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Mohd Suhaimi, N.S. Harnessing Trichoderma in Agriculture. Encyclopedia. Available online: https://encyclopedia.pub/entry/17361 (accessed on 27 July 2024).
Mohd Suhaimi NS. Harnessing Trichoderma in Agriculture. Encyclopedia. Available at: https://encyclopedia.pub/entry/17361. Accessed July 27, 2024.
Mohd Suhaimi, Nurul Shamsinah. "Harnessing Trichoderma in Agriculture" Encyclopedia, https://encyclopedia.pub/entry/17361 (accessed July 27, 2024).
Mohd Suhaimi, N.S. (2021, December 21). Harnessing Trichoderma in Agriculture. In Encyclopedia. https://encyclopedia.pub/entry/17361
Mohd Suhaimi, Nurul Shamsinah. "Harnessing Trichoderma in Agriculture." Encyclopedia. Web. 21 December, 2021.
Harnessing Trichoderma in Agriculture
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This entry is adapted from the peer-reviewed paper 10.3390/agronomy11122559

Increased agricultural activities driven by rising food demand have led to environmental problems mostly arising from the high levels of external inputs and resources that are required. Additionally, environmental changes, such as global warming, can lead to various biotic and abiotic stresses, which have negative impacts on crop production. Numerous solutions and agricultural strategies have been introduced to overcome these problems. One of the ways to improve plant production as well as to increase resistance towards biotic and abiotic stresses is by utilizing beneficial microbes as soil inoculants. A better understanding of the ability of Trichoderma to enhance crop production and the mechanisms that are involved are important for deriving maximum benefits from their exploitation. These versatile fungi hold great promise for the development of viable commercial products that can be used widely in agriculture for increasing crop productivity in a more sustainable way.

Trichoderma growth promoter fungi sustainable agriculture stress tolerance biocontrol

1. Introduction

Continuous growth in the world’s population has led to a corresponding increase in food demand, which has necessitated the mass production of agricultural products [1]. By 2050, the population to be fed will be over 9 billion people. Not only do we have to increase food availability, but we also must ensure that supplies are sustainably produced by not compromising the services that nature is able to provide [2]. Intensive large-scale industrial agriculture requires high-external input and resources, and these ultimately cause environmental problems such as water shortages, destruction of biodiversity, a decline in soil fertility, and elevated levels of greenhouse gases, leading to an increase in biotic and abiotic stresses, which threaten agricultural productivity and food security [3][4].
Beneficial microbes employ various mechanisms of action that increase plant productivity through the promotion of plant growth and health, such as (a) colonizing soil and/or plant parts, thereby occupying space and limiting the proliferation of phytopathogens; (b) producing enzymes, antibiotic substances, and volatile organic compounds that suppress the phytopathogens; (c) facilitating nutrient and water uptake; (d) producing phytohormone; (e) inducing local or systemic resistance responses in plants; and (f) improving various physiological and molecular processes [5][6][7]. Trichoderma is among the most widespread fungi in the world and is a plant symbiont that resides in varying habitats, including the rhizosphere and plant tissue (as an endophyte). Trichoderma is also widely used as biocontrol agent against phytopathogenic microorganisms. For example, Trichoderma was found to endophytically colonize Brassica oleracea (kale) and activated the systemic resistance of kale plants against the bacterial pathogen, Xanthomonas campestris [8]. Some of the mechanisms involved in promoting plant growth and disease protection by means of endophytic fungi include increasing access to nutrients (nitrogen, phosphorus, potassium, zinc, iron, etc.), the production of antibiotics, the production of plant hormones, a reduction in ethylene, or an increase in water acquisition rate [9].
Numerous studies have been conducted to elucidate the mechanisms by which Trichoderma confers resistance to plant pathogens and resilience against various kinds of biotic and abiotic stresses [10][11]. Over the years, scientists and agricultural practitioners have focused on the search for environmentally friendly options for the management of cropping systems. Finding the best method for improving crop production is crucial in order to achieve a sufficient food supply for the continuously rising population. Agroecology has been a prominent way of redesigning food systems to achieve greener agriculture approaches with higher sustainability [12][13]. One important agroecological approach for maximizing root and rhizosphere efficiency is the application of beneficial microbes, including Trichoderma [14][15]. This strategy can lead to improved crop productivity and better nutrient use efficiency while providing a friendlier option for human health and the environment [16][17].

2. Roles of Trichoderma in Sustainable Crop Production

The effects of root inoculation by Trichoderma are not restricted to the site of colonization but exist throughout the entire plant system. Colonization involves a complex system whereby the fungus is able to invade plant cells but can only live symbiotically without killing the plant. Trichoderma resides at the outermost layer of the roots and does not penetrate into the inner vascular tissue [18]. In Trichoderma studies with arabidopsis, the plants were seen to restrict the invasion of Trichoderma in the vascular bundle through the presence of metabolites such as salicylic acid (SA) and glucosinolates (GSLs) [19][20]. A successful Trichoderma–plant interaction results in improved plant growth and crop yield upon the cumulative positive effects induced by the fungus that subsequently improve nutrient uptake and transport in plants [21][22]. For instance, composted kitchen wastes comprising T. harzianum showed considerable promise as a biofertilizer for tomato plants with yield increases of up to 336.5% [23]. In a chickpea study, Trichoderma spp. caused an increase in the growth and yield parameters of the treated plants compared to the uninoculated controls. This result was found to be caused by the enhanced solubilisation and uptake of phosphate [24]. Furthermore, a maximum yield of chilies (69.55 q/ha) was recorded when the seeds were pre-treated with T. harzianum together with its foliar sprays.
Nutrient solubility and availability are induced by the acidification of soils by plant roots upon inoculation with the fungus. The process occurs through the secretion of some organic acids such as gluconic, citric, and fumaric acids [25]. In the case of sugarcane, both T. harzianum and T. viride were significantly effective in enhancing the uptake of phosphorus as well as other micronutrients, thereby improving germination, tiller population, millable canes output, and commercial cane sugar yield (CCS t/ha) [26]. In tomato plants, shoot and root growth attributes as well as chlorophyll content were significantly increased when sown in Trichoderma-fortified soil. Mineral contents in both shoot and root were higher compared to control plants [27]. Upon the application of T. virens, the efficiency of nitrogen uptake in lettuce and rocket plants was greater with enhanced crop yield and quality. Those acids reduce soil pH, subsequently allowing better nutrients solubility and uptake [28]. Other than acidification, the induction of root growth by the fungus and the increase in root biomass contributed to better nutrient absorption. It was observed that the single inoculation of broccoli plants with T. viride significantly increased the above-ground fresh weight, root length, chlorophyll b, head diameter, root phosphorus content, and shoot nitrogen content compared to uninoculated control plants [29].
Trichoderma sp. also secretes secondary metabolites that play important roles in elevating plant growth and yield. For example, T. harzianum and T. atroviride, with their main secondary metabolites harzianic acid (HA) and 6-pentyl-α-pyrone (6PP), respectively, were observed to improve grape plant growth, yield, and quality [30]. Vinale et al. [31] showed that the 6PP produced by Trichoderma has an auxin-like mechanism of action that is involved in plant growth improvement. Further study demonstrated that 6PP is responsible for promoting plant growth and regulating root architecture, inhibiting primary root growth, and inducing lateral root formation [32]. This study showed that 6PP modulated the expression of PIN auxin-transport proteins in a specific and dose-dependent manner in primary roots. Other than that, T. harzianum was found to release a metabolite called harzianolide, which is a plant growth regulator that is responsible for improving the growth of tomato seedlings [33]. This study revealed that harzianolide enhances root length and tips as well as induces the expression of genes involved in the salicylic acid (PR1 and GLU) and jasmonate/ethylene (JERF3) signaling pathways that are related to the plant defence mechanism. In arabidopsis, T. virens and T. atroviride were found to secrete indole acetic acid (IAA) and auxin-related substances; these metabolites are important for root development [34]. Studies have shown that rice plants inoculated with T. asperellum produced better plant architecture, higher panicle number, longer panicle length, and increased plant height [35][36][37]. This is in agreement with previous study on the application of T. harzianum on maize plants. When applied to the soil or directly to the seeds, the fungus caused an increase in all of the measured parameters, including growth parameters and levels of chlorophyll, starch, nucleic acids, total protein, and phytohormones of the plants [38].
Numerous studies have been conducted to elaborate the mechanisms by which Trichoderma promotes plant growth and development [30][31][39][40][41]. Some of these mechanisms can be explained by the upregulation of photosynthesis-related proteins resulting in a better photosynthetic rate, plant nitrogen use efficiency [39], and enhancement of plant nutrient uptake [42]. While molecular studies on Trichoderma effects are still in a nascent stage, some are showing promising results. For example, a large portion of the genes related to carbohydrate metabolism, stress modulation, and photosynthesis were up-regulated in maize plants upon inoculation with Trichoderma [43]. Similarly, in rice, the presence of T. asperellum was found to be correlated with the up-regulation of different genes, some of which have been identified to be involved in photosynthesis and chlorophyll biosynthesis. The up-regulation of genes related to CO2 fixation, response to light, and stomatal complex development indicated an enhancement of the plant’s efficiency in photosynthesis [44]. Table 1 summarizes the genes reported to be up-regulated in various plants upon Trichoderma inoculation.
Table 1. Up-regulated genes in some plants upon Trichoderma inoculation.
Plants Trichoderma Species Genes Observed Effects References
Arabidopsis, cucumber T. asperelloides MDAR Increased osmo-protection/oxidative stress. [45]
Arabidopsis T. atroviride,
T. virens		 AtERD14 Mitigated cold stress effects. [46]
Rapeseed T. parareesei NCED3, ACCO1, ERF1 and PYL4 Improved tolerance to drought and salinity. [47]
Wheat T. longibrachiatum SOD, POD, and CAT Seedlings were protected from salinity. [48]
Tomato T. harzianum TAS14 and P5CS Improved tolerance to cold. [49]
Potato T. harzianum Lox and GST1 Induction of plant disease resistance. [50]
Poplar T. asperellum PdPapARF1 Promoted growth and defence responses. [51]

3. Roles of Trichoderma in Sustainable Plant Disease Management

Since the 1920s, the very common, soil-inhabiting fungi, Trichoderma spp. have been recognized for their capability to act as biocontrol agents against many phytopathogens based on their abilities to parasitize other fungi and to produce antibiotics [42][52]. Later, their principal mechanism of action for plant protection was known to be based on the induction of disease resistance. Trichoderma has been documented to control many pathogenic microorganisms that affect plants, including bacteria (Pseudomonas and Xanthomonas), other fungi (e.g., Fusarium, Curvularia, Colletotrichum, Alternaria, Rhizoctonia, and Magnaporthe), the oomycetes (Pythium and Phytophthora), and at least one virulent virus (green mottle mosaic virus on cucumber) [42].

3.1. Trichoderma as Biocontrol Agents against Plant Pathogenic Bacteria

Plant diseases caused by bacteria are relatively difficult to control. However, the most common methods used to effectively control these diseases include plant breeding and cultural, chemical, biological, and physical control measures. Biocontrol agents are effective in controlling bacterial pathogens and are safer for the environment than chemical bactericides are. The excessive application of chemicals and consumer acceptance towards resistant cultivars can be very complex, which makes the use of biocontrol agents an attractive alternative [22].
Trichoderma showed an inhibitory effect on the growth and survival of the pathogenic Gram-negative bacterium, Ralstonia spp., in tomato plants, which was attributed to the secretion of various compounds such as lysosime, viridiofungin, and trichokonin [53]. Moreover, bacterial wilt caused by the soilborne bacterium R. solanacearum was inhibited by the application of T. asperellum, and the disease incidence was subsequently decreased with concomitant improvement in plant growth and yield under field conditions. This was achieved through the induction of a maximum level of defence enzyme activities, such as POX, PPO, and PAL, β-1,3-glucanase, and the total phenolic contents in plants [54]. Other examples of biocontrol of bacterial phytopathogens include the induction of resistance by Trichoderma conferred protection in tomato plants against Xanthomonas euvesicatoria (the causative agent of bacterial spot) and [55] cucumber plants grown in the presence of Trichoderma exhibiting greater protection against Pseudomonas syringae pv. lachrymans infection. T. harzianum activated separate metabolic pathways in cucumber that are involved in plant signaling and biosynthesis. Plant protection may be conferred by a combination of several modes of action provided by Trichoderma, such as phytoalexins biosynthesis, lignification, and the accumulation of pathogenesis related proteins and antimicrobial secondary metabolites [56].

3.2. Trichoderma as Biocontrol Agents against Phytopathogenic Fungi

Other than bacterial infections, fungal diseases are often associated with damage to crops, causing major losses in agricultural activities and food production. Thus, finding the best option to eradicate this problem is crucial. Trichoderma was found to have the ability to eliminate phytopathogenic fungi through a mechanism known as mycoparasitism. This involves the suppression of other microorganisms at the same site, thereby making it the dominant organism at the location [15][57].
Mycoparasitism by Trichoderma species involves an attack on the pathogen’s cell or structures [58]. It was reported that T. koningii did not invade healthy tissues but colonized infected or damaged onion root tissues as a secondary colonizer, where it reduced Sclerotium cepivorum infection by destroying the hyphae [59]. On the other hand, T. virens not only parasitized the hyphae of many pathogenic fungal species, but also penetrated and destroyed some of the resting structures of these fungi, thereby reducing their inoculum potential in soil [60]. The pre-emergence of damping-off diseases in cotton seedlings caused by Rhizopus oryzae was observed to be controlled upon T. virens treatment. This fungus metabolized the pathogen propagule germination stimulants that emanated from the germinating cotton seed [61].
Several species of Trichoderma also produce volatile and non-volatile antibiotics and enzymes, which have shown antagonistic effects towards phytopathogenic fungi [62]. Protease, endochitinases, β-glucosidases, mannosidases, and phosphatases released by T. harzianum were found to be involved in the biocontrol of various pathogens, including Guignardia citricarpa (the causative agent of citrus black spot). These enzymes are involved in the degradation of pathogen cell wall membranes and proteins [63]. Trichoderma also releases metabolites that are capable of diminishing or antagonizing pathogenic microbes [64]. Fungal terpenoids (desoxyhemigossypol, hemigossypol, and gossypol) synthesized in cotton roots by T. virens were found to be involved in combating R. solani-incited cotton seedling [65]. The application of Trichoderma on R. solani-infected chilies improved plant growth and yield. This was attributed to the reduction of the damping-off disease of seedlings as well as to reducing root and stem rot in chilies [66].
In another report, inoculation of T. harzianum inhibits R. solani growth by the induction and expression of lipoxygenase (Lox) and glutathione S-transferase (GST1) genes in the roots of potato plantlets that have been simultaneously inoculated with both organisms [50]. The Lox gene product is crucial for lipid peroxidation processes during plant defence responses to pathogen infection [67]. On the other hand, GST1 is a defence gene that is involved in the detoxification of toxic substances by their conjugation with glutathione, the attenuation of oxidative stress, and participation in hormone transport [68]. Biotic stresses can induce plants to produce higher levels of damaging reactive oxygen species (ROS). The excessive production of ROS causes oxidative stress resulting in the damage of cellular components, consequently leading to the death of plant cells [69]. A study conducted by Herrera-Téllez et al. [70] found that tomato plants pre-treated with T. asperellum and that were subsequently challenged with two fungal pathogens, Fusarium oxysporum and B. cinerea, experienced less severe wilting and stunting symptoms compared to non-treated plants due to the ROS modulation by Trichoderma.
Besides their direct antagonistic effects against fungal and bacterial plant pathogens, Trichoderma species have also been found to induce resistance against various plant diseases. This resistance induction can be either localized or systemic. The effects of systemic resistance induced by Trichoderma were recorded using a model rhizobacterium. For example, T. virens successfully induced plant-systemic resistance in maize against Colletotrichum graminicola [71]. Other than that, T. virens was capable of inducing localized resistance against R. solani infection of cotton roots through the stimulation of terpenoid synthesis by the plant [65]. The mechanisms involved in these inductions are associated with different kinds of changes at the biochemical and molecular levels in the plants [72].
The capability of Trichoderma to protect plants against different bacterial and fungal pathogens is summarized with examples in Table 2.
Table 2. Trichoderma species and their biotic stress regulation mechanisms.
Plants Trichoderma Species Phytopathogens Observed Effects References
Tomato T. harzianum Clavibacter michiganensis Prevented the incidence of bacterial canker. [73]
Tomato T. harzianum and T. longibrachiatum X. euvesicatoria, Alternaria solani Reduced bacterial spots, triggering systemic acquired resistance (SAR) or induced systemic resistance (ISR). [55]
Tomato T. harzianum Ralstonia spp. Trichoderma spp. AA2 inhibited the growth and survival of Ralstonia spp. [53]
Tomato T. asperellum R. solanacearum Delayed wilt development, effectively decreased disease incidence, increased fruit yield, and improved plant growth promotion. [54]
Tomato T. asperellum F. oxysporum,
B. cinerea		 Inhibited ROS production. [70]
Arabidopsis
thaliana		 T. asperelloides P. syringae Lesser necrotic lesions surrounded by extensively spreading chlorosis. [74]
Radish,
lettuce,
tomato		 T. hamatum X. campestris Lowered bacterial population and disease severity (bacterial leaf spot). [75]
Rice T. harzianum X. oryzae Bacterial leaf blight severity was reduced while plant growth was improved. [76]
Cucumber T. asperellum P. syringae pv. lachrymans Transcript accumulation of biosynthetic defence related genes and accumulation of phenolic compounds (antimicrobial activity). [56]
Citrus T. harzianum G. citricarpa The involvement of protease affecting the germination of G. citricarpa conidia, able to deactivate the pathogen’s hydrolytic enzymes that are responsible for plant tissues necrosis. [63]
Onion T. koningii S. cepivorum Destroyed the hyphae, making it detached at septa, cell walls dissolved, and many hyphal apices burst. [59]
Cotton T. virens R. solani Induced terpenoid synthesis, toxic to the pathogen. [65]
Cotton T. virens and T. longibrachiatum R. oryzae Metabolized pathogen propagule germination stimulants that emanate from the germinating cotton seed. [61]
Cotton T. virens R. solani Penetrated and destroyed some of the resting structures of the pathogen. [60]
Sunflower T. koningii,
T. aureoviride,
T. longibrachiatum		 S. sclerotiorum Head rot incidence was significantly reduced, delayed epidemic onset. [77]
Wheat T. harzianum,
T. aureoviride,
T. koningii		 Pyrenophora triticirepentis Pathogen mycelium on the leaf surface collapsed or disintegrated. [78]
Rambutan T. harzianum Botryodiplodia theobromae, Colletotrichum gloeosporioides, Gliocephalotrichum microchlamydosporum Reduced the occurrence of the three postharvest diseases, also retained the overall quality and colour of the fruits. [79]
Chickpea T. atroviride,
T. koningii,
T. harzianum,
T. hamatum		 F. oxysporum,
Ascochyta rabiei		 Suppressed fungal infections by mycoparasitism, antibiosis, and competition for space and/or nutrients. [80]
Arabidopsis,
Rapeseed		 T. harzianum B. cinerea Induction of systemic defence, mediated by jasmonic acid. [81]

3.3. Trichoderma as Biocontrol Agents against Pests and Plant-Parasitic Nematodes

Plant diseases caused by insect pests and plant-parasitic nematodes (PPNs) are also considered to be a significant threat to global agricultural productivity and sustainability. Insect pests can cause agricultural losses of up to 70% [82], while 12% of worldwide food production is lost due to plant-parasitic nematodes (PPNs) [83].
Among the common nematode antagonistic fungi, also known as nematophagous fungi, T. harzianum. T. viride, and T. lignorum have been commercially produced as fungal biocontrol agents for the management of phytonematodes [84]. An experiment employing Trichoderma for the control of the root-feeding nematode Meloidogyne hapla in tomatoes revealed that tomato plants that were prior inoculated with Trichoderma exhibited a lower number of nematode eggs laid on or near the roots of about 1000 (2%) eggs compared to 50,000 eggs laid on the roots of untreated plant controls [85]. Earlier, an experiment in India showed that the bio-integration of T. harzianum in combination with oil cakes could significantly reduce the population of citrus nematode Tylenchulus semipenetrans in both soil and root [86].
Fungi belonging to the Trichoderma genus are also well-known for their beneficial effects in conferring plant protection against insect pests and parasitic nematodes. Based on previous studies on the mode of action of Trichoderma as the mycoparasite fungus, Trichoderma species can act directly as an entomopathogen through parasitism, and the production of insecticidal secondary metabolites, antifeedant compounds and repellent metabolites. On top of that, this versatile fungus can act indirectly as a mycoparasite through the activation of systemic plant defensive responses, the attraction of natural enemies, or the parasitism of insect-symbiotic microorganisms [82]. For example, T. longibrachiatum that was formulated into a biopesticide was reported to be able to control the insect pest Leucinodes orbonalis in brinjal plants as well as increasing crop yield by 56.02% [87]. Moreover, under laboratory conditions T. harzianum exhibited an inhibitory activity of around 70-80% towards Xylotrechus arvicola (an important pest in vineyards) and Acanthoscelides obtectus (a causal agent of severe post-harvest losses in the common bean) [88].
The application of T. gamsii to the roots of Arabidopsis thaliana decreased the feeding behaviour of herbivore Trichoplusia ni through the modulation of the metabolome as well as affecting the content of phytohormones in plant leaves. T. gamsii-inoculated plant leaves recorded higher levels of amino acids and abscisic acid and lower concentrations of sugars compared to untreated plants [89]. Maize plant roots associated with T. atroviride recorded higher resistance against the insect herbivore Spodoptera frugiperda compared to untreated plants. Further examination indicated that there was a significant increase with regards to the emission of volatile terpenes and the accumulation of jasmonic in roots of inoculated rice plants. Chemical analyses revealed that T. atroviride produced the volatiles 1-octen-3-ol and 6-pentyl-2H-pyran-2-one, which were believed to have an important role in reducing the consumption of the foliar tissue of maize plants by S. frugiperda [90].
The inoculation of T. atroviride in tomato plants induced plant resistance to the insects Spodoptera littorali and Macrosiphum euphorbiae. These protection capacities were attributed to a plant response induced by T. atroviride that was linked with molecular and biochemical changes in tomato plants. T. atroviride also produced alterations in plant metabolic pathways leading to the production and release of volatile organic compounds (VOCs) that are involved in the attraction of the aphid Aphidius ervi (a parasitoid with activity against many pests), thus reinforcing indirect plant defence barriers [91]. The insecticidal efficacy of T. harzianum with natural protectants was also found to be an acceptable approach for the management of stored product damage resulting from the insects Callosobruchus maculatus and C. chinensis in cowpea seeds. The T. harzianum-based biofungicide formulation caused complete insect mortality and inhibited progeny production. Thus, this eco-friendly product can be an effective strategy for the management of both insects on stored cowpea seeds [92].

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