Indian Journal of Agricultural Research

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Indian Journal of Agricultural Research, volume 57 issue 3 (june 2023) : 273-282

Trichoderma Species: An Overview of Current Status and Potential Applications for Sustainable Agriculture

Eman F.A. Awad-Allah1,*, Ibrahim A.A. Mohamed2, Sherin F.A. Awd Allah3, Amany H.M. Shams4, Ibrahim H. Elsokkary1
1Department of Soil and Water Sciences, Faculty of Agriculture, Alexandria University, Alexandria, 21545, Egypt.
2Department of Botany, Faculty of Agriculture, Fayoum University, Fayoum 63514, Egypt.
3Department of Nematology Research, Plant Pathology Research Institute, Agricultural Research Center, Egypt.
4Department of Plant Pathology, Faculty of Agriculture, Alexandria University, Alexandria 21545, Egypt.
Cite article:- Awad-Allah F.A. Eman, Mohamed A.A. Ibrahim, Allah Awd F.A. Sherin, Shams H.M. Amany, Elsokkary H. Ibrahim (2023). Trichoderma Species: An Overview of Current Status and Potential Applications for Sustainable Agriculture . Indian Journal of Agricultural Research. 57(3): 273-282. doi: 10.18805/IJARe.AF-751.
In agro-ecosystems, Trichoderma species are beneficial microorganisms that improve soil health and crop development. They form mutualistic endophytic relationships with a wide range of plant species, promoting host growth, protecting against pathogen attack, and improving micro-and macronutrient uptake and use efficiency. As a result, they should be promoted because they have the potential to improve agricultural sustainability while reducing the use of harmful chemicals in agriculture. This review provides an overview of the current and potential applications of Trichoderma species for sustainable agriculture, their beneficial roles and how they can be used to boost plant growth and crop yield.
Soil microbes are important components of nutrient cycling; consequently, the structure and functions of soil microbial communities influence soil health and richness (nutrient pool) (Prakash et al., 2015). Recently, various environmentally friendly approaches, such as the use of natural microorganisms that boost plant development and disease resistance capability, have been frequently utilized to promote sustainable agriculture and environmental protection (Prakash et al., 2015; Rajamanikyam et al., 2017). Through their various activities, different classes of microorganisms (fungi [endophytic, ectomycorrhizal, and arbuscular] and bacteria [cyanobacteria]) play significant roles in nutrient mobilisation and uptake, plant growth promotion, and disease suppression (Cao et al., 2020; Prakash et al., 2015). Additionally, these microorganisms assist plant survival by increasing disease resistance and tolerance to various stresses, such as drought and salinity (Fig 1).

Fig 1: Various fungal partners involved in plant growth, survival and nutrition.



Plants host numerous endophytic microbes that improve their performance, particularly under biotic and abiotic stresses (Rajamanikyam et al., 2017; Tseng et al., 2020). Endophytic fungi (EF) are organisms which live in healthy plant tissues with no signs of disease or morphological changes during the entire plant’s life cycle (Rajamanikyam et al., 2017). Endophytes respond variably to different stressful factors that affect plant growth (Fig 2). Plants colonised by such endophytic plant symbionts are bipartite symbioses in which both members benefit each other; therefore, they have various advantages over similar plants that are not colonised (Harman et al., 2019).

Fig 2: Endophytic fungal response against stressful factors affecting plant growth.



Arbuscular mycorrhizal fungi (AMF) are beneficial soil microorganisms that form mutualistic symbiotic relationships with the roots of important food crops and play critical roles in the soil’s long-term fertility and health (Cao et al., 2020; Prakash et al., 2015). AMF are a biotechnological tool for improving plant stress tolerance and restoring degraded ecosystems (Begum et al., 2019; Cao et al., 2020). AMF symbiosis protects plants from a variety of abiotic stresses via a variety of mechanisms, including increased photosynthetic rate, mineral nutrient uptake, osmoprotectant accumulation, antioxidant enzyme activity up-regulation, and changes in the rhizosphere ecosystem (Begum et al., 2019).

Ectomycorrhizal (ECM) fungi are key organisms in the nutrient and carbon cycles of forest ecosystems, forming mutualistic symbioses with the roots of many tree species (Anderson and Cairney, 2007; Stuart and Plett, 2020). These fungi colonise the lateral roots of host trees, generating a network of interlacing mycelial filaments that penetrate root epidermal cells (Stuart and Plett, 2020). During this association, three features are generally recognised: (1) the formation of a fungal hyphae mantle or sheath, (2) the development of hyphae between root cells to form a Hartig net and (3) hyphae that grow into the surrounding soil (extra-radical mycelium) (Prakash et al., 2015). These unique structures serve as nutrient exchange sites and provide a large surface area between the two symbiotic partners (Stuart and Plett, 2020).

Plant growth-promoting fungi (PGPF) are a diverse group of non-pathogenic fungi that live freely on the root surface, inside the root, or in the rhizosphere and promote seed germination, seedling vigour, plant growth, flowering, and productivity in a wide range of host plants (Hossain et al., 2017). PGPF have prompted a lot of attention as biofertilizers and biocontrol agents because of their many beneficial impacts on plant quantity and quality, as well as their positive interaction with the environment (Hammad and Elbagory, 2019). Understanding how PGPF induces plant responses is critical for developing new strategies to manage plant growth and disease (Hossain et al., 2017).

In summary, fungi such as AMF, ECM, EF, and PGPF play beneficial roles in plant survival by assisting them in different ways, including induced systemic resistance, plant growth promotion, host resistance to insect feeding, disease resistance, phosphorus solubilisation, production of plant growth-promoting (PGP) hormones, increased aboveground photosynthesis, and plant tolerance to abiotic stresses, such as drought, salt and heavy metals (Fig 3).

Fig 3: Beneficial roles of arbuscular, ectomycorrhizal, endophytic and plant growth-promoting fungi in plant nutrition and growth.


 
Plant growth enhancement by Trichoderma spp.
 
Trichoderma is a fungus belonging to the Hypocreaceae family that is found in all soils (Chen et al., 2021). The majority of Trichoderma species studied colonise the root surface or live as endophytes within root tissues; however, some species can be isolated from plant aerial parts (Ruano-Rosa et al., 2016; Samolski et al., 2012; Tseng et al., 2020). As shown in Fig 4A and Fig 4B, Trichoderma strains started out white and cottony, then developed into yellowish-green to deep green compact tufts, particularly in the center of a growing spot. Fig 4C depicts a dual culture assay demonstrating the mycoparasitic and antagonistic activity of Trichoderma spp. against the pathogen Fusarium oxysporum.

Fig 4: Different isolated strains of Trichoderma spp., (A) T. harzianum, (B) T. viride, (C) A dual culture plate demonstrating the mycoparasitic behaviour of Trichoderma spp. and the soil-borne pathogen Fusarium oxysporum 10 days post inoculation.



Trichoderma species can promote the growth of their hosts while also protecting them from pathogenic attacks (Tseng et al., 2020). Additionally, various Trichoderma species can improve root growth and development, confer abiotic stress tolerance, and improve micro-and macronutrient uptake and use efficiency, resulting in increased crop productivity (Mehetre and Mukherjee, 2015). Therefore, these species can create mutualistic endophytic relationships with several plant species (Fig 5).

Fig 5: Diagrammatic depiction of beneficial effects of Trichoderma spp.



The use of Trichoderma spp. has frequently resulted in increased plant growth and improved crop yields, but the exact mechanism of action remains unknown (Mehetre and Mukherjee, 2015). One possible mechanism for increased plant growth is an increase in the total absorptive surface, which facilitates nutrient uptake and translocation in the shoots, resulting in increased plant biomass through the efficient use of macronutrients (N, P, and K) and micronutrients (Samolski et al., 2012). Several mechanisms for how Trichoderma spp. impact plant growth and development have been proposed, including solubilisation of many plant nutrients from their solid-phase compounds (Altomare et al., 1999), production of growth hormones (Jaroszuk-Ściseł et al., 2019), upregulation of genes and pigments that improve the plants’ photosynthetic capability and activate biochemical pathways that reduce reactive oxygen species to less harmful molecules (Harman et al., 2019), increased uptake and translocation of less available minerals (Fiorentino et al., 2018) and suppression of pathogens (Khalili et al., 2016; Awad-Allah et al., 2022). Plant growth stimulation is evidenced by increases in biomass, productivity, stress resistance, and nutrient absorption (Guzman-Guzman et al., 2019). Moreover, PGP compounds produced by certain Trichoderma species stimulate plant growth (Studholme et al., 2013). Most studies found that Trichoderma spp. improve overall plant health and growth by providing a suitable environment and producing a large number of secondary metabolites, as shown in Table 1.

Table 1: Effect of Trichoderma spp. on plant growth and development.



Furthermore, Trichoderma and other microorganisms in soil can detoxify toxic compounds and accelerate the degradation of organic material (Zin and Badaluddin, 2020). Recent research has shown that Trichoderma spp. can degrade chemical pollutants by acting on chemicals and metal contaminants via the activity of various enzymes, as well as improve soil physical and chemical properties and make nutrients available to plants from agrochemicals (Tripathi et al., 2013; Awad-Allah  et al., 2022).
 
Trichoderma-mediated nutrient use efficiency (NUE) of crop plants
 
Agricultural production is based on the ability of plants to convert solar energy into chemical energy through photosynthesis with the help of chlorophyll (Kathpalia and Bhatla, 2018). Importantly, plants require an adequate supply of 13 essential mineral elements in addition to carbon, hydrogen and oxygen to accomplish this critical role (Vatansever et al., 2017). Mineral nutrients are classified into two types: macronutrients and micronutrients (Vatansever et al., 2017). Macronutrients are nutrients that are needed in relatively large amounts and are further classified into two types: primary and secondary nutrients (Shang et al., 2014). N, P and K are primary nutrients, while Ca, Mg and S are secondary nutrients (Shang et al., 2014). In contrast, micronutrients (trace/minor elements) are essential elements for plant growth and are required in very small quantities, for example, Zn, Mn, Fe, Cu and Mo (Kathpalia and Bhatla, 2018).

NUE is a measure of how effectively plants use available mineral nutrients (Baligar and Fageria, 2015). It is defined as the yield (biomass) per unit of nutrient intake from the soil and/or fertiliser (Baligar and Fageria, 2015; Mehetre and Mukherjee, 2015). NUE is divided into two interactive components: nutrient acquisition efficiency (i.e. the amount of nutrients taken up by plants from the soil in relation to nutrient supply) and nutrient utilisation efficiency, which informs the biomass generated by the unit of nutrients assimilated by plants (Nieves-Cordones et al., 2020). Improving NUE is not only required for increasing crop production into low-nutrient-availability marginal areas, but it is also a technique to minimise the usage of inorganic fertilisers (Baligar and Fageria, 2015).

Microbe-mediated improvement of NUE is important in alleviating gradual loss of soil fertility/productivity caused by intensive agriculture (Mehetre and Mukherjee, 2015). Microorganisms in the soil and rhizosphere influence plant nutrient availability by facilitating the degradation of soil organic matter during an important process known as composting (Mehetre and Mukherjee, 2015; Mostafa et al., 2019). Humus, or humified organic matter, is found in compost and serves as a “bank” or reservoir for essential plant nutrients (Awad-Allah and Elsokkary, 2020; Mehetre and Mukherjee, 2015; Mostafa et al., 2019). Trichoderma spp. can accelerate the composting process and play a positive role in the process of compost humification (Mehetre and Mukherjee, 2015; Randhawa et al., 2020). Therefore, combining organic fertilisers (compost) with Trichoderma spp. as biofertilizers may be a more effective way to increase plant biomass than only using organic fertilisers or Trichoderma separately (Zhang et al., 2018). This could be because Trichoderma biofertilizers effectively regulate soil chemistry and microbial communities, resulting in significantly higher aboveground plant biomass than organic fertilizer without Trichoderma (Zhang et al., 2018). In addition, root colonisation by Trichoderma spp. promotes root growth and development, which directly leads to enhanced nutrient absorption and translocation in the shoots, resulting in higher plant biomass via the effective utilisation of of N, P, K and micronutrients (Mehetre and Mukherjee, 2015; Samolski et al., 2012). As shown in Table 2, there are strong indications and experimental evidence that applying Trichoderma spp. increases nutrient absorption. According to Fiorentino et al., (2018), Trichoderma inoculation could be a viable strategy for managing the nutrient content of leafy horticulture crops grown in low-fertility soils, assisting vegetable growers in reducing the use of synthetic fertilisers and developing sustainable management practises to optimise N use efficiency. Moreover, Trichoderma can also improve Fe nutrition of plants and provide long-term control of Fe deficiency in calcareous soils (Santiago et al., 2013). As a result, significant efforts must be made to incorporate the potential of microbes such as Trichoderma spp. in the biofortification of Zn and Fe in food grains (Singh and Prasanna, 2020). Hence, Trichoderma spp. can be used as bioinoculants for plant growth and development, resulting in eco-friendly and sustainable farming practices (Sharma and Borah, 2021; Molla et al., 2012; Awad-Allah et al., 2022).

Table 2: Trichoderma improves nutrient use efficiency in crop plants.


 
Trichoderma as biocontrol agents for plant disease management
 
Biological control occurs when a biocontrol agent is applied to a host plant to prevent the spread of pathogen-caused plant diseases. It is a viable alternative to chemical control (Awad-Allah et al., 2021). Trichoderma spp. are the most widely used biocontrol agents for a variety of root, shoot and postharvest diseases, having antagonistic capabilities based on the activation of several pathways (Abdel-lateif, 2017; Zin and Badaluddin, 2020). According to Benitez et al., (2004), Trichoderma spp. exert biocontrol against fungal phytopathogens either indirectly (by competing for nutrients and space, influencing environmental conditions, stimulating plant development, plant defence mechanisms and antibiosis), or directly (via mycoparasitism). During mycoparasitic interactions, Trichoderma spp. initiate the synthesis of hydrolytic or lytic enzymes, such as glucanase, chitinase and protease, which degrade the chitin polymers of the fungal pathogen cell wall (Mukhopadhyay and Kumar, 2020; Parmar et al., 2015). Trichoderma may also create antibiotics or low-molecular-weight diffusible compounds such harzianic acid, tricholin, peptaibols, 6-pentyl-pyrone, viridin and heptelidic acid, all of which hinder the development of other microbes (Abdel-lateif, 2017). These indirect and direct mechanisms may work together and their importance in the biocontrol process is influenced by the Trichoderma spp., antagonistic fungus, crop plant and environmental conditions, such as nutrient availability, pH, temperature and iron content (Benitez et al., 2004). For these reasons, Trichoderma spp. can be used as effective biofungicides and alternative agents against phytopathogens (Belaidi et al., 2022; Srivastava et al., 2016). To provide a better understanding, important studies involving the antifungal potential of Trichoderma spp. for controlling plant diseases, as well as several mechanisms for plant disease management, are summarised in Table 3.

Table 3: Effect of Trichoderma spp. on some plant diseases.


 
Potential use of Trichoderma-based products in agriculture
 
Trichoderma-based agricultural products are marketed worldwide as bio-pesticides, biofertilizers, growth promoters, and natural resistance boosters (Abdullah et al., 2021). They are used in a variety of cultivated environments, such as fields, greenhouses, and nurseries, as well as in the production of a wide range of horticultural crops, such as fruits, trees, and ornamental crops, to protect crops from various plant pathogens or to boost plant growth and productivity (Meher et al., 2020; Launio et al., 2020; Abdullah et al., 2021). They are applied by seed treatment, bio-priming, seedling dip, soil application, or foliar spray (Meher et al., 2020; Abdullah et al., 2021). A list of marketable Trichoderma-based agricultural products is shown in Table 4. Bio Spark Trichoderma, for example, is effective against the damping-off of vegetables and some tropical fruit diseases. Notably, Trichoderma-based products have been reported as a success story not only in crop disease control but also in enhancing farmer income, particularly in Philippine highland farms (Launio et al., 2020).

Table 4: Some commercial products of Trichoderma spp. used in agriculture.



The potential uses of Trichoderma-based products to promote crop health or control plant diseases are dependent on the development of commercial formulations with appropriate organic and inorganic carriers that enable Trichoderma to live for a long length of time (Meher et al., 2020). Moreover, Trichoderma formulations with strain mixtures perform better than individual strains for the management of pests and diseases of crop plants, as well as plant growth stimulation (Meher et al., 2020). For example, Biota Max™ is a unique soil probiotic and biofertilizer that includes a variety of Trichoderma spp., including T. harzianum, T. viride, T. koningii and T. polysporum, as well as other beneficial soil microorganisms. Therefore, the beneficial soil microorganisms in Biota Max™ help plants grow stronger, healthier root systems while using less N fertilisers. However, the lack of a proper screening protocol for selecting promising Trichoderma candidates, lack of sufficient knowledge on the microbial ecology of Trichoderma and plant pathogens and awareness, training and education shortfalls are some of the factors that limit Trichoderma-based product development and utilisation worldwide (Meher et al., 2020). Therefore, the sustainability of these commercial Trichoderma-based agricultural products is critical for ensuring the productivity of agricultural crops with Trichoderma spp. (Zin and Badaluddin, 2020; Launio et al., 2020).
Trichoderma spp. are versatile filamentous fungi that can be found free-living in soil, colonising dead organic matter, and forming beneficial endophytic relationships with plants. They have the potential to be effective biocontrol agents by inhibiting the growth of many phytopathogenic fungi. However, their characteristics and mechanisms must be fully understood before they can be used in the field to limit the spread of phytopathogens. Furthermore, Trichoderma spp. promote root growth, induce plant defence, and boost plant growth in the face of biotic and abiotic stresses, such as drought, salinity, and the presence of poisonous metal ions. Finally, Trichoderma spp. can be used as effective biofungicides and biofertilizers in field crops, reducing the need for harmful synthetic fungicides and fertilisers while also promoting eco-friendly and sustainable farming practices. However, further research is needed to improve the efficacy and safety of these fungi.
The authors declare that they have no conflict of interest regarding the publication of this paper.
This research received no external funding.
Data is contained within the article.
Not applicable.
Not applicable.

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