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Article

In Vitro Study of the Compatibility of Four Species of Trichoderma with Three Fungicides and Their Antagonistic Activity against Fusarium solani

by
Conrado Parraguirre Lezama
1,
Omar Romero-Arenas
1,*,
Maria De Los Angeles Valencia de Ita
1,
Antonio Rivera
2,
Dora M. Sangerman Jarquín
3 and
Manuel Huerta-Lara
4,*
1
Centro de Agroecología, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Edificio VAL 1, Km 1.7, Carretera a San Baltazar Tetela, San Pedro Zacachimalpa 72960, Puebla, Mexico
2
Centro de Investigaciones en Ciencias Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Ciudad Universitaria, Puebla 72570, Puebla, Mexico
3
Campo Experimental Valle de México-INIFAP, Carretera Los Reyes-Texcoco Km 13.5, Coatlinchán 56250, Texcoco, Mexico
4
Departamento de Desarrollo Sustentable, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Ciudad Universitaria, Puebla 72570, Puebla, Mexico
*
Authors to whom correspondence should be addressed.
Horticulturae 2023, 9(8), 905; https://doi.org/10.3390/horticulturae9080905
Submission received: 15 June 2023 / Revised: 1 August 2023 / Accepted: 2 August 2023 / Published: 8 August 2023
(This article belongs to the Special Issue Sustainable Control Strategies of Plant Pathogens in Horticulture)
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Abstract

Strawberry wilt is a disease caused by Fusarium solani, which it provokes the death of the plant. Farmers mainly use chemical methods for its control, which has a negative impact on the environment and human health. Given the growing demand for organic agricultural products, compatible alternatives must be sought for disease management that can reduce the doses of fungicides. A combination of pesticides and biological control agents could be an alternative for the management of F. solani. Consequently, investigations on fungicide compatibility and synergistic effects are recommended in relation to the biological control of strawberry wilt. In this study, potential antagonism was calculated according to the class of mycoparasitism and the percentage inhibition of radial growth in order to later design a compatibility model of the different species of Trichoderma with three protective fungicides at different concentrations. The potential antagonism showed that Trichoderma asperellum presented high compatibility with the fungicides Captan and Mancozeb added in concentrations of 450, 900, and 1350 mg L−1. The use of antagonistic strains together with the fungicide Chlorothalonil in its three concentrations showed a negative effect on the growth of Trichoderma species, which caused low and null compatibility against the MA-FC120 strain of F. solani in vitro.

1. Introduction

Crown and root rot in strawberry cultivation is the most important and destructive disease of the crop worldwide [1]. The disease limits plant growth and fruit production, causing large economic losses and low yields [2,3], especially when heat and humidity stress is induced [4].
Strawberry wilt is a disease induced by Fusarium solani, which produces stunted plant growth, followed by wilting, and finally plant death [5,6,7]. Lately, in Spain, it has been reported in strawberry crops, both in nurseries and production fields [8]. Likewise, it has been described as a strawberry pathogen in Italy [9], Iran, and Pakistan [10]. However, in Mexico there have been few reports [11].
To reduce losses caused by F. solani in strawberry production, farmers use chemical control methods, which have become an essential part of agriculture [12,13]. Consequently, chemical fungicides are still used recklessly as the primary means of disease control throughout the world. Isolates of F. solani species have recently been reported to show reduced susceptibility to azoles in agriculture, an attention-grabbing fact [14,15]. In addition, the intensive use of fungicides has an adverse effect on human health and a negative impact on the environment [16,17].
There is currently awareness and concern among fruit and vegetable consumers regarding pesticide residues in food, with an emphasis on minimizing their use and application without increasing risks in agricultural production [18]. It is crucial to intensify efforts to develop alternative farm management practices that can reduce the use of chemicals to control F. solani in a sustainable and environmentally friendly manner. A combination of pesticides and biological control agents (BCAs) could be an effective tool and improve the fight against plant pathogens in a more reliable way [19]. Likewise, environmental impacts could be reduced by using low concentrations of fungicides, which would help to minimize the danger associated with the use of chemical pesticides [20,21,22].
The possibility of generating a synergistic effect with the application of fungicides and biological antagonists, such as Trichoderma spp. has been reported by several authors [23]. Terrero et al. [24] reported the compatibility of Trichoderma species with azoxystrobin and copper hydroxide fungicides, and Ruano et al. [25] implemented the use of Trichoderma spp. and the fungicide fluazinam (in concentrations of 0.01 and 0.05 mg L−1) for the control of Rosellinia necatrix in avocado plants. In a study conducted by Wang et al. [26], a greater control of root rot was reported as well as elevated survival of coneflower seedlings (Echinacea spp.) with the combination of Trichoderma and fludioxonil against Fusarium sp. in greenhouses. However, the control of wilting of strawberry crops remains a challenge. Therefore, the objective of this investigation was to evaluate the in vitro compatibility of four species of Trichoderma with three broad-spectrum fungicides through potential antagonism (PA) against the MA-FC120 strain of F. solani.

2. Materials and Methods

2.1. Biological Material

The strains used were T-H4 of Trichoderma harzianum, T-K11 of Trichoderma koningiopsis, T-AS1 of Trichoderma asperellum, and T-A12 of Trichoderma hamatum, isolated from the root of Persea americana; the sequences of these strains were deposited in the National Center for Biological Information (NCBI) database with accession numbers MK779064, MK791648, MK778890, and MK791650, respectively. The MA-FC120 strain of F. solani was used, which is pathogenic for strawberry cultivation [3], with accession number OM616884, characterized by the Phytopathology Laboratory 204 of the Agroecology Center of the Institute of Sciences, BUAP.

2.2. Characterization of the Rate of Development and Growth

For the evaluation of development rate, 10-day-old fragments of 5 mm in diameter with active growth of F. solani (MA-FC120), T-H4 of T. harzianum, T-K11 of T. koningiopsis, T-AS1 of T. asperellum, and T-A12 of T. hamatum were seeded individually in Petri dishes (9 cm in diameter) containing 20 mL of PDA (Bioxon, Becton Dickinson, Cdad., Mexico, Mexico) and incubated at 28 °C for 10 days in the dark. Every 12 h, the diameter of the mycelium was measured with a digital vernier (CD-6 Mitutoyo, Naucalpan de Juarez, Mexico) to assess the growth rate (cm d−1), which was calculated with the linear growth function [27] as per Equation (1):
y = mx + b
where
  • y = Distance;
  • m = Slope;
  • x = Time;
  • b = Constant factor.
The experiment was repeated in duplicate in a completely randomized statistical design, with three replicates for each treatment.

2.3. Dual Test on Poisoned Culture Medium In Vitro

The controlled poisoning technique was performed [28] on potato dextrose agar (PDA, Bioxon, Becton Dickinson and Company, Querétaro, Mexico) using three protective fungicides (Chlorothalonil, Mancozeb, and Captan) at different concentrations (Table 1). To determine the percentage inhibition of radial growth (PIRG), we used PDA discs (5 mm in diameter) with the mycelium of Trichoderma spp. and F. solani. They were placed at the ends of the poisoned Petri dishes with 7.5 cm between them (antagonist–phytopathogen). All plates were sealed with Parafilm® and incubated in the dark at 28 °C for 10 days.
Radial growth of the fungal colony was evaluated every 12 h until the first contact between the mycelia of each antagonist with F. solani occurred. The percentage inhibition of radial growth (PIRG) was calculated based on the formula of Equation (2) [29]:
PIRG% = (R1 − R2)/R1 × 100
where
  • PIRG = Percentage inhibition of radial growth;
  • R1 = Radial growth (mm) of F. solani without Trichoderma spp.;
  • R2 = Radial growth (mm) of F. solani with Trichoderma spp.
Mycoparasitism ability due to the invasion of the antagonist or colonization on the mycelial surface of F. solani was evaluated according to the scale proposed by Bell et al. [30] (Table 2).
The experiment was repeated in duplicate in a completely randomized statistical design, with four replicates for each treatment.

2.4. Potential Antagonism

Potential antagonism (PA) was calculated by averaging the results of the mycoparasitism class (Bell) and percentage inhibition of the radial growth rate (PIRG), as proposed by Reyes-Figueroa et al. [31] (3):
PA% = (Bell + PIRG)/2
where
  • PA = Potential antagonism expressed as a percentage;
  • Bell = Trichoderma mycoparasitism against F. solani;
  • PIRG = Inhibition of radial growth of F. solani.
The design of the model of compatibility (C) of Trichoderma with different fungicides included the identification of the highest and lowest potential antagonism (PA). Then, the difference between them was calculated and divided by four [32]. Finally, the quotient was added to the lower performance progressively until the formation of four groups was achieved (Table 3).

2.5. Statistical Analysis

Data were analyzed using ANOVA (two-way) in the statistical package SPSS Statistics version 17 for Windows. Growth rate and development rate were response variables. Data were subjected to Bartlett’s test of homogeneity, and subsequently a Tukey–Kramer comparison of means test was performed with a probability level of p ≤ 0.05.
The mycoparasitism class (Bell), percentage inhibition of radial growth (PIRG), and potential antagonism (PA) of the strains were expressed in percentages and transformed with angular arccosine √x + 1. Subsequently, the variable compatibility (C) was analyzed under the analysis of variance (multivariate ANOVA) using a quadratic response model to determine significant differences between treatments, under the following mathematical model (4):
Cγj = μ + ti + εij
where
  • Cγj = Value of the response variable of the experimental unit associated with the γ-th treatment and the j-th repetition;
  • μ = Corresponds to the overall mean of the response variable in the experiment;
  • ti = Effect of the γ-th treatment;
  • εγj = Error of the experimental unit associated with the γ-th treatment;
  • j = The j-th repetition;
  • γ = 1, 2, 3, 4, …, 40;
  • j = 1, 2, 3, 4;
  • C = Compatibility (C%).
Finally, a Tukey–Kramer mean comparison test was performed with a probability level of p ≤ 0.05.

3. Results

The rate of development and growth had highly significant differences (p ≤ 0.05); T. koningiopsis (T-K11) obtained the highest value with 1.17 ± 0.02 mm/h−1 and 26.82 ± 0.6 cm d−1, respectively (Table 4). F. solani showed the lowest growth rate (6.71 ± 0.08 cm d−1).
The percentage inhibition of radial growth (PIRG) in the control group did not show significant differences (p = 0.087). Confrontation of the different Trichoderma species against F. solani showed an inhibition between 60 and 70% from the tenth day (Table 5). However, the highest percentage inhibition was obtained with T. harzianum (DTHR0), achieving 67.31%. Similarly, T. hamatum (DTH0) presented the second-best inhibition with 66.95%; both antagonistic strains presented a class II classification (Figure 1) on the scale established by Bell et al. [30]. T. konigiopsis presented the lowest percentage inhibition of radial growth of 64.34%.
In general, the class of mycoparasitism found in this study at 10 days was similar in all Trichoderma strains. In the present investigation, the Trichoderma strains demonstrated a class II classification (Figure 1) according to the scale of Bell et al. [30].
The treatment that obtained the highest percentage inhibition of radial growth (PIRG) in the poisoned culture medium was DTA1 (76.33%), in which the antagonist strain corresponded to T. asperellum in potato dextrose agar dishes with 450 mg L−1 of Captan fungicide added. This difference was statistically significant with respect to the other treatments (p = 0.007). Similarly, T. harzianum (DTHR1) showed the second-best inhibition at 74.82% with the same concentration of Captan fungicide.
T. konigiopsis presented the lowest percentage inhibition of radial growth (PIRG), 64.84%, in the PDA culture medium with 1350 mg L−1 of Captan fungicide added (Table 5). The antagonistic strains T. asperellum and T. harzianum demonstrated a class I classification (Figure 2) according to the scale of Bell et al. [30]. This was dissimilar to T. konigiopsis and T. hamatum which had a classification of mycoparasitism II.
The behavior of the Mancozeb fungicide showed significant differences (p = 0.002). The highest percentage of radial growth inhibition (PIRG) was obtained in the DTHR4 treatment (69.60%), corresponding to T. harzianum in the PDA culture medium with 450 mg L−1 of Mancozeb fungicide. Similarly, T. asperellum (DTA4) demonstrated the second-best inhibition at 68.56%, classified as class I on the scale established by Bell et al. [30], of the three concentrations used. T. konigiopsis presented the lowest percentage inhibition of radial growth (PIRG), between 62.47 and 64.84%, in the potato dextrose agar dishes with 450, 900, and 1350 mg L−1 of Mancozeb fungicide (Table 5). The antagonistic strains T. konigiopsis, T. hamatum, and T. harzianum demonstrated a class II classification (Figure 3) according to the scale of Bell et al. [30].
The treatments in which the Chlorothalonil fungicide was not added presented a higher PIRG; however, we observed that T. konigiopsis (DTK8) demonstrated the best inhibition (55.38%), classified as class III on the scale established by Bell et al. [30]. This difference was statistically significant with respect to the other treatments (p = 0.001).
T. hamatum in the treatments with 450, 900, and 1350 mg L−1 of the fungicide Chlorothalonil (Table 4) in the PDA culture medium presented the second-best percentage inhibition of radial growth (PIRG). The results obtained were between 48.05 and 49.52%. The strain that presented the least antagonism was T. asperellum, reaching a PIRG of 24.35% in the potato dextrose agar dishes with 450 mg L−1 of the Chlorothalonil fungicide, classified as grade IV mycoparasitism (Figure 4). This was followed by the T. harzianum strain with the same concentration.
The MA-FC120 strain of F. solani presented greater radial growth in the treatments with 450, 900, and 1350 mg L−1 of the fungicide Chlorothalonil (Table 4) in the PDA medium in vitro. Likewise, less inhibition exerted by the four Trichoderma strains was observed, classified as grade III and IV mycoparasitism on the scale established by Bell [30] (Figure 4). Furthermore, a 70% decrease in the development rate of the four Trichoderma strains was observed in comparison with the control group. The T. asperellum strain T-AS1 was the most affected of the three concentrations evaluated.
Potential antagonism (PA), in terms of the fungicide and the Trichoderma species evaluated in the present study, revealed a biologically important scenario. The strains of T. asperellum and T. harzianum presented higher levels of PA than T. konigiopsis and T. hamatum (Figure 5) with the fungicides Captan and Mancozeb at the three concentrations evaluated. We might expect that the known intraspecific compatibility variability of different Trichoderma species and phylogenetic affinities towards PA against F. solani would not apply to all species tested. However, when we analyzed the data by species and compatibility, we surprisingly found that the Chlorothalonil fungicide at concentrations of 450, 900, and 1350 mg L−1 presented a low PA in the PDA culture medium when added to the four species of Trichoderma. For the most part, this was below 50%.
In all cases, we observed that treatments with 450, 900, and 1350 mg L−1 of the fungicide Chlorothalonil added to the strain of T. konigiopsis demonstrated the best antagonism potential (58.94%). Statistically significant differences were observed with respect to the other treatments (p = 0.001). T. hamatum in the treatments with 450, 900, and 1350 mg L−1 of the Chlorothalonil fungicide (Figure 5) showed the second-best PA at 49.19%. The strain that showed the lowest PA was T. harzianum, reaching 27.36% in the treatment with 900 mg L−1 of the fungicide Chlorothalonil in the PDA medium in vitro.
Table 6 shows the summary of the multivariate ANOVA analysis for the quadratic response surface model, which revealed highly significant statistical differences. The model values of F = 64.55 (PIRG), 157.538 (Bell), and 204.495 (PA) implied a highly significant model for compatibility (C) in vitro.
The compatibility association analysis considering mycoparasitism, PIRG, and potential antagonism (PA) showed that T. asperellum presented high compatibility (100%) with the fungicides Captan and Mancozeb added at concentrations of 450, 900, and 1350 mg L−1. Compatibility was low–null (25–50%) with the fungicide Chlorothalonil. T. hamatum showed high compatibility (100%) with the fungicide Captan at 450 and 900 mg L−1. Compatibility was medium (75%) with the fungicide Mancozeb in its three concentrations and with Captan at 1350 mg L−1, and low (25%) with the fungicide Chlorothalonil in its three concentrations (Figure 6).
T. harzianum showed high compatibility (100%) with the fungicide Captan at 450, 900, and 1350 mg L−1; medium compatibility (75%) with the fungicide Mancozeb at 450, 900, and 1350 mg L−1, and low compatibility (50%) with the fungicide Chlorothalonil at 450 mg L−1. Compatibility was null (25%) at the 900 and 1350 mg L−1 concentrations of Chlorothalonil (Figure 6). Finally, T. konigiopsis showed medium compatibility (75%) with Captan fungicide in its three concentrations, as well as with Mancozeb fungicide in all cases, and low compatibility (50%) with 450, 900, and 1350 mg L−1 of Chlorothalonil fungicide (Figure 6).

4. Discussion

The genus Fusarium develops in the vascular tissues of plants, causing necrosis in the xylem, which limits water transport and brings about wilting of the plant [33]. Chemical pesticides are still commonly used in strawberry cultivation to suppress F. solani [34,35]. The scant research available limits the ability of strawberry growers to choose effective products and increases the risk of generating strains resistant to the active principles used in fungicides [36]; therefore, this study examined the compatibility between biological and chemical control.
The rapid growth and development observed in the present study may explain the competitive ability of the four Trichoderma species against the MA-FC120 strain of F. solani. Morales et al. [37] found a lower growth rate for the TH-4 strain (1.86 ± 0.22 cm d−1) and a higher development rate (1.67 ± 0.01 mm h−1) in comparison with the present investigation. F. solani presented a slower growth rate (0.4718 ± 0.00063 mm h−1). The results obtained in the present investigation were consistent with a study carried out by Miguel Ferrer et al. [38], where different species of Trichoderma had superior mycelial growth compared with F. solani (4.71 cm d−1).
A reduction in growth rate in dual cultures is an indicator of the antagonistic capacity of Trichoderma [39]. Suárez et al. [40] studied 12 isolates of T. harzianum confronted with F. solani, and they obtained a PIRG of between 60 and 70% antagonism. This was similar to the results obtained in the present investigation for the PDA culture medium without the addition of fungicides. This indicates that T. harzianum has a higher ingestion and metabolism rate than F. solani, as well as different hydrolytic enzyme induction mechanisms that may be involved in fungicide degradation processes [41]. In addition, T. harzianum can inhibit the growth of F. oxysporum because it produces numerous antibiotics such as tricodermin, suzukacillin, alamethicin, dermadin, penicillin, trichothecenes, and trichorzianins, among others [42].
The integrated use of T. asperellum T8a and a low dose of Captan (0.1 g L−1) led to greater in vitro growth inhibition of C. gloeosporioides ATCC MYA 454, a pathogenic strain that causes anthracnose in mango [43]. Similarly, Ruocco et al. [44] explained that the ability of Trichoderma to resist relatively high concentrations of a variety of synthetic and natural toxic compounds depends on a complex system of membrane pumps through which efficient cellular detoxification mechanisms are carried out. In this regard, Singh and Varma [45] reported that the fungicide Mancozeb was the most effective in reducing the mycelial growth of F. solani and was compatible with T. harzianum and T. viride at concentrations of 0.05 and 0.1%.
In the present study, the fungicides Captan and Mancozeb demonstrated high compatibility with the four strains of Trichoderma spp. and inhibited the growth of the pathogen. González et al. [46] reported that the use of the C2A strain of T. reesei in combination with Mancozeb at a concentration of 0.1 mg L−1 improved the mycoparasitic capacity against F. oxysporum. This is in agreement with the results obtained in the present investigation, where the strain of T. asperellum was able to overgrow on Fusarium solani. Of note, Huilgol et al. [47] observed the compatibility of T. harzianum with Mancozeb (71.80%). Similarly, Maheshwary et al. [48] concluded that COC and Mancozeb at 500 ppm favor the growth of T. asperellum. This could explain the greater potential antagonism with respect to the control group in the present investigation.
There are reports of many factors causing the tolerance of Trichoderma strains to pesticides, such as the change in function of oxidoreductase genes and ABC transporter genes resulting in the tolerance of Trichoderma spp. to dichlorvos, Mancozeb, thiram, tebuconazole, and carbendazim [49,50,51].
Finally, it was found that the four strains of Trichoderma spp. were incompatible with the fungicide Chlorothalonil added at concentrations of 450, 900, and 1350 mg L−1. This was similar to the results obtained by Elshahawy et al. [52]. Likewise, Gangopadhyay et al. [53] reported that the fungicide Chlorothalonil is highly toxic for T. viride and T. harzianum, as was also observed in the present investigation, demonstrating no compatibility with T. harzianum. Chlorothalonil is a non-systemic organochlorine foliar fungicide that is widely used throughout the world [54]. Specifically, it is a broad-spectrum polychlorinated aromatic component that delays mycelial growth and inhibits spore germination. It acts mainly on the respiration of fungal cells; that is, it affects the Krebs cycle by reducing ATP synthesis, causing cell death [55]. For this reason, it may be incompatible with biological control agents, as is the case for different species of Trichodermas used in the present investigation.

5. Conclusions

The evaluation of different strains of Trichoderma showed a medium potential antagonism (PA) against the MA-FC120 strain of F. solani in a PDA medium without the addition of fungicides; however, T. harzianum was associated with the highest inhibition in vitro.
T. asperellum demonstrated the highest potential antagonism (PA) against F. solani in the poisoned culture medium, with the fungicides Captan and Mancozeb at concentrations of 450, 900, and 1350 mg L−1 showing greater compatibility. T. harzianum achieved the second highest, demonstrating a high potential antagonism (PA) against F. solani in the PDA medium with the fungicide Captan in the three concentrations evaluated. This was followed by T. hamatum at concentrations of 450 and 900 mg L−1.
T. koningiopsis demonstrated a medium potential antagonism (PA), inhibiting the growth of F. solani by between 60 and 75% in the PDA medium with the fungicides Captan and Mancozeb at the three concentrations evaluated in this study.
The use of Trichoderma strains, together with the fungicide Chlorothalonil at 450, 900, and 1350 mg L−1 in the PDA culture medium, showed an incompatible adverse effect on potential antagonism (PA) given the less than 59% inhibition against F. solani.
F. solani demonstrated better development and adaptation than the Trichoderma strains in the fungicide Chlorothalonil at concentrations of 450, 900, and 1350 mg L−1 in the PDA medium in vitro.

6. Recommendations

The results obtained in the present investigation are important, and we believe that they can be taken to the greenhouse and field for strawberry cultivation. It is recommended to use T. asperellum in combination with the fungicides Captan and Mancozeb at a concentration of 450 mg L−1. In addition, T. harzianum and T. hamatum should be used in combination with the fungicide Captan at a concentration of 450 mg L−1.
Finally, the use of the fungicide Chlorothalonil in combination with any strain of Trichoderma is not recommended to control crown and root rot in strawberry cultivation.

Author Contributions

Conceptualization, O.R.-A., C.P.L. and D.M.S.J.; methodology, A.R., D.M.S.J. and O.R.-A.; software, M.H.-L. and O.R.-A.; validation, M.D.L.A.V.d.I., A.R. and O.R.-A.; formal analysis, D.M.S.J., C.P.L. and O.R.-A.; resources, O.R.-A. and C.P.L.; original—draft preparation, M.D.L.A.V.d.I., M.H.-L. and O.R.-A.; writing—review and editing, A.R. and O.R.-A.; visualization, O.R.-A. and D.M.S.J.; supervision, M.H.-L.; project administration, O.R.-A.; funding acquisition, O.R.-A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT), number 47406; and Benémerita Universidad Autónoma of Puebla, number 100420500.

Data Availability Statement

Informed consent was obtained from all subjects involved in the study.

Acknowledgments

The authors are grateful to Consejo Nacional de Ciencia y Tecnología (CONA-CyT) and Laboratory 204 of the Center for Agroecology at Benémerita Universidad Autónomaof Puebla.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. In vitro mycoparasitism of 10-day-old species of Trichoderma against F. solani in PDA. (A) T. konigiopsis; (B) T. asperellum; (C) T. hamatum; and (D) T. harzianum.
Figure 1. In vitro mycoparasitism of 10-day-old species of Trichoderma against F. solani in PDA. (A) T. konigiopsis; (B) T. asperellum; (C) T. hamatum; and (D) T. harzianum.
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Figure 2. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Captan added at different concentrations. (A–D) Captan at 450 mg L−1; (E–H) Captan at 900 mg L−1; (I–L) Captan at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
Figure 2. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Captan added at different concentrations. (A–D) Captan at 450 mg L−1; (E–H) Captan at 900 mg L−1; (I–L) Captan at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
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Figure 3. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Mancozeb added at different concentrations. (A–D) Mancozeb at 450 mg L−1; (E–H) Mancozeb at 900 mg L−1; (I–L) Mancozeb at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
Figure 3. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Mancozeb added at different concentrations. (A–D) Mancozeb at 450 mg L−1; (E–H) Mancozeb at 900 mg L−1; (I–L) Mancozeb at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
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Figure 4. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Chlorothalonil added at different concentrations. (A–D) Chlorothalonil at 450 mg L−1; (E–H) Chlorothalonil at 900 mg L−1; (I–L) Chlorothalonil at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
Figure 4. In vitro mycoparasitism of different species of Trichoderma against F. solani in PDA medium with Chlorothalonil added at different concentrations. (A–D) Chlorothalonil at 450 mg L−1; (E–H) Chlorothalonil at 900 mg L−1; (I–L) Chlorothalonil at 1350 mg L−1; (A,E,I) T. konigiopsis; (B,F,J) T. asperellum; (C,G,K) T. hamatum; (D,H,L) T. harzianum.
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Figure 5. Potential antagonism (PA) of Trichoderma species against F. solani at different concentrations of fungicides.
Figure 5. Potential antagonism (PA) of Trichoderma species against F. solani at different concentrations of fungicides.
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Figure 6. Compatibility analysis of Trichoderma strains based on multivariate ANOVA analysis with the data of mycoparasitism (Bell), percentage inhibition of radial growth (PIRG), and potential antagonism (PA). The color intensity represents the degree of compatibility of Trichoderma strains under the effects of three fungicides at different concentrations (450, 900, and 1350 mg L−1).
Figure 6. Compatibility analysis of Trichoderma strains based on multivariate ANOVA analysis with the data of mycoparasitism (Bell), percentage inhibition of radial growth (PIRG), and potential antagonism (PA). The color intensity represents the degree of compatibility of Trichoderma strains under the effects of three fungicides at different concentrations (450, 900, and 1350 mg L−1).
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Table 1. Fungicides used at different concentrations evaluated.
Table 1. Fungicides used at different concentrations evaluated.
Fungicide
(Tradename)		Active IngredientMolecular FormulaConcentration (mg L−1)
LowRecommendedHigh
ControlWaterH2O---
Captan 50®CaptanC9H8Cl3NO2S4509001350
Mancosol 80®MancozebC4H6MnN2S4
Talonil 75®ChlorothalonilC8Cl4N2
Table 2. Mycoparasitism class using Bell scale [30] in vitro.
Table 2. Mycoparasitism class using Bell scale [30] in vitro.
ClassMycoparasitism (%)Characteristics
I100Trichoderma grew completely over F. solani and covered the entire mid-surface.
II75Trichoderma grew over at least two-thirds of the mid-surface.
III50Trichoderma and F. solani colonized approximately half of the mid-surface.
IV25F. solani colonized at least two-thirds of the mid-surface.
V0F. solani grew completely over Trichoderma and occupied the entire mid-surface.
Table 3. Compatibility of Trichoderma strains under different protective fungicides.
Table 3. Compatibility of Trichoderma strains under different protective fungicides.
GradeRanges (%)Compatibility
I23 to 42Null
II43 to 59Low
III60 to 75Medium
IV76 to 93High
Table 4. Development and growth rate of 10-day-old colony of Trichoderma strains and F. solani on PDA medium.
Table 4. Development and growth rate of 10-day-old colony of Trichoderma strains and F. solani on PDA medium.
CodeSpeciesStrains* Development Rate
(mm h−1)		* Growth Rate
(cm d−1)
DTF0F. solaniMA-FC1200.28 ± 0.08 e6.71 ± 0.08 e
DTH0T. hamatumT-A121.02 ± 0.02 d26.19 ± 0.53 b
DTA0T. asperellumT-AS11.07 ± 0.05 c24.92 ± 1.34 d
DTK0T. konigiopsisT-K111.17 ± 0.02 a26.82 ± 0.6 a
DTHR0T. harzianumT-H41.14 ± 0.5 b25.20 ± 0.02 c
* Means with different letters indicate statistically significant differences by ANOVA–Tukey test (p < 0.05).
Table 5. Percentage inhibition of radial growth (PIRG) and mycoparasitism on the Bell scale [30].
Table 5. Percentage inhibition of radial growth (PIRG) and mycoparasitism on the Bell scale [30].
CodeFungicideConcentration
(mg L−1)		Species* PIRG (%)SEBell Scale
DTH0Control
(PDA)		-T. hamatum66.95 bcde ± 0.34II
DTA0T. asperellum66.91 bcde ± 0.26II
DTK0T. konigiopsis64.34 def ± 0.59II
DTHR0T. harzianum67.31 bcde ± 1.16II
DTH1Captan450T. hamatum71.11 bcde ± 1.63II
DTA1T. asperellum76.33 a ± 1.16I
DTK1T. konigiopsis67.37 bcde ± 1.31II
DTHR1T. harzianum74.82 b ± 1.01I
DTH2900T. hamatum69.19 bcde ± 3.16II
DTA2T. asperellum73.68 bc ± 1.34I
DTK2T. konigiopsis66.30 bcde ± 0.32II
DTHR2T. harzianum74.58 b ± 1.11I
DTH31350T. hamatum68.37 bcde ± 2.19II
DTA3T. asperellum72.84 bcd ± 1.08I
DTK3T. konigiopsis64.84 cde ± 2.32II
DTHR3T. harzianum72.15 bcd ± 2.51I
DTH4Mancozeb450T. hamatum67.96 bcde ± 0.85II
DTA4T. asperellum68.56 bcde ± 1.40I
DTK4T. konigiopsis64.76 cde ± 1.09II
DTHR4T. harzianum69.60 bcde ± 1.27II
DTH5900T. hamatum65.88 bcde ± 1.00II
DTA5T. asperellum67.93 bcde ± 1.14I
DTK5T. konigiopsis62.82 efg ± 0.82II
DTHR5T. harzianum68.21 bcde ± 1.80II
DTH61350T. hamatum65.72 bcde ± 0.82II
DTA6T. asperellum66.16 bcde ± 0.91I
DTK6T. konigiopsis62.47 efg ± 0.15II
DTHR6T. harzianum67.29 bcde ± 0.60II
DTH7Chlorothalonil450T. hamatum49.52 h ± 1.22III
DTA7T. asperellum28.71 i ± 2.24IV
DTK7T. konigiopsis55.38 fgh ± 1.88III
DTHR7T. harzianum46.33 h ± 2.36III
DTH8900T. hamatum48.38 h ± 0.68III
DTA8T. asperellum28.62 i ± 2.94IV
DTK8T. konigiopsis50.91 gh ± 1.96III
DTHR8T. harzianum28.15 i ± 1.83IV
DTH91350T. hamatum48.05 h ± 3.65III
DTA9T. asperellum24.35 i ± 0.97IV
DTK9T. konigiopsis49.62 h ± 1.26III
DTHR9T. harzianum26.72 i ± 1.19IV
* Means with different letters indicate statistically significant differences by ANOVA–Tukey test (p < 0.05); SE = standard error.
Table 6. Quadratic model of surface response for compatibility (C).
Table 6. Quadratic model of surface response for compatibility (C).
OriginDependent
Variable		Sum of Squares (Type III)gLMean SquareFSig.
Corrected modeX1 = PIRG27,481.902 a39704.66464.55<0.001
X2 = Bell64,000.000 b391641.026157.538<0.001
X3 = PA41,743.713 c391070.352204.495<0.001
IntersectionX1589,547.51589,547.554,004.82<0.001
X2702,2501702,25067,416<0.001
X3644,671.11644,671.1123,166.8<0.001
Compatibility (C%)X127,481.939704.66464.55<0.001
X264,000391641.026157.538<0.001
X341,743.71391070.352204.495<0.001
ErrorX11309.98912010.917
X2125012010.417
X3628.0951205.234
TotalX1618,339.4160
X2767,500160
X3687,043160
Total correctedX128,791.89159
X265,250159
X342,371.81159
(a) R-squared = 0.960 (R-squared adjusted = 0.947); (b) R-squared = 0.989 (R-squared adjusted = 0.985); (c) R-squared = 0.986 (R-squared adjusted = 0.981).
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Parraguirre Lezama, C.; Romero-Arenas, O.; Valencia de Ita, M.D.L.A.; Rivera, A.; Sangerman Jarquín, D.M.; Huerta-Lara, M. In Vitro Study of the Compatibility of Four Species of Trichoderma with Three Fungicides and Their Antagonistic Activity against Fusarium solani. Horticulturae 2023, 9, 905. https://doi.org/10.3390/horticulturae9080905

AMA Style

Parraguirre Lezama C, Romero-Arenas O, Valencia de Ita MDLA, Rivera A, Sangerman Jarquín DM, Huerta-Lara M. In Vitro Study of the Compatibility of Four Species of Trichoderma with Three Fungicides and Their Antagonistic Activity against Fusarium solani. Horticulturae. 2023; 9(8):905. https://doi.org/10.3390/horticulturae9080905

Chicago/Turabian Style

Parraguirre Lezama, Conrado, Omar Romero-Arenas, Maria De Los Angeles Valencia de Ita, Antonio Rivera, Dora M. Sangerman Jarquín, and Manuel Huerta-Lara. 2023. "In Vitro Study of the Compatibility of Four Species of Trichoderma with Three Fungicides and Their Antagonistic Activity against Fusarium solani" Horticulturae 9, no. 8: 905. https://doi.org/10.3390/horticulturae9080905

APA Style

Parraguirre Lezama, C., Romero-Arenas, O., Valencia de Ita, M. D. L. A., Rivera, A., Sangerman Jarquín, D. M., & Huerta-Lara, M. (2023). In Vitro Study of the Compatibility of Four Species of Trichoderma with Three Fungicides and Their Antagonistic Activity against Fusarium solani. Horticulturae, 9(8), 905. https://doi.org/10.3390/horticulturae9080905

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