcd | -18.53 | 86.47 ± 7.56 bcd | -7.19 |
M1P1 | 83.50 ± 9.31 de A | -39.49 | 46.97 ± 4.00 e B | -49.59 |
M1P2 | 98.55 ± 9.53 de | -28.58 | 88.88 ± 12.02 bcd | -4.60 |
M2P1 | 142.59 ± 11.48 ab A | 3.34 | 77.96 ± 15.23 cde B | -16.33 |
M2P2 | 95.14 ± 14.66 de | -31.05 | 121.51 ± 9.64 b | 30.42 |
THM1 | 104.04 ± 14.12 cde | -24.61 | 75.28 ± 16.81 cde | -19.20 |
THM2 | 109.98 ± 12.71 bcd | -20.30 | 102.77 ± 19.31 bc | 10.30 |
THP1 | 99.36 ± 11.37 de | -28.00 | 118.49 ± 6.27 b | 27.17 |
THP2 | 73.09 ± 3.99 de B | -47.04 | 111.48 ± 14.26 bc A | 19.65 |
Mean | 104.7 ± 3.66 | | 97.45 ± 3.77 | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
Effect on Ascorbate Peroxidase (APX) Enzyme Activity
According to the APX activity data in Table 5, the differences between the treatments with and without broomrape infection were found to be statistically significant. Comparing the branched broomrape infected and uninfected treatments, the differences between the means were significant only for the K, P2, M1P2, THM1, and THP2 treatments. The highest APX content was detected in K and M1 in the treatments not infected with broomrape, while the highest APX content was detected in P2 and THM1 in the infection treatments. The lowest APX content was detected in P2, M1P2, M2P2, and THM1 in the noninfected treatments, and the lowest APX content was detected in P1, M2P2 and THP2 in the infected treatments.
Table 5
The effect of branched broomrape infestation and biological control agents on the APX enzyme activity (mmol g− 1 FW) in tomato
Treatment | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 0.045 ± 0.005 a A | | 0.027 ± 0.004 cde B | |
M1 | 0.031 ± 0.006 b | -30.00 | 0.038 ± 0.005 abc | 41.67 |
M2 | 0.029 ± 0.003 bc | -35.00 | 0.025 ± 0.003 cde | -5.55 |
P1 | 0.022 ± 0.003 bcd | -50.00 | 0.018 ± 0.001 e | -33.33 |
P2 | 0.018 ± 0.001 d B | -60.00 | 0.043 ± 0.006 a A | 61.11 |
TH | 0.022 ± 0.003 bcd | -50.00 | 0.033 ± 0.005 abcd | 22.22 |
MIX | 0.024 ± 0.003 bcd | -46.67 | 0.025 ± 0.003 cde | -5.55 |
M1P1 | 0.021 ± 0.002 bcd | -53.33 | 0.029 ± 0.006 bcde | 8.33 |
M1P2 | 0.020 ± 0.002 cd B | -55.00 | 0.033 ± 0.005 abcd A | 25.00 |
M2P1 | 0.022 ± 0.003 bcd | -50.00 | 0.028 ± 0.006 bcde | 5.56 |
M2P2 | 0.020 ± 0.002 cd | -55.00 | 0.018 ± 0.001 e | -33.33 |
THM1 | 0.020 ± 0.002 cd B | -55.00 | 0.040 ± 0.004 ab A | 50.00 |
THM2 | 0.025 ± 0.003 bcd | -43.33 | 0.024 ± 0.003 de | -11.09 |
THP1 | 0.030 ± 0.004 bc | -33.33 | 0.020 ± 0.002 de | -25.00 |
THP2 | 0.028 ± 0.003 bcd A | -38.33 | 0.018 ± 0.001 e B | -33.33 |
Mean | 0.025 | | 0.028 | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
All plants are exposed to biotic and abiotic stresses throughout their life (Davis and Swanson 2001; Jamshidi et al. 2020). Plant enzymes, such as CAT, SOD and APX, play a critical role in the growth and development of plants. These enzymes constitute the antioxidant defense system of plants, protecting them against oxidative stress induced by reactive oxygen species (ROS) (Rajput et al. 2021; Bhat et al. 2022). An increase in the SOD enzyme under biotic and abiotic stress conditions is crucial for plant survival under such stress (Büyük et al. 2012). When the SOD enzyme converts O2 formed under stress conditions into H2O2 and O2, the CAT enzyme directly converts H2O2 into H2O and O2, thereby shielding the plant against stress factors (Van Camp et al. 1997). Antioxidant enzymes such as ascorbate peroxidase (APX), glutathione reductase, catalase (CAT), and superoxide dismutase (SOD) reduce ROS production, preventing the harmful accumulation of H2O2 (Gill and Tuteja 2010; Kang et al. 2014).
Researchers have reported that plants respond differently to oxidative stress conditions in weeds ( Davis and Swanson 2001; Caverzan et al. 2019). The complex structure of beneficial microorganisms is the main reason that different microorganism treatments affect enzyme activity in plants in various ways. Plants tend to determine the optimal strategy to minimize damage caused by pest organisms, resulting in diverse responses of microorganisms to pests (Van der Putten et al. 2001; Caccavo et al. 2022). For instance, Madany et al. (2020) reported that CAT activity was significantly greater in tomato plants infected with broomrape than in uninfected control plants. Chen et al. (1993) reported that, along with the increase in CAT activity, plant cell wall resistance also increased, serving as a signal for the stimulation of defense genes. In three sunflower cultivars contaminated with broomrape, it was observed that broomrape caused variations in total SOD activity depending on the attachment time (Demirbaş and Acar 2008). Alam et al. (2023) reported that the APX content in three different tomato cultivars grown under drought stress differed according to the AMF species. In a study investigating the effects of F. oxysporum on Orobanche spp., it was determined that compared with the control treatment, F. oxysporum treatment increased the SOD content and decreased the CAT content (Aybeke, 2017). This is thought to be related to the penetration of the parasite into the tissue and the development of resistance against ROS in cells (Demirbaş and Acar, 2008).
In this study, the CAT content was significantly greater in the branched broomrape-infected plants than in the uninfected plants. The SOD content varied in both the broomrape-infected and uninfected treatments, showing an increase in some treatments and a decrease in others. Compared with that in the control group, the APX content decreased in the plants not infected with broomrape; however, compared with that in the control group, the APX content increased in some treatments and decreased in others in the plants infected with broomrape. Similarly, in a previous study conducted in various parts of the world, under stress conditions caused by broomrape infection, both the increase and decrease in the oxidative enzyme content increased and decreased, respectively.
Effect on Lipid Peroxidation [Malondialdehyde (MDA)] Activity
For the MDA content shown in Table 6, the differences between the means of the treatments not infected with broomrape were found to be statistically insignificant, while the differences between the means of the infected treatments were significant. The MDA content increased in all the treatments except for the K and M1P1 treatments compared with that in the uninfected treatment. The MDA content increased in all treatments in the presence of broomrape infection compared to that in the control group.
Table 6
The effect of branched broomrape infestation and biological control agents on the MDA content (µmol g− 1 FW)
Treatment | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 3.00 ± 0.23 A | | 2.12 ± 0.20 d B | |
M1 | 3.10 ± 0.44 | 3.32 | 4.52 ± 0.88 ab | 112.93 |
M2 | 2.77 ± 0.26 B | -7.44 | 5.00 ± 0.88 a A | 135.74 |
P1 | 2.32 ± 0.32 | -22.69 | 2.53 ± 0.51 cd | 19.39 |
P2 | 2.08 ± 0.26 B | -30.76 | 3.24 ± 0.37 bcd A | 52.60 |
TH | 2.87 ± 0.36 | -4.22 | 3.90 ± 0.65 abc | 84.03 |
MIX | 3.11 ± 0.33 | 3.68 | 3.68 ± 0.42 abcd | 73.38 |
M1P1 | 2.71 ± 0.43 | -9.60 | 2.55 ± 0.30 cd | 20.15 |
M1P2 | 2.79 ± 0.33 B | -6.91 | 4.49 ± 0.26 ab A | 111.91 |
M2P1 | 2.53 ± 0.29 B | -15.70 | 3.58 ± 0.23 abcd A | 68.82 |
M2P2 | 2.60 ± 0.27 B | -13.18 | 4.08 ± 0.45 abc A | 92.52 |
THM1 | 2.91 ± 0.41 | -2.78 | 3.46 ± 0.53 abcd | 63.24 |
THM2 | 3.48 ± 0.31 | 16.14 | 4.10 ± 0.36 abc | 93.54 |
THP1 | 2.98 ± 0.50 | -0.63 | 3.78 ± 0.22 abc | 78.45 |
THP2 | 1.77 ± 0.20 B | -41.08 | 3.81 ± 0.55 abc A | 79.47 |
Mean | 2.73 ± 0.9 B | | 3.66 ± 0.14 A | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
ROS cause increased lipid peroxidation in plants, and ROS production is inevitable in response to stress (Abogadallah 2010; Jamshidi et al. 2020). Lipid peroxidation leads to cell membrane damage, loss of cell fluid, and cell death, resulting in the plant producing MDA. In other words, the greater the degree of damage to the cell membrane structure, the greater the MDA content (Dhindsa and Matowe 1981; Yonghua et al. 2005). Therefore, MDA, a product of lipid peroxidation, is considered a biochemical indicator of oxidative damage (Apel and Hirt 2004). Madany et al. (2020) reported that IAA (indole acetic acid) and SA (salicylic acid) application to seeds had no significant effect on the MDA content in tomatoes compared to the control group, but the MDA content increased by 34% in tomatoes infected with broomrape. In cucumber studies, the MDA content increased in all cucumber genotypes as a result of P. aegyptiaca infection compared to that in the control (Faradonbeh et al. 2020; Faradonbeh et al. 2021). This study revealed that the MDA content generally increased in the broomrape-infected plants compared to that in the uninfected plants. In addition, in parallel with the studies mentioned above and in previous years, it was determined that the MDA content increased in the treatments infected with broomrape compared to the control.
Effects of Branched Broomrape Contamination and Biological Control Agents on Total Phenolic and Antioxidant Substances in Tomato
The differences between the means of both the infected and noninfected treatments were found to be statistically significant for the amount of phenolic substances given in Table 7. The greatest amount of phenolic matter was found in the M2 and M2P1 treatment groups in the noninfected treatment group, and the greatest amount was found in the THP2 and THP1 treatment groups in the infected treatment group. The lowest phenolic content was found in P1 and K in the uninfected treatments, and the lowest phenolic content was found in THM1 and P1 in the infected treatments. Compared with those in the control treatments, there was no significant increase in the amount of total phenolic substances in either the infected or noninfected plants, but there were differences between the treatments.
Table 7
The effect of branched broomrape infestation and biological control agents on total phenolic matter content (mg GAE/100 g)
Treatment | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 22.01 ± 1.70 c | | 25.82 ± 0.53 cdef | |
M1 | 25.22 ± 0.65 abc | 14.59 | 23.67 ± 0.71 ef | -8.30 |
M2 | 27.82 ± 1.76 a | 26.44 | 25.73 ± 1.31 cdef | -0.35 |
P1 | 21.23 ± 1.07 c | -3.53 | 22.70 ± 1.43 f | -12.08 |
P2 | 24.80 ± 0.62 abc | 12.70 | 27.32 ± 1.23 bcde | 5.83 |
TH | 23.28 ± 0.61 bc | 5.77 | 24.68 ± 1.92 def | -4.41 |
MIX | 22.48 ± 1.13 c B | 2.15 | 27.88 ± 1.21 bcd A | 7.97 |
M1P1 | 22.57 ± 1.37 c B | 2.56 | 28.71 ± 0.85 abcd B | 11.20 |
M1P2 | 27.27 ± 0.90 ab | 23.92 | 29.05 ± 0.77 abc | 12.52 |
M2P1 | 27.77 ± 1.11 a | 26.20 | 25.93 ± 0.54 cdef | 0.44 |
M2P2 | 27.57 ± 1.37 a | 25.30 | 27.81 ± 1.56 bcd | 7.74 |
THM1 | 23.99 ± 1.79 abc | 9.01 | 22.66 ± 1.52 f | -12.22 |
THM2 | 25.47 ± 1.73 abc | 15.72 | 27.98 ± 1.62 bcd | 8.38 |
THP1 | 24.55 ± 1.54 abc B | 11.57 | 30.90 ± 1.65 ab A | 19.71 |
THP2 | 23.22 ± 0.78 bc B | 5.51 | 32.41 ± 1.03 a A | 25.56 |
Mean | 24.62 ± 0.36 B | | 26.88 ± 0.39 A | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
The total antioxidant content shown in Table 8 revealed statistically significant differences between the means of both the infected and noninfected treatments. In the noninfected treatments, the highest total antioxidant amounts were observed in the M1 and M2P1 treatments, whereas in the infected treatments, the highest total antioxidant amounts were found in the M1 and M1P1 treatments. Conversely, the lowest levels of total antioxidants were found in M2P2 and P1 in the noninfected treatments and in THP1 and M2P1 in the infected treatments. Upon comparing the plants infected and not infected with broomrape to the control plants, an increase in the total antioxidant amount was observed in some treatments, while a decrease was observed in others.
Table 8
The effect of branched broomrape infestation and biological control agents on the total antioxidant content (Trolox µmol (Trolox equivalent) TE/100g)
Treatment | Uninfected with broomrape (Mean ± SE) | Rate of change compared to control (%) | Infected with broomrape (Mean ± SE) | Rate of change compared to control (%) |
K | 238.12 ± 13.34 bc | | 189.64 ± 21.65 abcd | |
M1 | 326.76 ± 30.04 a | 37.22 | 259.33 ± 25.98 a | 36.75 |
M2 | 232.68 ± 11.29 cd | -2.29 | 214.79 ± 29.39 abc | 13.26 |
P1 | 166.15 ± 14.99 ef | -30.22 | 220.70 ± 54.29 ab | 16.38 |
P2 | 213.73 ± 15.37 cde A | -10.24 | 134.33 ± 13.60 def B | -29.16 |
TH | 192.67 ± 11.00 cde | -19.09 | 214.64 ± 17.15 abc | 13.18 |
MIX | 239.03 ± 34.62 bc | 0.38 | 187.74 ± 11.35 abcd | -1.00 |
M1P1 | 169.18 ± 13.85 ef B | -28.95 | 258.58 ± 24.91 a A | 36.35 |
M1P2 | 210.09 ± 16.75 cde | -11.77 | 226.00 ± 11.08 ab | 19.18 |
M2P1 | 291.15 ± 28.98 ab A | 22.27 | 105.17 ± 11.48 ef B | -44.54 |
M2P2 | 127.89 ± 10.19 f | -46.29 | 105.58 ± 9.42 ef | -44.32 |
THM1 | 174.48 ± 23.41 def | -26.72 | 164.26 ± 24.92 bcde | -13.38 |
THM2 | 168.48 ± 12.55 ef | -29.25 | 145.64 ± 6.46 cde | -23.20 |
THP1 | 222.59 ± 11.04 cde A | -6.52 | 69.62 ± 3.28 e B | -63.29 |
THP2 | 182.78 ± 16.19 cdef | -23.24 | 172.02 ± 12.72 bcde | -9.29 |
Mean | 210.39 ± 6.5 A | | 177.87 ± 7.37 B | |
a, b, c: The difference between the means shown with different letters in the same column is statistically significant (p < 0.05).
A, B: The difference between the treatments with and without weed is significant at p < 0.05. SE: Standart error.
Treatments: K: Control, M1: Funneliformis mosseae, M2: ERS Commercial AMF, P1: Pseudomonas caspiana (V30G2), P2: Bacillus velezensis (V40K2), TH: Trichoderma harzianum (T22), MIX: Plant Success Great White Premium Mycorrhiza, M1P1: F. mosseae + P. caspiana (V30G2), M1P2: F. mosseae + B. velezensis (V40K2), M2P1: ERS + P. caspiana (V30G2), M2P2: ERS + B. velezensis (V40K2), THM1: T. harzianum T22 + F. mosseae, THM2: T. harzianum T22 + ERS, THP1: T. harzianum T22 + P. caspiana (V30G2), THP2: T. harzianum T22 + B. velezensis (V40K2).
Phenolic compounds, which are found in many plant organs, are nonenzymatic secondary metabolism products. These compounds play a role in ecological and physiological events and have antioxidant activity (Kıpçak et al. 2019). The total phenolic content of host plants can be affected by the use of biological control agents (Doley and Jite, 2014). In addition, the total phenolic content also changes due to infection of host plants by pathogens (Singh et al. 2013). Singh et al. (2013) reported that differences in the host plant's total antioxidant activity occurred due to pathogen infection, while Doley and Jite (2014) reported that the total antioxidant content was affected by the use of biological control agents. Faradonbeh et al. (2020) reported that increased phenol compounds in sunflower due to broomrape contamination can be considered a protective response against O. cumuna. This study examined the impacts of several mycorrhiza species on organic carrot farming and revealed that antioxidant activity was positively impacted. (Kiracı et al. 2014). In one study, it was determined that the biological control agents used in tomatoes did not have a significant effect on total phenolic matter or antioxidant activity, and there were changes depending on the application (Boyno et al. 2022). According to the data obtained in the present study, compared with those in the control group, the total phenolic matter and antioxidant content in plants not infected with broomrape increased in some treatment groups but decreased in other treatment groups.