Biochar and Trichoderma spp. in management of plant diseases caused by soilborne fungal pathogens: a review and perspective

A better understanding of the use of biochar with Trichoderma spp. (TRI), considered the most studied tool for biological control, would increase our ability to set priorities. However, no studies exist using the two inputs on plant disease management. Here, we hypothesized that biochar and TRI would be used for the management of soilborne plant pathogens, mainly due to changes in soil properties and its interactions. To test this hypothesis, this review assesses papers that used biochar and TRI against plant diseases and we summarize the handling mechanisms for each input. Biochar acts by mechanisms: induction to plant resistance, sorption of allelopathic and fungitoxic compounds, increase of beneficial microorganisms, changes the soil properties that promote health and nutrient availability. Trichoderma as biocontrol agents by different mechanisms: mycoparasitism, enzyme and secondary metabolic production, plant promoter agent, natural decomposition agent, and biological agent of bioremediation. Overall, our findings expand our knowledge about the reuse of wastes transformed in biochar combined with Trichoderma has potential perspective to formulate products as alternative management tool of plant disease caused by soilborne fungal pathogen and add important information that can be suitable for development of strategy for use in the global health concept.


Introduction
The growing need for a sustainable food production represents a major challenge for crop producers. The increase in demand for healthier food and the exponential growth of the world population pose difficulties to food production, intensified by climatic adversities as well as constant attacks of pests and diseases that compromise crop production. Plant diseases caused by soilborne pathogens decrease crop yields, resulting in great socioeconomic damage, due to the difficulty to diagnose and control these diseases, especially when symptoms occur only in the roots and not observed in the shoots (Ghorbanpour et al., 2018). Soil pathogens comprise fungi, oomycetes, bacteria, viruses, and nematodes (Montiel-Rozas et al., 219). Fungi stand out as the largest group causing root diseases in cropped plant species, since they occur in all agricultural ecosystems.
Although diverse, soil pathogens share similarities, such as the influence by biotic and abiotic soil components, poor dispersion (Liu et al., 2020), as well as the capacity of developing structures of resistance that allow these microorganinsms to survive long periods in the soil without a host plant, hindering their management.
Thus, research on efficient and sustainable management strategies is essential for a more integrative agriculture. The use of synthetic chemicals is the main method of pest and disease control in agriculture. However, the indiscriminate use of synthetic products has increased the resistance of pest and pathogens, damaged the environment, and affected human health 219). Alternative techniques for disease control, such as biological control (Zin & Badaluddin, 2020) has grown substancially in recent years with use of Bacillus spp., Metarhizium spp., and Trichoderma spp. Fungi of the genus Trichoderma are agents of importance in agriculture for biological control, due to their high potential as antagonist against many phytopathogens. The capacity of Trichoderma to remain in the soil for long periods characterizes an advantage for a preventive biological control (Da Silva et al., 2016). In addition, this fungus promotes the growth of host plants and stimulates plant resistance to the attack by pathogenic microorganisms that penetrate and colonize the root surface, limiting plant growth 219).
In recent years, biochar has been considered an important issue in management of soilborne phytopatogens since they provide several benefits for sustainable food production . Biochar is a solid compound that results from organic matter decomposition under high temperatures under low oxygen concentrations in a pyrolysis process (Lehmann et al., 2011). Silva et al. (2021) has studied the use of biochar as a low-cost alternative for waste reuse in agriculture, benefiting the soil, microorganisms, culture, and the environment. Biochar improves the soil physical, chemical, and biological parameters. It also increases retention of water and nutrients, favoring carbon sequestration and benefiting the soil microbiota (Lima et al., 2018;Medeiros et al., 2020a). Biochar has been used for the management of plant diseases caused by pathogens in the soil .
However, studies on the use of biochar combined with Trichoderma are still incipient. Therefore, it is crucial to investigate their use in combination to provide farmers a tool for the management of plant diseases caused by soilborne pathogens. Here, we hypothesized that the co-application of biochar and TRI would be used to the management of soilborne plant pathogen, mainly due changes soil properties and its interactions. To test this hypothesis, this review assesses twenty papers with biochar and thirty-three with TRI used as alternative tool to managemen plant diseases caused by soilborne pathogen and we summarize the handling mechanisms for each input.

Methodology
This study is a narrative review about the use of Biochar and Trichoderma spp. in the management of plant diseases caused by soil fungal pathogens. The selected literatures were extracted from the platforms: SciELO, ScienceDirect, Elsevier, PubMed, SpringerLink and Jornal CAPES.

Strategies for managing diseases caused by soilborne pathogens
Different strategies have been used to manage plant diseases caused by soil pathogens, such as the use of resistant cultivars, crop rotation, addition of organic matter sources, physical, chemical, and biological control techniques (Kazerooni et al., 2020;Medeiros et al., 2021). The use of resistant cultivars is a management strategy used in cropped areas with a history of pathogen infestation in the soil. This technique must be handled with care, as pathogens have a great capacity to overcome plant resistance, making them more susceptible to the disease. Crop rotation consists of alternating cultivation of different plant species to avoid as much as possible the contact of pathogens with susceptible crops (Hong et al., 2020). The introduction of new crops through this method allows the entry of microorganisms antagonistic against several soil phytopathogens (Larkin & Brewer, 2020).
On the other hand, the use of chemical control has increased considerably due to the expansion of agricultural areas over the years. This method involves the use of chemical compounds with specific action mechanisms that eradicate target microorganisms (Montiel-Rozas et al., 219). However, it is a practice that must be adopted carefully due to toxicological effects and occurrence of resistant phytopathogens (Coelho et al., 2020).
The biological control uses microorganisms that reduce the attack of pathogenic organisms through various interactions, such as antagonism, in which an organism produces substances that inhibit the development of others (Silva et al., 2017). Several microorganisms have been studied regarding mechanisms for their potential use as biocontrol agents. Fungi of the genus Trichoderma have mechanisms, such as antibiosis, predation, competition, and even induction of resistance to plants (Zin & Badaluddin, 2020). Therefore, the use of these fungi reduces the use of chemicals in agriculture, mitigating damages to the environment and providing more sustainable production.

Use of Trichoderma spp. in the biological control of plant diseases
The genus Trichoderma is widely studied and has several applications in the industry, in the environment, and mainly in agriculture. Trichoderma is known for the diverse benefits to plants, promoting plant growth (Medeiros et al., 2020a), producing phytohormones and enzymes that increase the root absorption area (Lee et al., 2016). These fungi promote phosphate solubilization (Chagas et al., 2017) and insoluble micronutrient, improving absorption of water and nutrients and inducing resistance to plants, contributing to the production of more vigorous plants. Trichoderma is a natural decomposition agent and thus used as a biological agent of bioremediation.
Moreover, it is the most studied species for biocontrol of plant disease (Zin & Badaluddin, 2020), for diverse soilborne pathogens (Elshahawy & El-Mohamedy, 2019;Lu et al., 2020). Different pathosystems using Tricoderma spp. in the biocontrol of plant diseases are shown in Table 1

Plant disease control mechanisms by Trichoderma spp.
The antagonism of Trichoderma involves a variety of mechanisms that confer success to the biocontrol of phytopathogens. Trichoderma is capable of surviving in unfavorable conditions and it also has a high reproductive capacity, efficient use of nutrients, modification of rhizosphere, root colonization, induction of resistance to host plants, and great aggressiveness towards phytopathogens (Kumar et al., 2017). Trichoderma also shows competition with other microorganisms for space and nutrients, inducing systemic resistance of plants to pathogens .
Mycoparasitism relationships are mechanisms for the biocontrol of pathogens that the Trichoderma species most use.
Antagonistic fungi recognize and attack pathogens directly, limiting their growth by strangling their hyphae, cause pathogen death (Alfiky, 2019), and excrets secondary metabolites and enzymes, such as exoglucanases, chitinazes, and proteases that degrade the cell wall of phytopathogenic fungi (Da Silva et al., 2016).

Use of biochar as management tool of plant diseases
Biochar has been considered an important tool to management of soilborne phytopatogens, due to its origin and production process, biochar has physicochemical properties and beneficial attributes . Biochar is a solid compound, rich in C obtained through the combustion of organic materials and could be produced from several types of raw material, such as agricultural waste, wood, and sewage sludge (Lehmann et al., 2011). The high carbon C in the biochar makes it an excellent source of substrate for microorganisms. Biochar remains in the soil for long periods, improving the physical, chemical, and biological soil attributes (Lima et al., 2018). Moreover, it shows high CEC, raises the pH, and increases water retention in the soil (Foster et al., 2016).
In addition, its high porosity and pore size provide an ideal habitat for the growth of microorganisms, which can ensure greater survival of beneficial microorganisms in the soil (Muter et al., 2017;Jaiswal et al., 2018). For example, the use of biochar changes the soil microbiome and can be as inoculant carrier of bacteria consortium against Fusarium sp., as these bacteria remain viable after more than six months of storage (Elhadidy, 2019) and is capable of plant growth promotion due to promote the nutrient availanility in the soil. Ajeng et al. (2020) showed that biochar act to the retention of nutrients to avoid being mathabolized by other phytophatogenic microrganisms or to leaching. This imputs plays an important role in the selective promotion of functional microorganism to dominate the soil microbial community (Liu et al., 2020), promoted root colonization by native arbuscular mycorrhiza and enriches the microbial network (Ajeng et al. 2020), as T. aureoviride (Medeiros et al., 2020b).

Plant disease control mechanisms by biochar
The  showed in a critical review in which 70% of the studies validated biochar as a strategy to manage diseases caused by pathogens in the soil. Studies show that biochar applied to the soil acts directly or indirectly in suppressing plant disease through mechanisms, such as (i) induction to plant resistance, (ii) sorption of allelopathic and fungitoxic compounds to the plant, (iii) increase of beneficial microorganisms, (iv) changes in the soil attributes that promote health and nutrient availability, and (v) changes of abiotic conditions that provide different management mechanisms for disease suppression (Figure 1).

Combined use of Trichoderma spp. and biochar in the management of plant diseases caused by soilborne pathogen
A better understanding of the use of biochar from different alternative waste sources with Trichoderma spp. (TRI), and the relationship between plant disease and environmental parameters would increase our ability to set priorities. Few studies reported the effects of the co-application of biochar with Trichoderma. (Medeiros et al., 2020a) and (Medeiros et al., 2020b) demonstrated the positive effects of the combined use of biochar and T. aureoviride on plant growth (melon and watermelon) and on the quality of sandy soils. Muter et al. (2017) observed that biochar applied in combination with Trichoderma increased germination and height of corn plants (Zea mays L.). Sani et al. (2020) showed that the co-application of biochar with Trichoderma promoted synergistically growth and flowering in tomato plants.
The effective growth promotion of antagonistic function of microorganisms against pathogens, as is the case of Trichoderma spp., are promoted due to the capacity of biochar to provide substrate and a shelter to these microorganisms, increasing the effectiveness of biological control (Muter et al., 2017). The porous structure of biochar allows the best development of plant roots, improving absorption of water and nutrients as well as significantly increasing biomass uptake to the entire plant. Biochar allows the increase of nutrients and their bioavailability in the soil. Moreover, Trichoderma spp.
ensures better absorption and assimilation of these nutrients by the plant, favored by the use of biochar, providing advantages to the soil-plant system (Jaiswal et al., 2018).
The use of biochar and Trichoderma spp. promotes agricultural practices in a more sustainable way by reducing the use of synthetic fertilizers, minimizing the use of chemicals for disease control, while reducing the use of inputs to increase agricultural productivity, mitigating the impacts caused to the environment by food production thus producing healthier foods ( Figure 1). Overall, our findings expand our knowledge about the reuse of wastes transformed in biochar, an alternative management tool of plant disease and add important information that can be suitable for development of strategy for use in the global health concept.

Conclusion
The use of biochar and Trichoderma spp. is a potential and low-cost alternative to sustainable agricultural production.
Their interaction promotes a series of benefits to soil quality and plant growth, reducing the use of synthetic products, increasing sustainable production and food security. This review showed that the biochar has potential for the formulation of new products, as it enhances the competitive power of Trichoderma spp. at the soil. Both can act as a powerful alternative tool to control plant diseases caused by pathogens inhabiting the soil, through different mechanisms. Future research should focus on exploring highly efficient strains, optimizing conditions, and assessing a comprehensive number of waste sources for biochar production as well as their efficacy in field experiments.