Introductory Chapter: Mycorrhizal Fungi – A Current Overview on Agricultural Productivity and Soil Health

1. Introduction

It is well known that near the roots of plants, at the zone called rhizosphere, there are several types of microorganisms, whether pathogenic or organic matter decomposing organisms (saprophytes,) or even those organisms that live in symbiosis with the plant as is the case of mycorrhizae [1].

The mycorrhiza is the positive association between the arbuscular mycorrhizal fungi (AMF) and roots of plants, which is named as mutualistic association. Mutualism is an ecological relationship between individuals of different species, in which both benefit from the interaction. Since it occurs among individuals of different species, it is a relationship called interspecific, and due to it benefits everyone involved, it is called a harmonic relationship. As its name says “mycorrhiza” comes from fungi and the “rrizo” that are the roots. Recently, these associations between fungi and roots have drawn attention as a scientific research topic when was discovered the ability of this mycorrhiza in increasing the absorption of nutrients by plants. As an example, the researchers have found a great ability of these fungi to increase the uptake of phosphorus by plants, especially in high-leached and poor soils. It is important to understand that the mycorrhiza will not increase the phosphorus content in the soil, as others solubilizing microorganisms do, these fungi will help enhance the absorption by roots as it will increase the specific surface area of that plant [2]. It is important to have not only the phosphorous (P) but also all essential elements (nutrients) available in the soil so that they can perform their effect in nourishing the plant. For this, and other facts, it is important to combine the biological with the chemical factors in soil for a healthier and more balanced environment.

The AMF are classified into two major groups. The first one is the ectomycorrhizae (ECM), which are those fungi that will not penetrate the plant or will not penetrate the roots of the plants. They will live there around the plant and over the roots, forming a kind of “ball” (called mantle) and Hartig net. This mantle will not only have the function of absorbing nutrients it also protects against some pathogens. This type of ectomycorrhizae association will happen mainly in forest species [2]. Another classification of mycorrhizae is endomycorrhizae. They have the ability to penetrate the roots of plants through the hyphae, which form structures within the cortical cells and also grow intercellularly. Inside the cell, those hyphae swell forming a kind of nutrient storage organ, which those elements will be used in the metabolism of that plant [1]. Therefore, the AMF receives carbohydrates provided by roots while the fungus transfers nutrients and water to the plant roots [3].

The endomycorrhizae occur mainly in crops of agricultural interest. These species are symbiotic obligatory since they need this lifestyle to survive. So, this kind of fungus will always have its host root being the connection between the plant’s roots and soil. There are several species of fungi to establish this kind of connection and association, in which each species has its own ability to absorb a specific nutrient. Thus, depending on the species, they will absorb a particular nutrient or much more one kind of nutrient than others [1].

The soil system is interesting to have large varieties of these microorganisms, as each one will bring different benefits to the plants according to their specificities. It is important to emphasize that human being can directly or indirectly induce mycorrhizal survival and abundance in the crop (Hartmann et al., [4]). So, as we are working with microorganisms, which are living organisms, it is necessary to give specific conditions for their proper establishment in the soil. Inoculating various beneficial microorganisms such as mycorrhizal fungi in an attempt to bring benefits to the crop without appropriate and healthy soil management will be a waste of time and an expense. We cannot forget that soil health is the continued capacity of soil to function as a vital living ecosystem that sustains plants, animals and humans, and connects agricultural and soil science to policy, thus soil health is not only focused on crop production, but also includes the role of soil in water quality, climate change, and human health [5]. As we can see, the soil is multifunctional and quite complex, so we must seek its most complete balance.

The soil management needs to be adequate for full-plant growth. For example, the excess of fertilizer and pesticides, and low addition of organic matter will affect the soil health, since the microorganisms are directly affected. Also, the monocrop causes negative impacts on the soil microorganisms, since the input of organic residue is limited from a single crop. It is important to keep in mind that the soil is alive and its biological compartment is as important as the chemical and physical factors [2]. Thus, based on what has been discussed, this chapter covers the main positive points under the symbiotic association between mycorrhizal fungi and agricultural crops, in addition, we discussed the main agronomic practices that negatively and positively impact the soil quality.

2. Symbiotic association between mycorrhizal fungi and agricultural crops

Crop production is the first step to produce foods, so it is essential to study the factors that directly affect this production, such as the biological ones. Initially, it is important to mention that mycorrhizal fungi are one of the varieties of fungi of extreme importance for agricultural production due to their great contribution to the nutrient absorption by plants and several other functions. It is known that some fungi species can interact with others organisms leading to the establishment of symbiotic associations, and mycorrhizae are one of these associations [6].

When a fungus establishes an association with the roots of certain plant species, we have the so-called mycorrhizae, which are divided into two major categories: ectomycorrhizae and endomycorrhizae. This classification is based according to the morphological and anatomical aspects of the fungal colonization of plant roots [6]. We can observe this difference in Figure 1.

Figure 1.

Ectomycorrhizae and endomycorrhizae scheme of colonization of roots. Source: [7].

Ectomycorrhizae are formed mainly by basidiomycetes and ascomycete fungi, representing about 3% of phanerogams [8], which phanerogams is mainly a subkingdom of the plant kingdom which produce seeds to reproduce. Whereas, in colder regions with cooler temperate, around 90% of forest species present mutualism with this fungus [8].

In tropical regions like Brazil, ectomycorrhizae are more studied and found mainly on economically exploited species such as pine, eucalyptus, and acacia. In ectomycorrhizae, the fungi associated with the root do not penetrate the living cells of the root; and the hyphae grow between the cells of the root cortex, forming a characteristic structure, the Hartig’s web (Figure 1). The roots of plants associated with ectomycorrhizae are devoid of hairs and their function is performed by fungal hyphae [9].

Endomycorrhizae are more common than ectomycorrhizae and occur in about 80% of vascular plants. The fungi that best represent this association are zygomycetes, which is a class of fungi with more than 1000 known species. The Endomycorrhizae penetrate the cortical cells of the plant roots, where they form very branched structures and chlamydospore (Figure 1), which is the defined as a thick-walled, non-deciduous, intercalary or terminal, asexual spore formed by the rounding of a cell or cells whose primary function is perennation, not dissemination [10]. Their hyphae extend for several centimeters in the soil, significantly increasing the amount of nutrients and phosphates essential for plant development.

Many studies have reported that root colonization by mycorrhizal fungi significantly increases the productivity of various plants in low-fertility soils [9]. This is due to the greater uptake of nutrients such as phosphorus, zinc, and copper which are essential for plant development. In turn, the fungus benefits greatly from this association since it can feed on the sugars, amino acids, and other organic sources (photoassimilates) produced by plants through photosynthesis [9].

As already well discussed, mycorrhiza is a symbiosis between plants and soil fungi in which both parties are mutually aided along the way. In this symbiotic relationship, first, organic carbon flows from the host plant to the fungi and then the inorganic elements flow from the fungi structure to the plant, so both parties benefit [11]. Mycorrhizal fungi can only survive when combined with plants because the fungi cannot produce its own food and although it decomposes organic compounds for energy acquisition, it is not enough, it needs to grow and develop together with plants [11].

In crops context, this symbiotic relationship is important as it determines the ability to stimulate plant growth due to higher nutrient acquisition and protection from pathogens attacks such as bacteria and fungi, protecting against diseases. As observed, microorganisms have great potential to increase crop productivity. Dark septate fungi, Pseudomonas bacteria, and bacteriocins are some of the studied microorganisms and substances that can lead to new agricultural bioproducts, as growth promoters or for the control of agricultural pests and diseases [11].

Researchers have demonstrated excellent results with the use of microorganisms in the soil to improve the agronomic efficiency of crops. Some selected bacteria have the ability to solubilize the phosphorus present in the soil and to promote it available to the plants, while others have the function of fixing nitrogen from the air into the roots. In general, soils in tropical regions are mostly deficient in nitrogen and phosphorus, and these fertilizers usually add up to more than 50% of the cultivation cost [11].

As we know, not all applied fertilizer is absorbed by plants, maize absorbs only 55–60% N [12], around 20% P [13], 50–70% potassium (K) [14], and 33% sulfur (S) [15]. One strategy to improve the plants’ ability to absorb nutrients and consequently reduce fertilizer application, especially of P, is to inoculate AM fungi. The final response will be a maize plant well-nourished and presenting full growth and development.

Dark septate fungi are promising microorganisms that promote plant growth. At this fungus contact, rice plants grew shoots and roots 30% faster. In addition, tillers, which are new branches of the plant, increased by about 50%, which means greater nutrient uptake and grain production capacity [16]. As we observed, this fungus group also improves the nutritional state of the plants. In tests performed on tomatoes, nutrients such as nitrogen, phosphorus, and potassium accumulated to a greater extent compared to plants without the presence of microbes. In this way, it is possible to optimize plant nutrient use and obtain more vigorous crops [16].

When the farmer decides to use arbuscular mycorrhizal fungus, the plant must be inoculated, as it grows the fungus slowly develops and multiply, which can take many days for them to become fully established. Conversely, with the dark septum fungus use, the inoculum will be established in a few days. Another interesting feature of dark septum is its resistance to water stress. Researchers have observed that in the presence of this fungus, even with a lack of water, the plant developed similarly to another plant grown under normal conditions (without drought stress), confirming the full potential of this microorganism [16].

Research has shown that fungi and bacteria are effective and responsive in the restoration of highly degraded soils. Legume plants associated with these microorganisms have been successfully applied in several regions of mining and impoverished soils to lead to their recovery. As we have seen, microorganisms increase the absorption capacity of the roots, making them more resistant to environmental stress. This technique allows rapid revegetation, even when the subsoil has been exposed. While bacteria provide plants with the nutrient nitrogen, mycorrhizal fungi help plants uptake other nutrients, especially phosphorus and water.

The researchers selected the bacterial strains most effective at nitrogen fixation for each plant species and using microbiological multiplication techniques in the laboratory, it is possible to increase these more resistant and nitrogen-self-sufficient strains.

3. Agronomic practices that negatively impact mycorrhizal fungi

Agronomic practices such as intensive monocrop, soil use with recurrent harrowing, and subsoiling lead to a significant degradation and decrease in soil microbial biomass. There are other important impacts that we should highlight such as intensive grazing, indiscriminate use of pesticides and fertilizers, and mining activities. All these activities are responsible for sick, impoverished, and unproductive soil.

It is important to emphasize that fungi do not always act in a positive way, sometimes these microorganisms are the cause of a large number of diseases. Therefore, it is important to be careful with agronomic practices since if a person without chemical and biological knowledge recommends some wrong strain for inoculation, it may not help, but greatly hinder the production [16]. It is common that many field technicians with the intention of fertilizing the soil to invest in mycorrhizal fungi inoculation, however, it is necessary for a specific professional in the area to make such a symbiotic association between mycorrhizal fungi and agricultural crops.

It is important to say that the control of the disease caused by fungi requires mainly preventive measures since it is necessary to pay attention to the choice of the area to be cultivated until the harvests. This is due to the fact that for chemical control of diseases there are several products available on the market, from different companies.

4. Agronomic practices that positively impact mycorrhizal fungi

The different types of crop residues are very important for healthy soil, not only for supplying nutrients via biogeochemical cycling, but also for functions directly affecting physical, chemical, and biological properties.

Microorganisms are vital to agriculture, especially in two biological processes: (i) Biological efficiency − In this process, certain types of fungi act as solubilizers of soil nutrients, optimizing yields. (ii) Biocontrol − The process by which a group of fungi can do the work of bio-pesticides and biocides to facilitate the management. In addition to their use in agriculture, they can also be used in the medical field, for drug development [17] due to their bactericidal properties. They also can be used to make antibiotics, such as penicillin, whose function is to fight infectious diseases caused by bacteria. Another area where fungi excel is food, some are edible and can be used as part of human consumption [17].

The no-till system (NTS) and crop rotation are essential practices for maintaining good biological soil quality. The no-till farming system is considered a conservationist and sustainable practice, this agricultural practice is a form of soil management that involves techniques recommended to increase productivity while conserving or continuously improving the cropping environment. The main practices are: Absence or minimal soil disturbance. In relation to crop rotation, we can say that is the practice of alternating the plant species grown each season over the years for a more productive system. This conservation agriculture technique aims to reduce soil exhaustion. The crop rotation can benefit soil macro- and micro-fauna, since the richness and abundance of edaphic organisms are determined, among other factors, by the quantity and quality of aerial and root phytomass added to the soil [18].

The crop rotation system combined with no-till farming promotes an improvement in soil quality, as there are erosion reductions, increases in nutrient cycling, and, consequently, better biological activity. The straw has a fundamental function in the no-till farming principle and is highly effective in protecting the soil, avoiding the impact of raindrops, wind, and solar rays. It is also responsible for reducing temperature and water amplitudes, favoring biological activity. In addition, it increases the soil’s chemical and physical characteristics such as organic matter content, cation exchange capacity (CEC), and water availability for plants and other organisms.

5. Yield increase X Arbuscular mycorrhizal fungi

Arbuscular mycorrhizal fungi (AMF) are the main microorganisms that compose the majority of the microbial biomass in cultivated soils. About 80% of plants are symbiotic with these fungi, and they are an important factor in improving soil quality and crop growth.

There is a great nutritional benefit for plants influenced by arbuscular mycorrhizal fungi. Phosphorus stands out among the nutrients that combine with the Arbuscular Mycorrhizal Fungi to facilitate uptake. This nutrient is very low in soil solutions due to sorption and precipitation reactions, also immobilization, this kind of behavior is common in heavily weathered soils. AMF hyphae help in accessing this nutrient because they utilize more soil and places that are difficult for plants’ roots to access.

There are also reports in the literature that these fungi assist in the uptake of sulfur, potassium, nitrogen, zinc, copper, magnesium, iron, manganese, and calcium. Therefore, plants with high levels of mycorrhizal colonization are expected to be more tolerant to eventual nutrient unavailability and less dependent on the application of external inputs than plants with low symbiosis.

Indirectly, mycorrhizae also improve plant tolerance to nematode and disease attacks on coffee, increasing plant vigor. In addition, improving tolerance to pest and disease attacks is important because these organisms cause significant yield losses [17].

As seen earlier, AMF is an important stress reliever. These microorganisms increase drought resistance because they provide plants with increased water uptake. The increased hydration and stomatal conductance in plants associated with mycorrhizae promote transpiration, the main mechanism for cooling the leaves. Thus, hypothetically, coffee plants with a high degree of symbiosis are better able to withstand a high-temperature summer and suffer less scalding. These fungi also increased tolerance to metal toxicity such as copper, zinc, and aluminum and reduced damage caused by high osmotic pressure.

Topical application of amide and ammonia nitrogen fertilizers is also a major problem in these systems, as excessive acidification of the wetting bulb can increase the solubility of metal micronutrients to toxic levels [18]. Thus, mycorrhizae can be an important stress reliever in irrigated coffee farming improving soil quality the extensive development of extra-radicular hyphae and secretion of glomalin by these fungi are important mechanisms for improving soil physical, chemical, and biological properties [19].

Arbuscular mycorrhizal fungi improve soil structure by connecting particles and forming stabilized aggregates. This is due to the mechanical effects of extra-radicular hyphae growth and the secretion of glomalin. This glycoprotein exhaled by fungi has adhesive properties in the soil, and its content has been correlated with aggregate stability and organic matter. It increases the carbon content in the soil, stimulating biological activity because there is more food for the microorganisms.

6. Conclusions and Future perspectives with the adequate management of mycorrhizal fungi

Although several studies have shown that inoculation in young plants grown in nurseries works well, it is still not a common practice in the production of seedlings of coffee for example, or other perennial plants. Studies applied to plants in the field have shown inconsistent results because most cultivated soils naturally have sufficient inoculum of arbuscular mycorrhizal fungi. The best option to benefit from this partnership is to adopt conservation practices that stimulate microbial activity and endemic populations of AMFs.

The use of harrowing and subsoiling to constantly turn the soil should be avoided. These tools disrupt hyphae networks and expose soil surfaces to high temperatures, promoting the degradation of stable organic matter. Excessive use of herbicides and fungicides also negatively affects the populations of these fungi. Soils that have a high biological activity are usually intensively cultivated, producing large amounts of biomass per unit area. Therefore, it is not advisable to exploit its productive capacity to the maximum in order to preserve it.

Conservationist practices benefit bioactivity and the presence of mycorrhizal fungi in the rhizosphere of plants, this makes the production system more resilient and improves the quality of the soil for cultivation. A significant portion of producers is changing their production system to a model that sees and values the complexities of production systems with their particularities [9].

Abandoning the idea of soil as an inert, lifeless substrate, and that everything can be solved with agricultural chemical inputs, is a big step toward sustainable production, which is certainly necessary to enter an increasingly demanding market. Increasingly, farmers will have a real sense of the importance of keeping the soil environment healthy and balanced for the optimal propagation and establishment of microorganisms such as arbuscular mycorrhizal fungi.

Conflicts of interest

The author declares no conflict of interest.