1. INTRODUCTION
Since the last few decades, the agricultural systems have continuously improved in efforts to maximize the production of a sufficient supply of safe, nutritious, and high-quality food globally. The wide use of agrochemicals such as synthetic fertilizers and pesticides undeniably plays a significant part in increasing crop yield in the shortest possible time and in maintaining sufficient food supplies [1,2]. However, a significant number of issues have arisen, which associate the usage of these agrochemicals to environmental issues. The excessive inputs of synthetic pesticides and fertilizers have led to many adverse effects such as the rise of resistant plant pathogens, atmospheric pollution, groundwater pollution, soil degradation, fertility reduction, health hazard, and environmental hazards [1,3,4]. These problems have prompted the need to identify harmless alternatives that are also inexpensive and sustainable. Therefore, eco-friendly alternatives such as biocontrol agents and biofertilizers were considered as a substitute to the use of synthetic chemicals in this present day.
The use of fungi as biological control agents has been widely practiced in forestry and industrial agriculture. In recent years, more studies are highlighting the importance of fungi with implications for plant yield and food production by a mechanism of suppressing undesirable diseases caused by pests or pathogens. Nowadays, there are many fungi used as biocontrol agents, some examples are Aspergillus spp., Ampelomyces spp., Candida spp., Coniothyrium spp., Gliocladium spp., and Trichoderma spp. [5-8]. Among these fungi, Trichoderma is the most competent for being able to control the development of pathogenic fungi [9] and to promote plant growth. The study would aim to describe the role of Trichoderma species in details as a biocontrol agent and biofertilizer along with the recent advancements, mechanism involved, and would attempt to brief on the commercially available products of Trichoderma species for application.
1.1. Trichoderma
Trichoderma is a genus of a heterogeneous group of fungal species. They are mainly classified as anamorphic Hypocreales and are further described by quick development and bountiful production of conidial spores as well as the capacity to produce sclerotia [10]. Trichoderma species are ubiquitous saprophytic fungi and they are usually found in the soil and root ecosystems [11-14] as well as above ground such as on rotting wood and other organic materials [15-19]. Some of them are capable of being mycoparasites [20] and may be antagonistic to other fungi using their cell walls and cytoplasmic parts as nourishing assets. Further, Trichoderma strains produce few pigments, ranging from a greenish-yellow up to a reddish tinge and sometimes colorless strains might likewise be available. The conidia can have different hues, going from drab to various tints of green or dim or earthy colored hints [10]. The characteristics of Trichoderma are as follows: Septate and translucent hyphae; conidiophores are short, translucent, branched often giving the pyramidal appearance, not verticillate, bearing phialides which may appear singly or in groups; spores produced are conidia which are translucent, ovoid in shape, borne in small terminal clusters at the tips of phialides [21,22].
In general, Trichoderma is not viewed as pathogenic or destructive to plant development. Their presence in the rhizosphere as biofertilizers can promote plant development and improvement [10]. Moreover, there have been numerous reports on the capacity of Trichoderma species to colonize roots as symbionts, and to initiate systemic and localized resistance in plants, which protects the plants against various pathogens such as fungi, bacteria, viruses, and even insects [10,11,18,23] as well as to stimulate plant development and growth [24]. In addition, Trichoderma can thrive effectively under very competitive conditions due to their natural resistance to antibiotics produced by other competing microorganisms [25]. In economic essence, they have a wide scope of valuable features for numerous biotechnological applications, mainly in agriculture, industry, and environmental biotechnology [10].
2. TRICHODERMA AS BIOCONTROL AGENTS
Plant diseases caused by pathogens have resulted in a decreased crop yield, growth, and development. Pathogens including certain fungal strains are mainly accountable for causing diseases in plants leading to high loss of yield [14,26-28]. Out of various ways to prevent yield losses due to pathogenic fungi, the use of synthetic fungicides is a widely practiced [14,27,29]. However, they may have destructive implications on the environment and human health [30-32], and it may also result in the resistance development of the pathogenic fungi infecting the plants [33]. Over time, once the pathogen develops resistance, the existing synthetic fungicides may become ineffective and the use of new fungicides will have to be implemented for future effective disease control [14]. A potentially effective and powerful method to control plant disease is using microorganisms as biocontrol agents as an alternative agro-practice [14,34]. This approach depends on the antagonistic relationship between such organisms and the target pathogens [35]. For example, soil-borne plant pathogens can possibly be controlled by the addition of antagonistic microorganisms to the soil, which is a non-chemical means for plant disease control [36].
Fungi in recent years are considered as good candidates for biocontrol agents and as good alternatives for substituting chemical usages. Köhl et al. [37] defined biological control as the process that lessens the number of microbial pathogens by other microorganisms that act as antagonists. Different mechanisms of biocontrol can operate under different conditions. Unlike other biocontrol agents such as viruses and bacteria, fungi do not need to be ingested to infect their hosts but rather they attack directly through the organisms. Trichoderma is commonly used in the development of biocontrol agents. Biocontrol agents are microorganisms that are capable to antagonize and suppress plant disease causing pathogens [10]. They are safer to be used compared to using chemical pesticides and at the same time are not any less effective. Biocontrol agents also have no harmful implications to other organisms that are beneficial for plant growth, health, and productivity. An effective biocontrol agent should be genetically stable, and able to be mass-produced efficiently using cheap media, as well as effective at low concentrations against various pathogens [38,39]. Moreover, the biocontrol agent must not be toxic to humans, be impervious to pesticides, not harmful to the environment, and not pathogenic to the host plant [14,39,40].
The unique property of Trichoderma spp. to secrete mycolytic enzymes and its non-phytopathogenic nature makes it a most attractive biocontrol agent [41] compared to the other fungal species known for their biocontrol activity. Biocontrol by Trichoderma involves a number of mechanisms including mycoparasitism or hyperparasitism, antibiosis, induction of resistance, and competition for nutrients and space with plant pathogens [12,15,20,33,42]. In addition, alteration of the root architecture which improves the plant’s resistance to pathogens, and destruction of the root-knot nematode at the different stages of its growth phases, and of certain segments of adult nematodes have also been reported [43]. Table 1 describes the various bio-active compounds secreted by the Trichoderma species and their roles in biological control. The mechanism of biocontrol activity of the species could be further categorized into two modes, that is, the direct and the indirect mode.
Table 1: Secondary metabolites secreted by Trichoderma spp. and their bio-active role
| Chemical nature | Secondary metabolites | Trichoderma species involved | Bio-activity observed | References |
|---|---|---|---|---|
| Alcohol | 1-Octen-3-ol | Trichoderma atroviride | Induces conidiation and defense responses through JA | [44-46] |
| 2-Phenylethanol | Trichoderma harzianum | Reduces the growth of Aspergillus flavus and aflatoxin production | [47,48] | |
| Tyrosol | Trichoderma harzianum | A quorum-sensing molecule | [47] | |
| Anthraquinone | Chrysophanol | Trichoderma aureoviride, Trichoderma viride | Related to pigmentation | [49] |
| Pachybasin | Trichoderma harzianum | Increases the number of coils of the biocontrol agent against R. solani | [50] | |
| Emodin | Trichoderma viride | Antimicrobial and antineoplasic agent | [51-53] | |
| Azaphilone | T22azaphilone | Trichoderma harzianum | Inhibits the growth of Rhizoctonia solani, Pythium ultimum and Gaeumannomyces graminis | [54] |
| Fleephilone | Trichoderma harzianum | Inhibitory activity against the binding of regulation of virion expression (REV) proteins to REV responsive element RNA | [55] | |
| Harziphilone | Trichoderma harzianum | Cytotoxicity against the murine tumor cell line M-109 | [55] | |
| Bisorbicillinoid | Bisvertinolone | Trichoderma longibrachiatum | Antifungal properties via inhibition of β-(1,6)-glucan biosynthesis | [56] |
| Trichodimerol | Trichoderma longibrachiatum | Inhibitory activity against lipopolysaccharide-induced production of tumor necrosis factor α in human monocytes | [57] | |
| Bisorbicillinol | Trichoderma spp. strain USF-2690 | Antioxidant properties | [58] | |
| Butenolide | 5-Hydroxyvertinolide | Trichoderma longibrachiatum | Potential antagonistic activity against the fungus Mycena citricolor | [59] |
| dehydro-derivative of harzianolide | Trichoderma harzianum | Antifungal activity against Gaeumannomyces graminis var. tritici | [60-62] | |
| T39butenolide | Trichoderma harzianum | [54] | ||
| Carotanes | Trichocaranes A, B, C and D | Trichoderma virens | Inhibits the growth of etiolated wheat coleoptiles | [63] |
| Diketopiperazine | Gliotoxin | Trichoderma hamatum Trichoderma viride Trichoderma virens | Antiviral, antibacterial, fungistatic activity and immuno-suppressive properties | [64,65] |
| Gliovirin | Trichoderma virens | Antimicrobial compound against oomycetes and Staphylococcus aureus | [66] | |
| Dipeptide | Trichodermamide A | Trichoderma virens | Has a weak cytotoxic effect on three cell lines, P388, A-549 and HL-60 | [67,68] |
| Trichodermamide B | Trichoderma virens | Displays cytotoxicity against HCT-116 human colon carcinoma | [64] | |
| Ergosterol-derivated compound | Ergokonin A | Trichoderma longibrachiatum, Trichoderma koningii, Trichoderma viride | Antifungal activity against Candida spp. | [64] |
| Hydrocarbonated compound | Ethylene (ET) | Trichoderma atroviride | Regulates cell diferentiation and defense responses | [69] |
| Hydrolytic enzymes | Cellulases | Trichoderma reesei | Degrades cellulase during root colonization to penetrate the plant tissue | [70,71] |
| β-1,6-Glucanases | Trichoderma spp. | Hydrolyses fungal pathogen cell walls of B. cinerea, R. solani, Phytophthora citrophthora | [16] | |
| Chitinases | Trichoderma spp. | Hydrolytic enzymes of the fungal cell wall | [72,73] | |
| Indolic compound | Indole-3-acetic acid (IAA) | Trichoderma atroviride, Trichoderma virens | Controls a number of growth and development processes in plants | [74] |
| Indole-3-acetaldehyde | Trichoderma atroviride, Trichoderma virens | Controls root growth in A. thaliana | [74] | |
| Indole-3-carboxaldehyde | Trichoderma atroviride, Trichoderma virens | Induces adventitious root formation in A. thaliana | [23] | |
| Isocyano metabolite | MR566A, a chlorine-substituted cyclopentyl isonitrile | Trichoderma harzianum | Inhibits melanin biosynthesis in B16 melanoma cells | [75,76] |
| Isoprenoid | Abscisic acid (ABA) | Trichoderma atroviride, Trichoderma virens | Regulates stomatal aperture in A. thaliana | [77] |
| Ketone | 3-Octanone | Trichoderma atroviride | Induces condiation | [45,46] |
| Koninginins | koninginins A–E | Trichoderma koningii Trichoderma harzianum | Antifungal activity against F. oxysporum, Fusarium solani, and Alternaria panax | [78-80] |
| Monoterpene | β-Myrcene | Trichoderma virens | Regulates the expression of genes related to abiotic and biotic stresses | [81,82] |
| cis- and trans-β-Ocimene | Trichoderma virens | Induces expression of JA defense response-related genes in A. thaliana | [81,82] | |
| Nitrogen heterocyclic compound | Harzianic acid | Trichoderma arundinaceum; Trichoderma harzianum | Antimicrobial metabolite, siderophore and plant growth regulator | [83-86] |
| Harzianopyridone | Trichoderma harzianum | Antifungal activity against Botrytis cinerea, R. solani and inhibitor of the protein phosphatase type 2A (PP2A) | [87,88] | |
| Melanoxadin | spp. strain ATF-451 | Inhibits melanin formation in the larval hemolymph of the silkworm, Bombyx mori | [89] | |
| Peptaibol | Alamethicin | Trichoderma viride | Induces plant defense in lima bean and pathogen resistance | [65,90,91] |
| Trichovirin II | Trichoderma virens | Induces resistance in cucumber plants | [65] | |
| sm1 | Trichoderma virens | Activates defense responses in cotton, rice and maize | [92,93] | |
| Epl1 | Trichoderma atroviride | Triggers defense responses through JA and SA in maize | [94] | |
| trichokonins VI, VII, and VIII | Trichoderma koningii | Broad-spectrum antimicrobial activity against a range of important plant pathogens, such as R. solani, Fusarium oxysporum, Verticillium dahliae, and Botrytis cinerea | [91,95] | |
| Peptide based antibiotic | Trichoderma citrinoviride VKPM F-1228 | Broad spectrum antibiotic activity against pathogenic bacteria, clinical Aspergillus spp., and micromycetes | [96] | |
| Peptide | Trichokonin VI (Tk VI) | Trichoderma longibrachiatum | Inhibits primary root growth in A. thaliana | [97] |
| Pyrane | Koninginin A | Trichoderma koningii | Plant growth regulator | [78] |
| Koninginin D | Trichoderma koningii | Alters pathogen fungal growth of R. solani, Phytophthora cinnamomi, Pythium middletonii, Fusarium oxysporum and Bipolaris sorokiniana | [98] | |
| Pyridones | Hharzianopyridone | Trichoderma harzianum | antifungal activity against plant pathogenic fungi, such as P. ultimum, G. graminis var. tritici, R. solani, and B. cinerea | [54,87] |
| Pyrones | 6-pentyl-2H-pyran-2-one | Trichoderma viride Trichoderma atroviride Trichoderma harzianum Trichoderma koningii | Antifungal activity against R. solani, F. oxysporum, Botrytis spp., Penicillium spp., Aspergillus fumigatus, Candida albicans and Cryptococcus neoformans Antinematode and plant growth-promoting activities in tomato and A. thaliana | [46,61,64,99, 100,101] |
| Viridepyronone | Trichoderma viride | Antagonistic activity against Sclerotium rolfsii | [102] | |
| Sesquiterpene | Cyclonerodiol | Trichoderma harzianum Trichoderma koningii | Inhibits growth of etiolated wheat coleoptiles | [79,103] |
| Heptelidic acid (koningic acid) | Trichoderma virens, Trichoderma viride | Potential activity against the human malaria parasite, Plasmodium falciparum | [64,104,105] | |
| β-Farnesene | Trichoderma atroviride | Acts as an alarm pheromone in aphids | [46,106] | |
| β-Caryophyllene | Trichoderma virens | Attracts nematodes that prey on insect larvae | [82,107,108] | |
| Setin-like metabolite | Trichosetin | Trichoderma harzianum | Inhibits the growth of rice, tomato and medicago | [64] |
| Siderophore | Fusarinine C | Trichoderma spp. | Fe-chelated, can be available to plants | [109] |
| Ferricrocin | Trichoderma atroviridea, Trichoderma virensa, Trichoderma reeseia | Key metabolite in the competition for iron in the rhizophere | [110] | |
| Coprogen B | Trichoderma spp. | Solubilizes iron unavailable to the plant | [103] | |
| Statin | Compactin (mevastatin) | Trichoderma longibrachiatum, Trichoderma pseudokoningii | Activity as a cholesterol-lowering agent | [111-113] |
| Steroidal compound | Viridin | Trichoderma koningii, Trichoderma virens, Trichoderma viride | Antifungal metabolite that alter the spore germination of Botrytis allii, Colletotrichum lini and Fusarium caeruleum | [64] |
| Viridiol | Trichoderma virens | Herbicidal properties | [114] | |
| Wortmannolone | Trichoderma virens | Inhibits phosphatidylinositol 3-kinase with potential to attack human neoplasms | [64,115] | |
| Virone | Trichoderma virens | Inhibits phosphatidylinositol 3-kinase | [64,115] | |
| Trichothecene | Trichodermin | Trichoderma brevicompactum | Fungitoxic metabolite against Candida spp. | [116,117] |
| Trichodermin | Trichoderma brevicompactum | Phytotoxic effect | [86] | |
| Trichodermin | Trichoderma viride, Trichoderma polysporum, Trichoderma sporulosum, Trichoderma reesei | Inhibits the elongation and termination steps in protein synthesis | [64] | |
| Trichodermol | Trichoderma spp. | Antimalarial agent | [64] | |
| Trichodermin and harzianum | Trichoderma arundinaceum | Plant defence | [118] |
2.1. Direct Mode of Biocontrol Activity by Trichoderma spp.
2.1.1. Mycoparasitism
Many studies have reported that Trichoderma can prevent some plant diseases via inhibition of the plant pathogens mostly found in the rhizosphere, through mycoparasitism or hyperparasitism [119,120]. It refers to the process in which Trichoderma lives in the expense of another plant parasite by either colonizing on the parasite or living inside the parasite [121-123]. For example, hyper-parasitic Trichoderma harzianum is used in controlling the choke disease caused by the fungal Epichloe typhina in a grass species Puccinellia distans [121]. This method has been widely used in controlling various plant pathogens such as Sclerotium rolfsii, Botrytis cinerea, and Rhizoctonia solani [124]. Trichodex is the commercially available Trichoderma formulation that is widely applied to reduce plant diseases [121,125].
Mycoparasitism is a common mechanism by which there is an antagonistic direct contact action towards a pathogen. There are several stages of mycoparasitism by Trichoderma including pathogen recognition, binding to the target, enzymatic disruption of the fungal cell wall, and assimilation of the cytoplasmic content [10,12,14,126]. Trichoderma can attach to a target pathogen by binding the carbohydrates of their cell wall to the lectin of the pathogen. Upon contact, Trichoderma will coil around the target fungus and develop appressoria. Trichoderma can produce cell wall degrading enzymes for example amylase, cellulase, chitinase, glucanase, lipase, pectinase, protease, and xylanase [127], and also numerous volatile compounds for example 6-pentyl-α-pyrone (6-PAP), toluene, D-limonene and α-bergamotene [128]. Other metabolites can also be produced [Table 1]. The cell wall degrading enzymes play a significant role in facilitating the hydrolytic degradation of the cell wall of the fungal pathogen, which can be made up of chitin and glucan polysaccharides [10]. Trichoderma can produce a high level of extracellular enzymes that degrade cellulose and chitin [10]. According to Howell [15], the preliminary degradation of the cell wall of Botrytis cinerea and Fusarium oxysporum by lytic enzymes enabled the easier penetration of antibiotics into the pathogen cells.
2.2. Indirect Mode of Biocontrol Activity by Trichoderma spp.
2.2.1. Antibiosis
Most fungal species are capable of secreting one or more compounds with antibiotic properties. Many Trichoderma species can produce low molecular weight secondary metabolites with antibiotic properties which can interfere with the development of various microorganisms through inhibition [10]. This inhibition action is called antibiosis. It is another mechanism found in Trichoderma for controlling plant pathogens, which depends on the secretion of antimicrobial compounds or specific secondary metabolites that exhibit inhibitory properties. There are more than 180 secondary metabolites of Trichoderma that has been characterized into various classes of compounds [64,129]. These compounds have different roles in the biological control of different pathogens. Some secondary metabolites have the capability of modifying plant metabolism and growth. Trichoderma strains, for example, Trichoderma viride, T. harzianum, and Trichoderma koningii, are capable of production and secretion of a volatile metabolite, 6-PAP which is responsible for the biocontrol of several pathogenic species such as Botrytis cinerea, Rhizoctonia solani, and Fusarium oxysporum [10]. According to Harman [11], different groups of metabolites might play an important role as plant resistance inducers.
2.2.2. Competition
Some studies suggest the existence of a competition between fungi and pathogens as another mechanism of biocontrol. Trichoderma may compete for essential nutrients and limit the growth of pathogens [130]. Apart from nutrients, Trichoderma can also compete with other pathogens for space including infection sites on plant roots [10]. Trichoderma can easily colonize the rhizosphere of diverse environments and cause significant changes in plant metabolism [11,42]. The mechanisms which aid in the colonization of the diverse ecological niches are exceptionally evolved and vary in Trichoderma [12,131,132]. Moreover, Trichoderma is resistant to toxic metabolites that are produced by plants such as flavonoids, terpenoids, phenols, and phytoalexins in response to infection. Trichoderma can defend plants against pathogens through a physical interaction between Trichoderma and the plants up to the outer layer of the epidermis and the root bark [42]. Trichoderma can acidify their surrounding environment to produce adverse conditions for the growth of pathogens [10,33]. Furthermore, the wide metabolic versatility of many Trichoderma species has enabled them to use different and complex carbon and nitrogen sources, which allow Trichoderma to limit competing pathogens from growing and spreading in the environment [25].
2.2.3. Induction of systemic resistance
Trichoderma spp. are capable of inducing systemic and local resistance in the plants against the plant pathogens as a result of the physiological and biochemical changes initiated by complex interactions between the microbial biomolecules and plant receptors [11,133,134]. This triggers the formation of the defense enhancing chemical, that is, salicylic acid in the entire plant as a systematically induced defense mechanism and also by inducing the synthesis of regulatory plant proteins that could help in the defense mechanism by recognizing the microbial biomolecules [135]. It is also documented that the induction of systematic and local resistance in a plant is further dependent on the plant species, pathogenic microbial species, environmental factors, and rhizosphere and symbiont relationship [136].
3. TRICHODERMA AS BIOFERTILIZERS
Biofertilizers are defined as substances containing beneficial living microorganisms that colonize the soil ecosystems and enhance plant growth by increasing the supply of primary nutrients to the host plants [1,137,138], improve soil chemical and biological properties, phosphates solubilization, and agricultural production [139]. Biofertilizers have many benefits compared to synthetic fertilizers such as they increase absorption of nutrients in plants, minimize leeching, and are involved in composting of solid wastes [14,137,138,140]. One of the main sources of biofertilizers is fungi that are used for the inoculation of seed and soil to increase nutrient availability for plants [141]. They can restore the nutrient cycle in the soil, form soil organic matter by releasing growth-promoting hormones and improve root proliferation [1]. These biofertilizers are capable of fixing atmospheric nitrogen, decomposing organic materials, and solubilizing soil phosphates, which are beneficial in improving soil fertility as well as enhancing plant growth through the supply of nutrients [14,142]. Furthermore, they are environmentally friendly and are safe for crops or other plants [143].
Trichoderma species are known biofertilizers for promoting plant growth and development, and are regularly utilized by most crop types with or without amendments [19]. They are well known to improve plant nutrient uptake, produce growth hormones and provide plant protection from pathogens [144,145]. According to Chang and Baker [146], when Trichoderma are applied regularly to plant soil, they promote plant growth and seed germination, development of roots, and improvement in height and weight of the plant. Trichoderma are known to improve overall plant health and produce different types of secondary metabolites including growth hormones and certain enzymes, and to benefit plants through Trichoderma-plant interactions [19,33]. From these interactions, it is evident that plant growth is stimulated from the production of vitamins, increased availability of biogenic elements such as nitrogen and phosphorus, mobilization of nutrients in soil and plants, and improved mineral uptake and transport [10] [Table 2].
Table 2: Trichoderma sp. as bio-fertilizers and their role in promoting plant growth and yield.
| Compound | Strain | Crops | Application mode | Beneficial outcome | References |
|---|---|---|---|---|---|
| Biofertilizer | Trichoderma azevedoi | Lettuce | Simple exposure | Increases carotenoids and chlorophyll with reduction in the white mould attack to about 78.83% | [147] |
| Trichoderma afroharzianum | Tomato | Seed inoculation or treatment | Helps in the secretion of phytohormones like homeostasis, antioxidant activity, phenylpropanoid biosynthesis and glutathione metabolism | [148] | |
| Trichoderma harzianum, Trichoderma asperellum, Trichoderma hamatum, Trichoderma atroviride | Chinese cabbage | Irrigation | Increases soil enzyme activity, yield by 37%, and increases the concentration of inorganic nitrogen and phosphorus content of the soil | [149] | |
| Trichoderma brevicompactum, Trichoderma gamsii, Trichoderma harzianum | Tomato | Seedling drenching | Improved growth and yield due to the production of indole-3 acetic acid | [19,150] | |
| Trichoderma harzianum Rifai, Trichoderma asperellum | Tomato | Seed treatment | Improves phosphorus uptake | [151] | |
| Trichoderma brevicompactum, Trichoderma gamsii, Trichoderma harzianum | Tomato | Seed drenching | Improves phosphorus solubilization | [150] | |
| Trichoderma erinaceum | Rice | Seed treatment | Improves germination, vigor, and yield | [147] | |
| Trichoderma harzianum T22 | Tomato | Seed treatment | Improves soil fertility, level of minerals and antioxidants, nutrient uptake, and yield | [152] | |
| Trichoderma harzianum T22 | Tomatp | Soil amendment as compost | Increase in yield to about 12.9% | [153] | |
| Trichoderma viride | Sugar cane | Powder as fertilizers | Improves nutrient uptake | [154] | |
| Trichoderma asperellum T34 | Cucumber | Seedling drenching | Enhanced nutrient uptake | [155] | |
| Trichoderma harzianum | All crops | Compost | Enhances residue decomposition resulting in availability of soil nutrients | [20] | |
| Trichoderma simmonsii | Bell pepper | Seedling drenching | Improves yield to about 67% | [156] | |
| Trichoderma reesei | Chickpea | Seed treatment | Enhanced mineral uptake | [157] | |
| Trichoderma harzianum | Mustard | Soil inoculation | Improved nitrogen absorption and increased yield to about 108 and 203% | [43,158] | |
| Trichoderma harzianum | Chilli | Soil inoculation | Increased yield | [159] | |
| Trichoderma harzianum | Barley | Seed inoculation | 17% increase in yield | [160] | |
| Trichoderma viridae | Wheat | Soil and seed inoculation | 75.8% increase in yield with improved nutrient absorption | [161] | |
| Trichoderma viridae | Potato | Soil inoculation | Increased yield with an average of 16.25 tubers/ plant | [162] | |
| Trichoderma viridae | Red beet cabbage | Seed inoculation | 29% increase in yield | [163] | |
| Trichoderma harzianum | Onion seedlings | Seedling inoculation | Enhanced growth and yield | [164] | |
| Soil conditioner | Trichoderma asperellum | Maize | Soil granules | Improves yield | [161,165] |
Mastouri et al. [165] stated that these fungi mobilize nutrients in plants to increase crop yield. Some Trichoderma strains can produce organic acids such as gluconic acid, citric acid, and coumaric acid and acidify the surrounding environment to solubilize phosphorus ions, micronutrients, and mineral cations, for example, Fe3+, Mn4+, and Mg2+, which then become available in the soil for plants utilization [11,19,133]. Trichoderma strains are also known to produce phytohormones to promote root and shoot growth in plants [11,167]. As an example, Trichoderma can produce zeaxanthin and gibberellin compounds that help in rapid seed germination [10]. The fungal biofertilizer can be used as a soil conditioning agent which helps in improving the diversity and concentration of plant beneficial microorganisms thus helping in the mitigation of greenhouse gases (carbon dioxide and methane) that cause climate change [19]. Trichoderma strains can also eliminate minor pathogens in the rhizosphere to maximize the potential of plant growth [10,168]. Further, their ecofriendly and human friendly nature has attracted various researchers and farmers worldwide, increasing their usage and application [160]. The phytohormones and enzymes produced by Trichoderma eventually help in promoting plant growth, yield, nutrient absorption, phosphate solubilization, mineral absorption, antioxidant activity, and soil conditioning [169-176]. They are also reported to improve the nutrient absorption quality and yield of many vegetables that include brinjal, tomato, sugar beet, chilies, potato, cauliflower, onion, peas, and also other plants such as groundnut, cotton, wheat, tobacco, Bengal gram, sugarcane, red gram, banana, soybean, citrus, and sunflower [19,150,177].
Phytohormones play a key role in the plant growth, especially during the shoot and root elongation. Appropriate levels of phytohormones in the requisite time of support would enable the increased and healthy plant growth which generally leads to the increased crop yield [175]. The presence of Trichoderma in the germination stage of a seed helps in the improved production (balanced quantities) of growth hormones such as gibberellic acid and indole-3-acetic acid which improves the germination rate and seedling vigor [147] [Table 2].
Similarly, phosphate being an important nutrient that plays an imperative role in the plant growth and development is always inadequately absorbed by the plants or inadequately available for plant’s absorption especially in the acidic soil [164]. Many Trichoderma species, specifically T. harzianum and Trichoderma reesei, are well known for their ability to solubilize phosphorous with the production of a specific enzyme phytase which on reaction with insoluble tricalcium phosphate solubilizes it and makes it available for plants absorption [150,173,178] [Table 2]. On the other hand, Trichoderma koningiopsis produces alkaline phosphatase enzyme for the effective solubilization of the insoluble phosphate available in the soil [174].
As nutrients are the essential compound promoting the plant growth and development, an altered uptake of nutrients can result in the malnourished crops with stunted growth and reduced crop yield. Trichoderma application as biofertilizer improves the uptake of nutrients in crops and also the availability of nutrients in soil for crop’s absorption. Yadav et al. [153] have suggested that the presence of T. viride in soil improved the uptake of nitrogen, phosphorus, potassium, and organic carbon in the sugarcane crops. Another report stated that the presence of Trichoderma in rhizosphere can lead to the colonization of crop roots as endophytes, which in turn enabling the solubilization, better availability, and improved absorption of nutrients by the crop [179].
4. COMMERCIALLY AVAILABLE TRICHODERMA BASED BIOACTIVE COMPOUNDS AND BIOFERTILIZERS
Several commercial formulations of Trichoderma as bioactive compounds and biofertilizers are known and are used worldwide. Moreover, many initiatives and studies were carried out by various researchers and commercial agencies for the development and usage of Trichoderma as an agent controlling plant diseases and enhancing plant growth [180]. As these compounds are prepared to support the plants during adverse environmental conditions, it is highly essential to stipulate standard norms for the production and the maintenance of the compound as altered environmental conditions such as pH, temperature, and so on could influence the formulation’s activity. Hence, it has been stipulated that the standard formulation should have a shelf-life period of 2 years, easy handling procedures, and should have an endurance to the temperature ranging from 5°C to 35°C [181]. It should also not be phytotoxic, cost effective, easily get dissolved in water, easy, and cheap availability of carrier materials, and should be compatible with agrochemicals [182]. Table 3 describes the various formulations available worldwide with its applications. Further, these formulations are available in two different forms namely solid and liquid forms.
Table 3: Description of commercially available bioactive compounds and biofertilizers produced from Trichoderma species.
| Trichoderma species | Commercial products barnd/name | Activity | Manufacturer details |
|---|---|---|---|
| Trichoderma harzianum | Root shield | Fungicide/fertilizer | BioWorks, New York (https://bioworksinc.com/?s=Trichoderma) |
| Trichoderma sp. | Mikrobs | Fertilizer | Arizona (https://www.arbico-organics.com/product/mikrobs-soil-amendment-bioinoculant/trichoderma-soil-borne-disease-resistance) |
| Trichoderma viride | Trichoderma viride powder | Fungicide/fertilizer | OrganigDews, Bio Organic, India |
| Trichoderma harzianum, Trichoderma polysporum | Binab T | Bioactive compound | BINAB Bio-Innovation AB, Sweden (http://www.algonet.se) |
| Trichoderma harzianum | Plant shield | Bioactive compound | BioWorks, Inc., USA (http:// www.bioworksbiocontrol.com) |
| Trichoderma spp. | Antagon | Bioactive compound | DeCeusterMeststoffenN.V. (DCM), Belgium (http:// www.agreoBiologicals.com) |
| Trichoderma spp., Trichoderma harzianum, Trichoderma koningii | Promot Plus WP Promot PlusDD | Bioactive compound | Tan Quy, Vietnam |
| Trichoderma viride | Antagon TV | Bioactive compound | Green Tech Agroproducts, Tamil Nadu, India [181] |
| Trichoderma harzianum | Trichostar | Bioactive compound | Green Tech Agroproducts, Tamil Nadu, India [181] |
| Trichoderma virens | Gliostar | Bioactive compound | GBPUAT, Pantnagar, India [181] |
| Trichoderma sp. | Monitor | Bioactive compound | Agricultural and Biotech Pvt. Ltd. Gujarat, India [181] |
| Trichoderma viride, Trichoderma harzianum | Bioderma | Bioactive compound | Biotech International Ltd. India [181] |
| Trichoderma viride | Bio Fit | Bioactive compound | Ajay Biotech (India) Ltd. India [181] |
| Trichoderma viride | Ecofit | Bioactive compound | Hoechst Schering Afgro Evo Ltd, India [181] |
| Trichoderma viride | Trichoguard | Bioactive compound | Anu Biotech Int. Ltd. Faridabad, India [181] |
| Trichoderma viride | Biocon | Bioactive compound | Tocklai Experimental Station Tea Research Association, Jorhat (Assam), India [181] |
Kumar [182] have suggested that the solid formulations are available as dry dust, wet dust, capsules, and granules at the concentration of 108 to 109 propagules available in a gram of the carriers such as clay, compost, and adhesives such as Arabic gums and carboxymethylcellulose. Further, they are formulated by pulverizing and grinding the dried Trichoderma mats which are further mixed with the appropriate carriers for different applications. Similarly, liquid formulation is limited in production due to difficulty in handling and maintenance. They are generally applied through irrigation of the crops [181].
5. SUMMARY ON FEW REVIEWS AVAILABLE
Few other reviews are available explaining the beneficial role of Trichoderma spp. either as a biocontrol agent or as an effective biofertilizer. The antagonistic biocontrol activity exerted by Trichoderma spp. following the direct and indirect mechanisms and the influence of extrinsic factors such as available fungal pathogen, crop species, pH, available nutrient conditions in soil, iron concentration, and temperature has been elaborated by Benítez et al. [33]. Similarly, Zin and Badaluddin [20] have presented in detail the role of Trichoderma spp. as plant growth promoter, as a plant disease controlling agent, secondary metabolites produced, and their role in decomposition and bioremediation processes. Further, Nusaibah and Musa [134] have specifically explained the current updates on the mechanism of Trichoderma spp. in controlling stem rot of oil palm disease caused by the devastating fungi Ganoderma spp. Ty?kiewicz et al. [183] have reported in detail the various beneficial role of Trichoderma spp. along with their mechanism especially on the phytohormones and the 1-aminocyclopropane-1-carboxylate deaminase enzyme produced by the fungi. In 2018, Kamal et al. [19] have outlined the factual data and information on the commercialization of Trichoderma spp. biofertilizers and the widespread use of the biofertilizer among the farmers. They have also suggested that biofertilizers improves the uptake of micronutrients from the soil and enhances the production of plant growth stimulating hormones with their secondary metabolites. Likewise, Kubheka and Ziena [184] have detailed the sustainable role of Trichoderma spp. as biofertilizer and bio-fungicide.
6. CONCLUSION
This report reviews the importance of the application of Trichoderma as a biocontrol agent to control diseases in plants by suppressing the growth of the fungal pathogens and as a biofertilizer to improve plant growth and development in industrial agriculture. These eco-friendly alternatives can substitute the excessive use of synthetic products that can cause problems in the long term. There are many commercial mycofungicides and biofertilizers available that are produced from fungi such as Trichoderma globally. The biotechnological advances from these microorganisms such as fungi are immense and yet to be explored. Thus, more studies need to be explored on the development of sustainable biotechnological applications of the products developed on the biocontrol agents and biofertilizers.
7. FUTURE NEEDS AND LIMITATION
Although several studies have been carried out on the beneficial role of Trichoderma spp. as a biocontrol agent and biofertilizer, it is essential to well define the mode and mechanism of the species specific and pathogen specific antagonistic behavior expressed by the fungi. Also, it is imperative to ascertain the dose concentration of the plant growth stimulating metabolites and their activity specific to each plant species.
8. AUTHOR’S CONTRIBUTION
All authors of the paper have made substantial contributions in conceptualization and designing of the manuscript, data acquisition and interpretation of the results, and drafting and revising the manuscript with all the possible intellectual content. Further all the authors mutually agree to submit to the manuscript; approved the version to be published; and agreed to be accountable for all aspects of the work. All the authors are eligible to be an author as per the International Committee of Medical Journal Editors (ICMJE) requirements/guidelines.
9. FUNDING
All authors would like to thank Universiti Brunei Darussalam for the research grant UBD/RSCH/URC/NIG/1.0/2019/003.
10. Conflict of Interest
The authors have mutually agreed to submit the manuscript to the journal and declare no financial or other conflict of interest in the work discussed.
11. ETHICAL APPROVALS
This study does not involve experiments on animals or human subjects.
12. Data availability
Study does not involve any huge data acquisition and the corresponding author may be contacted for further assistance of the subject discussed.
13. PUBLISHER’S NOTE
This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.
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