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Cuban agriculture works on a general agroecological pest management scheme, where biological control is of great importance. Traditionally, arbuscular mycorrhizal fungi (AMF) have been considered as biofertilizers, undervaluing their potential for plant protection. The objective of this research was to evaluate the effect of AMF as a biological control agent of Meloidogyne incognita in combination with irrigation with magnetically treated water (MTW) in protected cultivation. It was carried out in the Campo Antena protected cultivation unit in Santiago de Cuba, Cuba, in the tomato, pepper, cucumber and chard crops. It was determined that AMF inoculation combined with MTW is viable to manage M. incognita populations, in vegetables under protected cultivation conditions, achieving an increase in yields and a decrease in nematode populations. This work supports the results obtained from the selection of promising strains given the type of existing soil. In addition, it provides practical elements that make up a modified methodology for the use of AMF + MTW in the management of nematodes in intensive vegetable production systems under protected cultivation conditions.
Departamento de Agronomía, Facultad de Ingeniería Química y Agronomía, University of Oriente, Santiago de Cuba, Cuba
Siannah María Más Diego
Centro Nacional de Electromagnetismo Aplicado, University of Oriente, Santiago de Cuba, Cuba
Gerardo Montero Limonta
Departamento de Agronomía, Facultad de Ingeniería Química y Agronomía, University of Oriente, Santiago de Cuba, Cuba
Miriela Rizo Mustelier
Departamento de Agronomía, Facultad de Ingeniería Química y Agronomía, University of Oriente, Santiago de Cuba, Cuba
*Address all correspondence to: dvuelta@uo.edu.cu
1. Introduction
Modern, industrial, conventional or green revolution agriculture is in crisis and affects the economy of all countries in the world. The effects are socioeconomic and ecological in nature, which means that producers cannot cope with the high price of modern products and technologies. On the other hand, its effect is manifested in the progressive decrease in agricultural yields, in addition to the loss of biodiversity [1, 2]. The indiscriminate use of pesticides affects the population of beneficial insects and has caused pest resistance. An attempt has been made to alleviate this situation with the mixture of more toxic products that, although they can temporarily solve the problem, result in new resistance, resurgence, outbreak of secondary pests and a decrease in natural enemies [3].
Plant-parasitic nematodes are associated with effects on the development and production of agricultural crops, being recognized as one of the limiting factors in yields [4]. Among root-knot nematodes such as Meloidogyne incognita (Kofoid and White), Chitwood is the species most commonly found on vegetables. Plant-parasitic nematodes are associated with effects on the development and production of agricultural crops, being recognized as one of the limiting factors in yields [4, 5], causing damage to numerous crops of agricultural interest.
The most important species in Cuba is M. incognita, and for its management various practices are used that include the use of biological control agents [6], and it constitutes one of the most important phytosanitary problems of horticultural crops [7]. The root-knot nematode, Meloidogyne incognita, is an emergent nematode in protected conditions. This nematode can cause chlorosis, stunted growth, and reduced host plant yields. Root-knot nematodes severely affect the root system of the plant by inducing the formation of specialized nutritional cells, that is, giant cells in the vascular tissues. Recently, this nematode has been considered as a global threat in protected cultivation technology [8].
Farmers apply pesticides due to the need to protect their crops, without taking into account the toxicity of the product, which leads to contamination of crops by chemical residues, which has repercussions on the soil, air and water [9]. Currently, alternatives to chemical control have been sought with the use of microorganisms and cultural practices that allow integrated management of nematodes [10].
Furthermore, it is important to point out the need to consider the health of plants and their microbiome within the “one health” concept, closely linked to the health of the environment, soil, animals and people. In the context of agroecological production based on the sustainable management of natural resources, integrated pest management has been promoted to reduce the use of pesticides and mitigate negative effects on human and environmental health. For this, biological control has contributed to achieving this goal [11].
Biological control applies to the use of living organisms, as AMF, to suppress the population density or impact of a specific pest organism. In this case, biological control of nematodes is manifested by the regulation of nematode populations or their damage through the action of antagonistic organisms, and this occurs naturally or through manipulation of the environment or the introduction of antagonists [12].
Arbuscular mycorrhizal fungi (AMF) constitute a functional group that is important in the soil biota, as it favors the improvement of the structure, the multifunctionality of the ecosystem and the productive development of crops [13]. The importance of the study of AMF lies in the fact that there is evidence of its association with more than 80% of plants, as well as its role in protecting the root system from phytopathogenic agents, promoting mineral nutrition and facilitating water absorption, which contributes to the improvement of plant growth and survival [14].
Effective management of mycorrhizal associations may be a means to increase the productivity of agricultural crops, as AMF are vital components of the rhizosphere of these crops. Plants maintain a close relationship through a network of interconnected hyphae that increase the area of soil explored by roots, improve their structure and facilitate the absorption of nutrients and water, among other essential functions. The effects of these microorganisms not only have consequences on development and nutrition but can also increase the natural resistance of plants in situations of biotic (pathogenic) or abiotic (water or saline stress) imbalances [15].
Although it can be applied in the field, with various restrictions, the main application of these fungi is in those systems that require a nursery phase, before they are released into the field. The management or establishment of the biotechnology represented by arbuscular mycorrhizal fungi (AMF) must be carried out in the first phases of the growth and/or establishment of the plants, so that they receive the greatest benefit prior to their commercial exploitation in orchards [16]. There are several studies on the effects of AMF on plants attacked by nematodes [17], in most of which a decrease in the severity of the infestation is observed. The mechanisms are related to the contribution of resistance to the plant and in general depend on changes in the host’s physiology. Changes in root exudates would modify the attraction of nematodes to the roots [18].
Mycorrhiza-forming fungi provide innumerable benefits for the plant and services for the functioning of the ecosystem, contribute to plant nutrition, health and water balance and generate a network of mycelium in the soil, through which the roots communicate with each other and share information, water and nutrients. This network is a valuable way to conserve soil carbon and nutrients (these are considered ecosystem services). Furthermore, mycorrhizae are involved in the production of a binding substance for soil particles that favors the formation of aggregates and reduces the risk of erosion [19].
The use of the magnetic field (CM) influences microbial growth, either inhibiting it or stimulating it, and this depends on the intensity and time of exposure. The effect of CM on microbial growth is not only one, and it can be classified as unobservable, inhibitory and stimulatory [20].
In Cuba, there is the National Center of Applied Magnetism (CNEA) which is a multidisciplinary institution with the purpose of researching and applying magnetic and electromagnetic fields in industry, medicine, agriculture and the environment, and in its work, it has carried out numerous investigations in agriculture demonstrating the positive effects of magnetically treated water (MTW) on crops [21, 22, 23]. There are few studies that propose the use of MTW to combat pests, specifically nematodes, as plants subjected to magnetically treated water tend to behave tolerant to these pathogens [24, 25, 26, 27], but information on its direct effect on nematode control is limited.
The technology of protected cultivation houses is a form of intensive agriculture that can contribute to local food security, its advantages are protection against extreme weather conditions, obtaining permanent crops through continuous sowing, better quality of the harvest, reduction of soil erosion, planting of selected materials, significant increase in yield, decrease in pest attack, due to physical barriers such as meshes, more efficient use of the growing area and opportunity to access new markets, due to the improvement in the safety of the crops products [28].
However, the high incidence of nematodes causes considerable damage to the production of protected crops. This situation limits producers from obtaining high yields from their crops and also implies a high cost for the use of chemical nematocides. Therefore, the objective was to evaluate the management of nematodes with the combined application of AMF and MTW, which allows reducing the impact to acceptable levels in protected cultivation conditions.
2. Use of arbuscular mycorrhizal fungi and magnetically treated water for the management of nematodes in protected culture conditions
The research was carried out in the municipality of Santiago de Cuba in the Protected Crop Unit in Campo Antena, of the Socialist State Company América Libre, and was carried out in the period from February 2018 to March 2021. The entity where the research was developed is located on the Santiago de Cuba; reference coordinate (X: 60757330 Y: 156332149). It has an area of 1.52 ha, with 23 cultivation houses that are used for the production of vegetables, such as pepper, tomato, chard and cucumber during the experiment period.
For the application of the treatments, a high-frequency localized irrigation system was implemented, which allowed the immediate application of water after magnetization. The experiments used external permanent magnet or static magnetic field devices, designed at the National Center for Applied Electromagnetism (CNEA).
A part of the water circulation pipe was placed at the two poles of the magnetizer, and the direction of water flow is perpendicular to the direction of the magnetic induction line. The magnetic inductions were set at 0.05–0.07 Tesla (T) and 0.1–0.12 T. The treatment was carried out at the time of watering the plants, throughout the crop cycle until development of the fruits. Irrigation was carried out once a day through a drip system, for 30 minutes. The conditions established for irrigation considered the water speed (1.4–1.6 m s−1) and the pump flow (2.54–2.91 m3 h−1). The treated water began to be used immediately after transplanting and until the end of the experiment.
The experimental design was completely randomized, with four replications and 12 treatments.
Three strains of AMF were used in the research:
Rhizophagus irregularis (Błaszk., Wubet, Renker & Buscot), C. Walker & A. Schüßler.
Funneliformis mosseae (T.H. Nicolson & Gerd.), C. Walker & A. Schüßler.
Glomus cubense (Y. Rodr. Dalpé).
2.1 Forms of seed inoculation
For the treatment of the seeds, a homogeneous paste was prepared with water, in a proportion of 1 kg of each inoculum for every 10 kg of seed, and the seed was covered with it until it was completely covered according to the methodology [29]. The inoculated mixture was allowed to rest in the shade for 10 minutes, and then the seedbed was established.
The seeds were sown by treatments in polyfoam trays (expanded polyethylene), each with 150 truncated pyramidal alveoli, previously washed with soap and water and subsequent disinfection by immersion in chlorinated solution (concentration) or agricultural iodine (5 mL/L of water) [30]. The substrate was composed of worm castings (80%) and peat (20%).
Sowing was carried out manually, by depositing two to three seeds per socket at a depth of 2–3 mm. Subsequently, the trays were placed in the dark for three days. Then, they were moved to a protected area with a flexible polyethylene cover, anti-bemisia lateral meshes, and separated from the ground between 60 and 100 cm. Daily localized irrigation or with a watering can was maintained. Table 1 shows the description of the treatments used in this research.
Treatments
1
Control without inoculation of AMF
2
Culture without inoculation of AMF + MTW (0.05–0.07 T)
3
Culture without inoculation of AMF + MTW (0.1–0.12 T)
4
Rhizophagus irregularis
5
Funneliformis mosseae
6
Glomus cubense
7
Rhizophagus irregularis + MTW (0.05–0.07 T)
8
Rhizophagus irregularis + MTW (0.1–0.12 T)
9
Funneliformis mosseae + MTW (0.05–0.07 T)
10
Funneliformis mosseae + MTW (0.1–0.12 T)
11
Glomus cubense + MTW (0.05–0.07 T)
12
Glomus cubense + MTW (0.1–0.12 T)
Table 1.
Description of the treatments.
2.2 Tomato cultivation (Solanum lycopersicum L.)
The crop used was tomato (hybrid variety HA 3057) of determined growth. It was evaluated from transplant to final production. Four houses of 0.080 ha were used for a total experimental area of 0.22 ha, with a duration of 120 days. The planting frame was 1.04 m × 0.30 m.
2.3 The cultivation of pepper (Capsicum annuum L.)
The crop used was the Locumone hybrid variety pepper. It was evaluated from transplantation to final production. Four houses of 0.08 ha were used as the experimental area for a total experimental area of 0.32 ha. The duration of the crop cycle was 120 days.
2.4 Cultivation of cucumber (Cucumis sativus L.)
I grow indeterminate growing cucumber. Hybrid Variety YA 2005. The stage from transplanting root balls to final production was evaluated. The duration of the crop cycle was 120 days. The planting frame was 1.5 m × 0.30 m.
2.5 The cultivation of chard (Beta vulgaris var. cicla L.)
For this experiment, chard (improved variety PK – 7) was used as a crop. The period evaluated was from sowing to final production. Four cultivation houses of 0.054 ha were used for a total experimental area of 0.22 ha. The duration of the crop cycle was 45 days. The planting distance was 1.04 m × 0.25 m × 0.25 m from ridge to double furrow and 0.25 m from nose (two or three seeds per row). Optimum population density was 20–30 plants/m2 at the bottom of the furrow.
For the agronomic management of the crops, we proceeded as stipulated by the Manual for the Protected Production of Vegetables [31].
2.6 Statistical analysis
For the comparison of treatments, simple classification analysis of variance was performed, and the means were compared by Tukey’s multiple range test at a 5% probability. For non-parametric evaluations, the Kruskal-Wallis test was used. For each analysis, the assumptions of normality and homogeneity of variance were checked (Bartlett’s test and Kolmogorov-Smirnov test, respectively) in each variable evaluated through the statistical program R commander version 4.1.1.
3. Evaluation of the application of arbuscular mycorrhizal fungi and magnetically treated water for the management of nematodes in protected culture conditions
Samples were processed in the provincial plant health laboratory, and the nematological analysis carried out on soil and roots showed densities of 40 Juveniles in their second stage (J2) per 100 cm−3 in soil and 130 J2 10 g−1 in roots. Once the perineal patterns were studied, the presence of the nematode Meloidogyne incognita was determined. Although there is the possibility of finding variability in morphometric parameters within the same species, which may be linked to environmental factors that directly influence the development of nematode populations, this way of identifying species is recognized by researchers [32].
3.1 Tomato cultivation (Solanum lycopersicum)
The results revealed that the use of AMF with pre-sowing inoculation is a practice with positive results; as the levels of pest infestation were reduced, the performance of the crop is even better when the AMF were combined (specifically G. cubense and R. irregularis) with MTW. G. cubense + MTW (0.1–0.12 T) provides the highest values of the means, although it does not statistically surpass G. cubense + MTW (0.05–0.07 T) (Figure 1a–c). This is because in addition to the effects exerted individually by both practices, it is added that, together, they show greater potential for crop development and a more effective response against nematode attacks.
Figure 1.
Root galling index (a). Meloidogyne incognita egg mass, number of females and juveniles J2 (b). Percentage of radical colonization of AMF (c) for tomato cultivation. 1: control without AMF inoculation; 2: culture without AMF + MTW inoculation (0.05–0.07 T); 3: culture without inoculation of AMF + MTW (0.1–0.12 T); 4: Rhizophagus irregularis; 5: Funneliformis mosseae; 6: Glomus cubense; 7: Rhizophagus irregularis + MTW (0.05–0.07 T); 8: Rhizophagus irregularis + MTW (0.1–0.12 T); 9: Funneliformis mosseae + MTW (0.05–0.07 T); 10: Funneliformis mosseae + MTW (0.1–0.12 T); 11: Glomus cubense + MTW (0.05–0.07 T); 12: Glomus cubense + MTW (0.1–0.12 T).
Inoculation with AMF of plants that are subsequently infected by Meloidogyne allows nutrient uptake, plant growth, production of bioactive compounds and fruit production to increase. These benefits can extend over several cycles. In addition, it promotes complex physiological changes that can decrease the attraction of nematodes to the root. These physiological changes include the activation of defense mechanisms (elicitation), including increased activity of defense enzymes, increased production of nematicidal compounds, increased root lignification and alteration in cell wall composition, which can reduce the number of nematodes that penetrate and infect the roots [33].
The three AMF strains presented fungal functioning in relation to the control without inoculation and the treatments without inoculation + MTW. The trend is shown toward higher values of percentage of root colonization for Glomus cubense and Rhizophagus irregularis in combination with MTW, respectively, highlighting Glomus cubense + MTW (0.1–0.12 T). This may be due to the fact that, in the presence of MTW, the growth of AMF is stimulated, and at the same time, the plant’s defense mechanisms are favored.
In the coffee plant (Coffea arabica) crop, AMF inoculation increases the root system and can reduce susceptibility and damage caused by nematodes [17]. The existence of mechanisms such as greater absorption of nutrients, alteration of root morphology, competition for space and nutrients and induction of systemic resistance of the plant can contribute to improving the response of the plant to pest attack [34].
This result is determined by the pH in water (5.8–7.3) in which this process was developed since it was influenced by the neutralization of the bicarbonates contained in the irrigation water, which is more suitable for the normal development of the strains. The values could be given by the ability of efficient AMF strains to establish a molecular dialog with the macrosymbiont in close relationship with the edaphic environment of the soil and stimulate higher percentages of root occupancy. It is necessary to highlight the importance of the edaphic environment and pH on the effectiveness of AMF strains [35].
Mycorrhizae allow plants to absorb more phosphorus, nitrogen and water, improving their resistance to extreme environmental conditions. It also allows you to hinder the attack of pathogens that cause root diseases, protect the environment and completely avoid the use of agrochemicals. For its part, biocontrol using AMF arises from the need to look for alternatives that ensure protection for agriculture but at the same time do not have consequences on the environment. This has driven the search and development of new options for chemical agents [36].
It can be seen that considering the effects of AMF on plants attacked by nematodes, in most cases, a decrease in the severity of the infestation is observed, possibly due to the fact that plant-parasitic nematodes are antagonists, obligate biotrophs, like AMF. Likewise, it was proven that there is an antagonistic relationship caused by arbuscular mycorrhizal fungi toward pathogens and that the reduction of damage due to their attacks is not based solely on a greater number of roots [37, 38].
Numerous mechanisms are manifested when AMF promote biocontrol. They can be grouped into two: those that include a direct effect of the fungus on the pathogen such as competition for nutrients, space and infection/colonization sites and those that include indirect effects on the pathogen such as improvement in host nutrient uptake, changes in the architecture of the roots, changes in the interaction of rhizosphere microorganisms and activation of plant defense mechanisms [39].
The different mechanisms cannot be considered completely independent of each other, that is, the resulting biocontrol comes from a combination of several of them. Mechanisms include increased plant tolerance, direct competition for nutrients and space, induced systemic resistance and rhizosphere interactions [40].
Plants have defense systems against various stresses through the production of hormones, of small molecular weight, to activate their response/attack arsenal, and adapt to the new adverse condition. Salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) are hormones which modulate the activation of defense genes for the immediate response against biotic stress (bacteria, fungi, insects, etc.) In general, against the attack of a biotrophic living pathogen (that feeds on living cells), plants defend themselves producing SA and alerting systemically to distal sites such as leaves, flowers and fruits (SAR), and this can be induced by AMF [41].
Plants are attacked by a multitude of pathogens and pests, some of which cause epidemics that threaten food security [42]. After infection by a pathogen, the colonization of roots with beneficial microorganisms such as AMF allows many plants to establish a physiological situation called “activated” or “primed” state. This allows them to respond more quickly and/or effectively when they are re-exposed to biotic or abiotic stress, a characteristic that is frequently associated with greater resistance to diseases.
There are also studies [43] that show that MTW provides greater tolerance to crop plants against pathogen attack. A decrease in the nematode root-knot index is also reported due to the influence of MTW, which improves the fitness of the plant that serves as host, as the plant has good vigor due to greater availability of nutrients [24]. Furthermore, in another investigation [22], they managed to increase yields by more than 10% with the use of magnetically treated water in tomato cultivation under protected cultivation house conditions.
Although the application of water treated with a magnetic field reduces the galling rate of Meloidogyne, it cannot be classified as a method of nematode control, as no mechanism has been found that can exert any control over the populations of the phytonematode, constituting a non-conventional alternative for phytosanitary protection against phytonematodes of the genus Meloidogyne due to the protection it confers on the crop [24].
Regarding the mechanisms that participate in this biological protection, they are not yet fully characterized. Other authors [44] argue that the effective “biological protection” against root pathogens, granted by AMF, is probably a consequence of several indirect mechanisms since they do not interact directly with pathogens through antagonism, antibiosis or parasitism. In the literature, [45, 46] propose several mechanisms: such as compensation of damage due to the better nutritional status of the host, anatomical and morphological changes of the root system that hinder the penetration of the pathogen, competition for colonization and infestation sites, competition for photosynthates, deposition in the rhizosphere of nematicidal and nematostatic metabolites, changes in soil microbial populations and activation of the plant defense response, induced resistance.
Various investigations have shown that the use of inoculation with AMF facilitates the absorption of water and nutrients, improves the physiological performance of crops attacked by nematodes, reduces stress and reduces the damage caused by this pest, which is why it is considered as a biological tool to be considered in a management plan [47, 48]. Furthermore, due to its characteristics, tomato tends to be frequently attacked by this pest [49, 50]. Plants interact with microorganisms, and these interactions have a notable impact on plant health. The oldest and most widespread mutualistic symbiosis between plants and microorganisms is that established with mycorrhizal fungi. Consequently, plants have evolved mechanisms to restrict pathogenic interactions while promoting mutualistic relationships.
The efficiency of these mechanisms depends on the adequate and timely recognition of the interacting fungi and the strict regulation of the immune responses triggered to control (promote or contain) fungal colonization. For example, nitric oxide (NO) acts as an intra- and intercellular signaling molecule. Involved in the regulation of many cellular functions in different species, NO produced after the recognition of pathogens by plants is part of the signaling cascades that trigger the expression of defense genes, the production of secondary metabolites and finally, hypersensitivity (HR) and systemic-acquired resistance (SAR) [51].
3.2 The cultivation of pepper (Capsicum annuum)
At the beginning of the investigation, the nematological analysis of the soil was carried out, which resulted in grade 1 of infestation; however, over the course of the experience, the control increased to grade 2.6, while treatments 2 and 3 without AMF inoculation presented grade 2, the other treatments (with AMF inoculation) showed galling rates below grade 2, the two treatments of G. cubense + MTW are the ones with the lowest rate with statistical differences to the other treatments which constitute a positive effect by providing the AMF and the magnetically treated water with greater tolerance to the crop to face the attack of nematodes (Figure 2a–c). The same behavior is observed in the population indicators of the nematode, as the treatments with G. cubense + MTW have the lowest average values, which demonstrate that the synergistic action of AMF and MTW causes a decrease in nematode populations.
Figure 2.
Root galling index (a). Meloidogyne incognita egg mass, number of females and juveniles J2 (b). Percentage of radical colonization of AMF (c) for the pepper crop. 1: control without AMF inoculation; 2: culture without AMF + MTW inoculation (0.05–0.07 T); 3: culture without inoculation of AMF + MTW (0.1–0.12 T); 4: Rhizophagus irregularis; 5: Funneliformis mosseae; 6: Glomus cubense; 7: Rhizophagus irregularis + MTW (0.05–0.07 T); 8: Rhizophagus irregularis + MTW (0.1–0.12 T); 9: Funneliformis mosseae + MTW (0.05–0.07 T); 10: Funneliformis mosseae + MTW (0.1–0.12 T); 11: Glomus cubense + MTW (0.05–0.07 T); 12: Glomus cubense + MTW (0.1–0.12 T).
Authors such as in [52] propose that mycorrhizae, when establishing symbiosis with the roots of plants, emit their hyphae, which constitutes an elongation of the root system, providing it with a more favorable water and nutritional state compared to plants that are not mycorrhizal, which allows them to be able to face the impact of pathogens in a better situation. In his research [53], he points out that inoculated arbuscular mycorrhizal fungi managed to reduce the damage induced by the nematode, in C. annuum, with control effects superior to the chemical nematicide oxamil, improving the growth and agronomic vigor of the plants.
They also associate with plants and constitute a mutualistic relationship which is used in horticultural production, where they are implemented as a strategy to improve crop nutrition and reduce abiotic stress, and as biological control agents of root pathogens, they compete with nematodes for spaces in the root, modify the chemical composition of radical exudates that inhibits the penetration of J2 and activate defense mechanisms in plants [54, 55].
Regarding the percentage of radical colonization, the Glomus cubense + MTW treatment with the highest magnetic induction has the best result, statistically surpassing the other treatments, followed by the other combination of Glomus cubense and MTW, which is the control without inoculation of lower value than the average. Similar results were obtained [56], when evaluating the effectiveness of these strains in the cultivation of pepper in protected conditions, and for the same type of soil at pH levels of 7.2, the Glomus cubense strain stands out as the one that performed best.
It is suggested that the minimum percentage of AMF colonization should be greater than 40% to favor the symbiotic relationship with the plant and serve as a biological indicator of soil quality. The values could be given by the ability of efficient AMF strains to establish a molecular dialog with the macrosymbiont that is closely related to the type of soil and the pH level [57].
For its part, the authors of [58] demonstrated that treatments inoculated with Glomus cubense showed significantly higher percentages of mycorrhizal colonization, visual density and number of spores in the rhizosphere than those not inoculated for brown soils without carbonates. The above corroborates the effectiveness of this strain to achieve, at least under the conditions of this experiment, higher radical occupancy levels than native AMF. All these are added to the biostimulant effect of magnetically treated water that enhances the development of mycorrhization.
In a research carried out in pepper with another strain of AMF [59], they managed to reduce the population of nematodes, and with this, the reduction of damage to the roots, the reduction of the reproduction of the nematode and, in turn, the AMF favored the growth of the plants.
AMF have frequently been considered as a method to help the host plant attenuate damage caused by pathogens and predators [60]. In a study carried out by these authors, they evaluated the effects of a commercial AMF inoculum against Meloidogyne incognita in pepper. Under controlled conditions, the results were that the association of mycorrhizae decreased the development of M. incognita and improved tolerance to nematode infestation. These researchers suggest rapid mycorrhization of plants is essential to achieve protective effects against biotic stress.
The root-knot nematode Meloidogyne incognita causes galls on the roots of pepper resulting in yield losses. Although they recognize that the control of this pest in pepper with chemical nematicides is effective, there are environmental and health concerns that constitute serious drawbacks and limit their possible use [61]. They used four species of AMF in the cultivation of pepper in greenhouse conditions. They suggest using arbuscular mycorrhizal fungi to control this nematode as it may represent a solution to inhibit infestation by nematodes, improving the growth and fruit yield of this crop. Based on the results obtained, these AMF species could be used as biocontrol agents for M. incognita.
AMF are capable of improving plant growth by increasing the absorption of nutrients in exchange for photosynthetic carbon from their hosts, achieving successful biocontrol of nematodes as they reduce their population and reduce the number of galls, plants respond favorably in all parameters of growth and development, as well as showing an increase in yield [62].
It is generally recognized that arbuscular mycorrhizal fungi promote plant growth. Furthermore, they induce a defense response by plants against soil-borne pathogens such as plant-parasitic nematodes [63].
With mycorrhization, constant increases in plant weight are achieved, and it is recommended that root colonization by AMF should be established before nematode attack to ensure that prepared plants trigger effective immune action response capable of limiting the damage caused by infection [64]. Therefore, the optimal doses of the formulations, the age of the plant, the time between AMF inoculation and exposure to nematodes, soil type, growing conditions, etc., should be investigated and standardized to make of AMF treatment a successful and widespread component of integrated pest management in conventional and organic agriculture.
3.3 Cultivation of cucumber (Cucumis sativus)
When analyzing Figure 3a–c, which shows the Meloidogyne incognita galling index in each treatment in the cucumber crop and the percentage of root colonization by AMF, it can be seen that the treatments with AMF inoculation present the best behavior in the presence of the nematode M. incognita and manage to reduce galling to 1.5 in the case of the combination G. cubense + MTW, which statistically surpasses the control without inoculation, although they do not present significant differences with the other treatments. In the case of the percentage of root colonization, the behavior of the treatments with AMF inoculation statistically surpassed the treatments that do not present inoculation; however, the treatments with the G. cubense + MTW strain were the ones with the best results, although there were no differences among the inductions under study.
Figure 3.
Root galling index (a). Meloidogyne incognita egg mass, number of females and juveniles J2 (b). Percentage of radical colonization of AMF (c) for cucumber cultivation. 1: control without AMF inoculation; 2: culture without AMF + MTW inoculation (0.05–0.07 T); 3: culture without inoculation of AMF + MTW (0.1–0.12 T); 4: Rhizophagus irregularis; 5: Funneliformis mosseae; 6: Glomus cubense; 7: Rhizophagus irregularis + MTW (0.05–0.07 T); 8: Rhizophagus irregularis + MTW (0.1–0.12 T); 9: Funneliformis mosseae + MTW (0.05–0.07 T); 10: Funneliformis mosseae + MTW (0.1–0.12 T); 11: Glomus cubense + MTW (0.05–0.07 T); 12: Glomus cubense + MTW (0.1–0.12 T).
The use of AMF as an alternative for the control of root pathogens in horticultural crops is an area of study little explored in several countries. Among the main factors that are considered at the time of evaluation are the effect of AMF on nematodes to reduce their reproductive capacity, such as the estimate of reduction of eggs and females by the nematode and the severity of the damage it induces in the roots, where the number of galls and their arrangement on the root are considered, as well as their ability to promote crop growth considering this parasitic load [65].
AMF can reduce nematode development. Sustainable agriculture is currently promoted throughout the world, which guarantees human food security without negatively impacting the environment. AMF, naturally present in the soil and acting as biostimulators and bioprotectors, can be very beneficial for sustainable agriculture, maintaining plant production and reducing pathogens without harming the environment. Given the importance of sustainable crop management and the lack of studies specifically addressing the interactions of AMF and Meloidogyne, it is important to conduct research [33].
The biocontrol characteristics of arbuscular mycorrhizal fungi (AMF) against root pathogens are known, but information on the mode of biocontrol action and biocontrol efficiency of AMF species is limited. In general, it is considered that the biocontrol characteristics of AMF in terms of tolerance induction depend on the AMF species. These differential traits of AMF should be considered when developing biocontrol strategies against cucumber root pathogens [66].
Treatments inoculated with Glomus cubense showed significantly higher percentages of mycorrhizal colonization in the rhizosphere than those not inoculated for brown soils without carbonates [67]. The above corroborates the effectiveness of this strain to achieve, at least under the conditions of this experiment, higher radical occupancy levels than native AMF. Other authors [68] state that another group of potential fungi in the biocontrol of nematodes is that of arbuscular mycorrhizal fungi (AMF), which function as obligate symbionts of plant roots. The plant provides photosynthetic carbon for symbionts, while helping roots absorb more nutrients and stimulating both root growth and leaf structure.
Furthermore, AMF often compete for nutrition and space with these soil pathogens and induce systemic plant resistance. Also, the authors of [69, 70, 71] state that plants can still be immunized against nematode attacks through beneficial microorganisms of the rhizosphere, such as arbuscular mycorrhizal fungi that can induce systemic responses of acquired resistance against nematodes.
3.4 The cultivation of chard (Beta vulgaris var. cicla)
When analyzing Figure 4a–c, it can be seen that, in the control (where mycorrhizae was not applied), there was an increase in the nematode galling index with an average of 3.50, if it is considered that the initial galling index was 3. The two treatments consisting of the application of MTW (with the two inductions under study) also showed effects by nematodes; however, in the rest of the treatments, the means were 0, which statistically exceeds the control and the treatments without AMF + MTW inoculation.
Figure 4.
Root galling index (a). Meloidogyne incognita egg mass, number of females and juveniles J2 (b). Percentage of radical colonization of AMF (c) for the Swiss chard crop. 1: control without AMF inoculation; 2: culture without AMF + MTW inoculation (0.05–0.07 T); 3: culture without inoculation of AMF + MTW (0.1–0.12 T); 4: Rhizophagus irregularis; 5: Funneliformis mosseae; 6: Glomus cubense; 7: Rhizophagus irregularis + MTW (0.05–0.07 T); 8: Rhizophagus irregularis + MTW (0.1–0.12 T); 9: Funneliformis mosseae + MTW (0.05–0.07 T); 10: Funneliformis mosseae + MTW (0.1–0.12 T); 11: Glomus cubense + MTW (0.05–0.07 T); 12: Glomus cubense + MTW (0.1–0.12 T).
This seems to be motivated by the protective effect exerted by mycorrhizae in their symbiosis with plant roots. It is also proposed that the action of AMF minimizes the physiological damage caused by nematodes [72]. The increase in the percentage of root colonization could be caused by the actions exerted by AMF in the increase and absorption of nutrients available for plants. This increase could be the result of competition between AMF and nematodes for root space. This would stimulate the growth of intraradical mycelium, favor its development and increase colonization levels.
With the use of arbuscular mycorrhizal fungi (AMF), it is inferred that the participation of these associated with agricultural crops can influence the dynamics of mineral elements such as copper, zinc, iron and manganese, reflected in the concentration in their plant tissue through the homeostasis of heavy metals and their transcriptional activity, which is why it biofortifies vegetables, especially leafy ones such as chard, and this adds to the already known benefits that these microorganisms provide [73].
Antagonistic microorganisms such as AMF have mechanisms that regulate nematode population densities, so culture-independent and culture-dependent approaches have been adopted and used in several studies to analyze the diversity of bacteria or fungi associated with nematode genera plant parasites [74].
Related to this [75], it is stated that soil biota performs a series of functions that are essential for the integrity and productivity of agricultural systems, which is why it constitutes a fundamental part of terrestrial biodiversity. The composition of this biota can be manipulated, almost always temporarily, to maintain and increase the productivity of a soil.
AMF in combination with MTW act on the plant and enhance the induced systemic resistance. During their life, plants interact with numerous pests, which have different modes of attack and life forms. The primary immune response evolved toward the recognition of organisms that interact with the plant and the translation of such recognition into defense responses specifically directed against the invading organism. This type of resistance often acts systemically and is effective against a wide spectrum of pests [76].
The use of beneficial microorganisms is a viable alternative for production since they constitute an economically attractive and ecologically acceptable medium. They reduce external inputs, improve the quantity and quality of internal resources, as well as guarantee greater efficiency in the use of mineral fertilizers [77].
AMF considerably reduces the formation of galls and the reproductive capacity of the nematode in tomato, pepper, cucumber and chard crops.
Irrigation with MTW enhances the positive effects of AMF in the management of M. incognita, which demonstrates that its combined use can be a beneficial alternative for the management of nematodes in crops grown under protected cultivation conditions.
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Daniel Rafael Vuelta Lorenzo, Siannah María Más Diego, Gerardo Montero Limonta and Miriela Rizo Mustelier
Submitted: 28 May 2024Reviewed: 04 June 2024Published: 02 September 2024
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