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).
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).
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).
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.
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).
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.
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).
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.
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).
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).
