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Review

Microbial Metabolomics Interaction and Ecological Challenges of Trichoderma Species as Biocontrol Inoculant in Crop Rhizosphere

by
Saleh Ahmed Shahriar
1,
M. Nazrul Islam
2,
Charles Ng Wai Chun
3,
Parwinder Kaur
4,
Md. Abdur Rahim
5,
Md. Mynul Islam
6,
Jasim Uddain
7 and
Shafiquzzaman Siddiquee
8,*
1
School of Biological Sciences, Universiti Sains Malaysia, Gelugor 11800, Penang, Malaysia
2
Morden Research and Development Centre, Agriculture and Agri-Food Canada, Morden, MB R6M 1Y5, Canada
3
School of Industrial Technology, Bioprocess Technology Division, Universiti Sains Malaysia, Gelugor 11800, Penang, Malaysia
4
UWA School of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, Australia
5
Department of Genetics and Plant Breeding, Sher-e-Bangla Agricultural University, Dhaka 1207, Bangladesh
6
Plant Pathology Division, Bangladesh Agricultural Research Institute, Gazipur 1701, Bangladesh
7
Department of Horticulture, Sher-e-Bangla Agricultural University, Dhaka 1207, Bangladesh
8
Biotechnology Research Institute, Universiti Malaysia Sabah, Jalan UMS, Kota Kinabalu 88400, Sabah, Malaysia
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(4), 900; https://doi.org/10.3390/agronomy12040900
Submission received: 3 March 2022 / Revised: 4 April 2022 / Accepted: 6 April 2022 / Published: 8 April 2022
(This article belongs to the Special Issue From Soil-Plant-Microbial Interactions to New-Concept Biopesticides and Biofertilizers)
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Abstract

:
The fungal species belonging to the genus Trichoderma has been globally recognized as a potential candidate of biofertilizer and biocontrol agent to prevent devastating soil-borne fungal pathogens and enhance growth and productivity of agricultural crops. The antagonistic activity of Trichoderma to pathogenic fungi is attributed to several mechanisms including antibiosis and enzymatic hydrolysis, which are largely associated with a wide range of metabolites secreted by the Trichoderma species. Besides suppressing target pathogens, several metabolites produced by Trichoderma species may act against non-pathogenic beneficial soil microbial communities and perform unintended alterations within the structures and functions of microbial communities in the crop rhizosphere. Multiple microbial interactions have been shown to enhance biocontrol efficacy in many cases as compared to bioinoculant employed alone. The key advances in understanding the ecological functions of the Trichoderma species with special emphasis on their associations with plant roots and other microbes exist in the crop rhizosphere, which are briefly described here. This review focuses on the interactions of metabolites secreted by Trichoderma species and plant roots in the rhizosphere and their impacts on pathogenic and non-pathogenic soil microbial communities. The complex interactions among Trichoderma–plants–microbes that may occur in the crop rhizosphere are underlined and several prospective avenues for future research in this area are briefly explored. The data presented here will stipulate future research on sustainably maximizing the efficiency of Trichoderma inoculation and their secondary metabolites in the crop soil ecosystem.

1. Introduction

The Trichoderma species under the Hypocreaceae family has been commercially formulated as biological inoculants or biofungicides worldwide [1,2,3]. More than 50% of registered biofungicides against soil-borne pathogens are formulated based on Trichoderma [4]. Trichoderma species have a wide distribution and ecological plasticity due to their ability to generate a broad range of lytic enzymes to degrade substrates, a flexible metabolism, and high resistance to microbial inhibitors [5]. Therefore, Trichoderma is the most used bioinoculant due to its numerous beneficial characteristics, including producing several secondary metabolites, such as antibiotics, peptaibols, and other bioactive compounds with antibiosis properties for parasitizing soil pathogenic fungi [6]. As a result, mycoparasitism and antibiosis are thought to be the most important biocontrol mechanisms in Trichoderma species.
The effect of Trichoderma species as a biocontrol agent cannot be generalized since it has both harmful and beneficial impacts on pathogens and growth promotion that have been extensively studied [7,8]. Reports show that multidirectional metabolomic interactions occur in the soil ecosystem due to the interactions with introduced Trichoderma inoculants, plant root exudates, and resident microbial communities (e.g., antagonism or synergism) [9,10]. The species diversity of existing microbial communities and their richness in the root microbes results in the intra- and interspecies relationship among their members. Secondary metabolites (SMs) play a major role in executing these interactions as chemical signals [11].
In soil, how Trichoderma inoculants interact with other non-target and non-pathogenic microorganisms, which are inherently beneficial for crop productivity, is relatively lesser understood [12,13,14,15]. Several studies showed a significant increase in fungal population in rhizosphere soil upon inoculation of Trichoderma strains; consequently, this increased fungal population reduced the bacterial population [16]. In another study, Trichoderma koningii inoculation reduced the resting spore germination of arbuscular mycorrhizal (AM) fungi (e.g., Glomus spp.), which are considered key fungal communities responsible for enhancing soil biofertility and crop productivity [17,18,19]. For example, the volatile metabolites secreted by T. koningii inoculant suppressed spore germination of AM fungi and decreased the population of the beneficial Azospirillum species as well. Thus, Trichoderma application to control soil-borne pathogens and growth improvement requires comprehensive investigation considering the interactions not only with pathogens, but also with microbial communities already present in crop soils.
Overall, soil microbes contribute significantly to soil structure, fertility, and pathogens suppression [20,21]. At the same time, the release of root exudates (metabolites) influences the structure of the soil microbial population and its enzymatic activity, which provide essential nutrients to plants by decomposing and mineralizing the soil organic matters [22,23]. Furthermore, soil microbes are the primary source and mediators, such as biochemical changes during nutrients recycling, and hence play a critical role in biogeochemical process [24,25]. Research has sought to characterize these beneficial microbes from diverse agricultural ecosystems to obtain a better knowledge of the biodiversity of the soil microbial communities. However, the plant species and soil types primarily influence the composition of the soil microbial population; the interactions in the soil ecosystems are very complicated, particularly among the plants and soil microbes [26].
In this review, we categorized the effect of the metabolomic compounds secreted by different Trichoderma species on soil pathogenic (fungi), non-pathogenic (fungi and bacteria) microbial communities, and soil enzymatic activities, and outlined the ecological challenges of Trichoderma as a biofungicide/biocontrol inoculant in crop rhizosphere.

2. Trichoderma Species as a Commercial Biofungicide

Trichoderma is a filamentous fungus beneficial for its multi-prong action against numerous plant pathogens [27]. Biofungicide is an important approach against some notable plant pathogens. Several Trichoderma strains have been recognized as a potential source to formulate biofungicide because of their suitability to reduce disease incidences caused by several fungal plant pathogens [28]. Species belonging to the Trichoderma harzianum complex are mostly found in various soil habitats and on plant decay materials, and have shown parasitism to other fungi [29]. Recently, a few commercial strains, such as Trichoderma afarasin, T. afroharzianum, T. atrobrunneum, T. camerunense, T. endophyticum, T. guizhouense, T. harzianum, T. inhamatum, T. lentiforme, T. lixii, T. neotropicale, T. pyramidale, T. rifaii, and T. simmonsii, have been identified as effective biofungicide formulations [30]. T. afroharzianum is the mostly reported strain used as an active ingredient in several commercial biocontrol products [30,31]. The taxonomy of the T. harzianum complex formalized the phylogenetic progenies and opened new prospects for the revelation of biological utilities, particularly controlling the plant pathogens. For instance, newly recognized T. lentiforme and T. neotropicale showed strong antagonistic actions against the Moniliophthora roreri pathogen causing frosty pod rot disease of the cacao tree (Theobroma cacao) [32].
T. viride has also been extensively used as a well-known biofungicide that protects the plant from fungal diseases striving with systemic negative effects on foliar leaves and seedcoat. Bio-formulations based on T. viride work as potential biofungicides against seed-borne and soil-borne fungal pathogens including Armillaria, Pythium, and Rhizoctonia [33]. Moreover, Trichoderma species play a significant role against seed-borne fungi, such as Fusarium sp., M. phaseolina, and R. solani, which cause pre-harvest and post-harvest losses in cotton, cowpea, mungbean, sorghum, soybean, and tomatoes [33]. The dry powder or dust of Trichoderma is used to coat seed for seed treatment just before sowing [34,35]. T. harzianum, T. virens, and T. viride were proven as potential seed protectants against the Pythium sp. and R. solani. Incubation of Trichoderma–treated seeds under warm and humid conditions right before radical emergence, results in rapid and uniform seedling emergence [36]. Trichoderma germinates conidial masses on the seed surface and forms a layer surrounding the primed seeds. These primed seeds are capable of tolerating the adverse conditions of soil habitats, such as vegetable seedlings treated with Trichoderma spore or cell suspension showed antagonistic to damping-off disease. Trichoderma was successfully applied in aerial plant parts to control the decay fungi in wounded shrubs and trees [36]. For instance, across the globe, several Trichoderma–based commercial bioformulations are used in controlling plant pathogenic fungi are listed in Table 1.

3. Effects of Trichoderma Metabolites on Plant Root Exudates

The signaling between Trichoderma and plant roots is often performed with root-derived chemicals (Table 2). Plant roots exude various organic compounds into the rhizosphere, which create and promote contact with Trichoderma [37]. Sucrose is a key molecule in carbohydrate-mediated plant signaling. Plant cells degrades sucrose to provide a carbon source for Trichoderma during Trichoderma–plant interactions [37]. T. virens intracellular invertase (TvInv) is responsible to hydrolyze sucrose and production of normal T. virens in the presence of sucrose. A plant-like sucrose transporter (TvSut) carries sucrose from the plant to Trichoderma during their beneficial interactions [38]. The ThPTR2 gene encodes the PTR family di/tripeptide transporter, which is found in T. harzianum. The secreted proteins that are found in plant–pathogen and plant–mycorrhizal interactions, also play a significant role in Trichoderma–plant interactions. Trichoderma species produce and regulate hormonal signals that help to colonize in plant roots [3]. Auxin-induced root formations (e.g., increased number of root hairs) increase the total area of the absorptive surface in the root zones, making nutrient absorption easier and resulting in increased plant growth [39].
The exchange of root exudates and other signaling molecules between Trichoderma and plants is complex and not well characterized [40]. Thus, several antibiotics, toxins, and plant antimicrobial agents affect the Trichoderma species in the crop rhizosphere. For example, benzoic acid, cinnamic acid, ferulic acid, phenolic acids, vanillic acid, 3-phenyl propionic acid, and 4-hydroxybenzoic acid can inhibit the growth of Trichoderma [41]. However, some Trichoderma species induce root branching and increase shoot biomass by the presence of auxin-like compounds, which help to exchange these root exudates and signaling molecules between Trichoderma and plants in crop rhizosphere [40]. The ATP cassette-binding cell membrane pump of Trichoderma species is an important part of a comprehensive, potent cell detox system that explains the ability of Trichoderma to cope with various chemical stresses. In addition to co-inoculating other useful organisms such as the AM fungi, the Trichoderma species appears to have a role to play in attenuating plant hormone reactions to the root colonization process [42]. The effective colonization of the Trichoderma species on the roots of their hosts implies a reprogramming of the plant, with improved growth, yield, and pathogen resistance [43].

4. Effects of Trichoderma Metabolites on Soil and Root Pathogens

Trichoderma species are commonly found on plant root surfaces in various soil habitats where they control the soil-borne pathogens causing plant root diseases [44]. The most versatile strains from the Trichoderma genus, including Trichoderma arundinaceum, T. asperellum, T. atroviride, T. citrinoviride, T. cremeum, T. crissum, T. gamsii, T. hamatum, T. harzianum, T. pseudo-koningii, T. koningii, T. koningiopsis, T. longibrachiatum, T. longipile, T. ovalisporum, T. polysporum, T. reesei, T. saturnisporum, T. spirale, T. virens, and T. viride, secrete diverse chemical compounds [45,46,47] (Table 2). A large number of soil-borne fungi are capable of generating chemicals that are recognized for their antifungal efficiency. Trichoderma species possess the fungicidal and fungistatic characteristics as they generate various cell wall-degrading enzymes and secondary metabolites (SMs) [48,49]. These metabolites enhance the plant defense response when attacked by phytopathogens. Secreted antimicrobial compounds during the Trichoderma–mediated defense response pathways are often associated with the barriers of pathogen entry into the plant cells [43]. For example, the accumulation of secondary phenolic metabolites plays a crucial role in plant defense mechanisms against various pathogens. Trichoderma produces various peptides, proteins, and low molecular weight compounds, which are involved in biochemical resistance to pathogens and induce resistance in plants [50].
Various groups of compounds are secreted by the Trichoderma species trigger to induce the defense reactions in plants. Celluloses produced by T. harzianum have been proven to act as an elicitor for systemic acquired resistance (SAR) by causing peroxides and chitinase activity. Systemic plant reactions occur via the JA/ethylene signaling pathway (Figure 1). Trichoderma has been shown to release these enzymes or otherwise functioning proteins, avirulence gene (Avr) encoded homologous proteins, oligosaccharides, and other low molecular weight compounds [51]. The chitinase enzymes are commonly known as plant gene-encoding enzymes, which degrade cell walls, and are used to induce plant resistance against phytopathogens. In terms of antifungal efficiency, the chitinase genes from Trichoderma showed dominant expression over the corresponding plant genes resulting in improved pathogenic resistance [52]. Therefore, it is expected that the transgenes inserted in the plant-host increase the resistance level against a variety of plant pathogens [53]. The Trichoderma gene chit42 encodes a powerful endochitinase enzyme that exhibits strong antifungal activity against a broader range of plant pathogens as compared to other chitinolytic enzymes. The constitutive expressions of Trichoderma genes in plants have shown higher levels and improved resistance against soil-borne plant pathogens [54].
Table
Table 2. A list of metabolites and chemical compounds secreted by Trichoderma species affects soil pathogenic fungi.
Table 2. A list of metabolites and chemical compounds secreted by Trichoderma species affects soil pathogenic fungi.
MetabolitesCompoundTrichoderma SpeciesTarget Fungal PathogensReferences
Anthraquinones1,8-dihydroxy-3-methylanthraquinone,
1-hydroxy-3-methylanthraquinone and
6-methyl-1,3,8-trihydroxyanthraquinone		T. harzianumFusarium oxysporum, Macrophomina phaseolina, Rizoctonia solani, and Sclerotium rolfsii[55]
1,8-dihydroxy-3-methylanthraquinone and
1-hydroxy-3-methylanthraquinone		T. harzianumGaeumannomyces graminis var. tritici, and Pythium ultimum[56]
AzaphilonesHarziphilone, Fleephilone and
T22azaphilone		T. harzianumG. graminis var. tritici, P. ultimum, and R. solani[57]
T22azaphiloneT. harzianumLeptosphaeria maculans, and Phytophthora cinnamomi[58]
Epipolythiodio-xopiperazinesGliotoxinsT. virensM. phaseolina, Pythium aphanidermatum, Pythium deharyanum, Rizoctonia bataticola, R. solani, and S. rolfsii[1]
GliovirinT. longibrachiatumR. solani[1]
GliovirinT. virensP. ultimum[1]
Koningininskoninginins A, B, D, E, and GT. aureoviride
T. harzianum and T. koningii		G. graminis var. tritici[59]
koninginins A, B, and DT. koningiopsisF. oxysporum, F. solani, and S. rolfsii[59]
koninginin DT. harzianum and T. koningiiBipolaris sorokiniana, F. oxysporum, P. cinnamomi, and Pythium middletonii[6]
Lactonesaspinolide CT. arundinaceumFusarium sporotrichioides[60]
CerinolactoneT. cerinumRosellinia necatrix[60]
CremenolideT. cremeum.F. oxysporum and R. solani[60]
Peptaibolstrichokonins VI, VII, and VIIIT. koningiiF. oxysporum, R. solani, and Verticillium dahliae[55]
Trichokonin VIT. pseudokoningiiF. oxysporum, Phytophthora parasitica, and V. dahlia[55]
PolyketidesHarzianolide and
Dehydro Harzianolide		T. harzianumF. oxysporum and R. solani[61]
6-pentyl-α-pyroneT. harzianum
T. koningii
T. viride and Trichoderma spp.		R. solani[61]
6-pent-1-enyl-α-pyroneT. harzianum and T. virideR. solani[61]
Massoilactone δ-decenolactoneTrichoderma spp.R. solani and S. rolfsii[61]
Koninginia E, B, and AT. harzianum and T. koningiiG. graminis var. tritici[57]
Koninginin D and
Seco-koninginin		T. harzianumG. graminis var. tritici[57]
Koninginin CT. koningiiG. graminis var. tritici[57]
PyridonesHarzianopyridoneT. harzianumG. graminis var. tritici, L. maculans, P. cinnamomi, P. ultimum, and R. solani[57]
Pyrones6-Pentyl pyrone (6-PP)T. harzianum, T. koningii, and T. virideF. oxysporum and R. solani[62]
ViridepyrononeT. virideS. rolfsii[62]
SteroidsStigmasterolT. harzianum and T. koningiiF. oxysporum, M. phaseolina, R. solani, and S. rolfsii,[57]
Terpenes
(trichothecenes)		TrichoderminT. polysporum
T. sporulosum
T. reesei and T. virens		R. solani[63]
Harzianum AT. harzianumF. oxysporum[63]
Mycotoxin T2T. lignorumR. solani and S. rolfsii[63]
Terpenes
(triterpenes)
(sterols)		Ergokonin AT. koningii
T. longibrachiatum and T. viride		Phoma spp.[64]
ViridinT. koningii
T. virens and T. viride		F. oxysporum and R. solani[64]
TrichothecenesTrichoderminT. brevicompactumR. solani[65]
TrichoderminT. harzianumF. oxysporum and R. solani[66]

5. Effects of Trichoderma Metabolites on Soil Non-Pathogenic Fungal Communities

Microbial community structure, biodiversity, and functions are crucial for maintaining agroecosystem sustainability and productivity [67,68]. Very little is known about how Trichoderma interacts with non-pathogenic microbial communities. Trichoderma species secrete numerous cell wall-degrading enzymes such as cellulases, chitinases, glucanases, proteinases, and xylanases, which can substantially degrade the microbial cells (including pathogens) in soil habitats to absorb nutrients and persist longer. Thus, changing or altering the structure and functions of microbial populations, particularly fungal and bacterial communities [69,70].
Secondary metabolites (SMs) are secreted by Trichoderma play significant roles in signaling, developing, and establishing interactions with plants and soil microbes (Table 3). Trichoderma produces numerous secondary metabolites, such as peptaibols, polypeptides, pyrons, siderophores, steroids, terpenes, etc. [62]. The effectiveness of using Trichoderma in agriculture depends on their metabolic activity and the type of interaction with plants and other microbes. These fungi effectively colonize the plants roots and soil rhizosphere, and produce several metabolites with anti-microbial features [27]. For instance, T. atroviride and T. harzianum have developed different major antibiotics, such as azaphilone, butenolide, harzianolide, hydrazinopyridine, 1-hydroxy-3-methyl-anthraquinone, 1,8-dihydroxy-3-methyl-anthraquinone, and 6-Pentyl pyrone (6-PP) [71,72]. This low molecular weight, non-polar, volatile compounds (i.e., 6-PP) yield a high concentration of antibiotics in the soil environments, which influence the diversity, composition, and functional attributes of the long-distanced soil microbial community. On the other hand, the polar antibiotics and peptaibols affect the production of microbial hyphae within short-distanced ranges [73]. However, the contribution of other secondary metabolites (i.e., pyrones) by Trichoderma and their synergisms with other soil-root associated chemical compounds to beneficial soil microbial communities has not yet been well understood [74,75,76].
T. koningii producing volatile compounds induced the reduction in resting spore germination of non-pathogenic AM fungi (e.g., G. mosseae) [17]. However, these volatile compounds did not affect the mycelial growth of G. mosseae, affecting the spores produced only in the resting phase. Trichoderma inoculation on mycorrhizal maize plants reduced Azospirillum populations in soil [77]. This operation was only found in natural mycorrhizal plants as compared to non-mycorrhizal control plants. The relative abundance of fungal species was also found in the soil rhizosphere of black pepper (Piper nigrum L.). T. harzianum caused considerable alterations in the metabolic profiles of the black pepper rhizosphere, resulting in a lower number of metabolized compounds; although, absorbance was considerably greater for a specific set of metabolites in which Trichoderma was applied [78].
The treatment with T. harzianum MTCC 5179 altered the structure and functions of fungal communities such as Mortierella verticillata, Oidiodendron maius, Pseudogymnoascus pannorum, Rhizophagus irregularis, Talaromyces stipitatus, and T. harzianum [78]. Significant variations were observed among the fungal communities in the soil rhizosphere due to Trichoderma inoculation. For instance, Gibberella and Phoma were found as the dominant fungal genera, whereas relative abundances of other fungi, such as Monographella, Mortierella, Penicillium, Rhizophlyctis, Sphaerosporella, and Trichoderma, were reduced. Another study showed that after inoculation of Trichoderma, the relative abundance of Trichoderma was 98.41%, including resident Trichoderma species, while the relative abundances of other genera were reduced [79]. In contrast, inoculation of T. atroviride I-1237 resulted in a significant increase in the density of the other soil fungal community [80]. Similarly, T. longibrachiatum inoculation enhanced the capacity of microbial communities utilizing the carbon source that was the highest in rhizosphere soil [81].

6. Effects of Trichoderma Metabolites on Soil Bacterial Communities

Several metabolites released by Trichoderma species have been shown to substantially inhibit the growth of diverse bacterial strains in the tomato rhizosphere. Occasionally, volatile compounds (VCs) produced by indigenous bacterial communities affected the growth of Trichoderma and their secretion of antifungal/antibacterial metabolites. This counter-secretion within the rhizosphere raised the questions of whether these Trichoderma species significantly change the rhizosphere bacterial communities during biocontrol and how the consequent alterations influence soil and plant health. Trichoderma species strongly inhibiting the bacterial population implies that VCs might be used as soil fumigants. However, 373 distinct bacterial strains have been identified in the soil rhizosphere, though the specific activity of these microbes are still unknown in many cases [6,82,83].
Trichoderma has some fundamental functions to stimulate the plant beneficial bacteria to restrict pathogens through different mechanisms (Table 3) [84]. The non-target effects of T. harzianum, Bacillus megaterium, and Pseudomonas fluorescens were found on major actinomycetes and β-proteobacterial communities in soil rhizosphere [85]. T. harzianum and B. megaterium significantly increased the population of actinomycetes with greater abundance during the maturity stage of plants. Another study showed that Trichoderma inoculant reduced the total soil bacterial population of Pseudomonas fluorescens [16]. A study on biodegradation revealed, T. viride was inoculated together with a bacterial consortium of 195 strains [86]. After 12 months of observation of the biodegradation process, only 73 bacterial strains were found from the consortium population. T. viride proved to exert an antagonistic effect on the bacterial consortium; as a result, the lower relative abundance of bacterial communities was achieved, whereas higher relative abundance of bacterial communities was found in the control treatment. Gasoni et al. [87] found that the application of T. harzianum changed a particular group of compounds deferred from the uninoculated control, indicating that the inoculation of T. harzianum contributed to the growth of a distinct soil bacterial population, altering the microbial communities in the host rhizosphere.

7. Effects of Trichoderma Metabolites on Soil Enzyme Activities

The Trichoderma species applied in the crop rhizosphere affected soil enzyme activities. A variety of Trichoderma species substantially decreased the activities of β-glucosidase, chitobiosidase, and N-acetyl-β-D-glucosaminidage (NAGase) enzymes, thus inducing the plants to respond with their defense mechanisms [16]. These enzymes exhibited the alteration in microbial communities in the soil ecosystem [73] (Table 3). Enzymatic activities occurring in the soil are used to better understand the ecological functions of Trichoderma [88]. Several Trichoderma species reduced the activity of alkaline phosphatase resulting in the effective control of the soil-borne pathogen (P. ultimum). Different degrees of soil enzyme activities significantly inhibit the pathogenic effect of soil-borne fungi [16].
Trichoderma inoculation to AM fungi-colonized plants (G. deserticola) reduced phosphatase activity [73]. A significant increase in chitinase activity was found in the soil with Trichoderma inoculation of natural mycorrhizal fungi-colonized plants (121%) and non-mycorrhizal plants (151%). However, it considerably reduced the enzymatic activity of trehalase by 47%. The imbalance structure of the soil microbial community is the major reason for soil-borne diseases. Trichoderma species increase the contact area among the soil microbes and crop rhizosphere because of their strong colonization ability. Trichoderma species exhibit hyperparasitism due to their advantages of rapid growth and high vitality. The fungus secretes cell wall-degrading extracellular enzymes, such as cellulases, chitinases, glucanases, proteinases, and xylanases, which enhance the soil enzyme activity to repair soil health [89]. The inoculation of Trichoderma increases nutrient availability, nutrient recycling activity, and microbial biomass by degrading microbial cells, thus leading to the improvement of structure and function of the soil microbial community [90,91]. Trichoderma inoculation significantly enhances the nutrient contents and enzymatic activity in rhizosphere of Pinus sylvestris var. mongolica seedlings. T. virens ZT05 was proven to have a greater impact as compared to T. harzianum E15 on nutrient availability and soil enzymatic activity in the crop rhizosphere [75].
Table
Table 3. Rhizosphere metabolites secreted by crop roots, Trichoderma, and soil microbial communities.
Table 3. Rhizosphere metabolites secreted by crop roots, Trichoderma, and soil microbial communities.
Metabolites (Enzymes)Trichoderma StrainsBacteriaFungiHost PlantReferences
1,8-dihydroxy-3-methylanthraquinoneTrichoderma hamatum TR1-4Bacillus spp.Gaeumannaomyces graminis var. tritici, and Rhizoctonia solaniWheat and Eggplant[92,93]
1-hydroxy-3-methylanthraquinoneT. harzianum 2413Pseudomonas spp.Phytophthora capsiciPepper[94]
1,8-dihydroxy-3-methylanthraquinoneT. harzianum T-22Pseudomonas fluorescens Q8r1-96Gaeumannaomyces graminis var. tritici, and Pyrenophora triticis-repentisWheat[95,96]
HarzianopyridoneT. harzianum T-1Pseudomonas aureofaciens AB244Fusarium oxysporum; Pythium ultimum, and R. solaniBean and Tomato[97,98]
6-pentyl-α-pyroneT. harzianum 1295-22Pseudomonas fluorescens VO61R. solaniCreeping bent grass and rice[99,100]
Trichorzianin TA
Trichorzianin TB		T. harzianum Th-87Stenotrophomonas maltophilia C3R. solaniEggplant and Tall fescue[92,101]
TrichoderminT. harzianum BAFC 742Bacillus subtilis GB03Sclerotinia sclerotiorumSoybean[102]
β-1,4 endoglucanaseT. longibrachiatum CECT 2606Serratia plymuthicaP. ultimumCucumber[101,103]
6-pent-1-enyl-α-pyroneT. viride WT-6Bacillus subtilis GB03R. solaniEggplant[96]
3,4-dihydroxycarotaneT. virens GL-21Pseudomonas fluorescens VO61P. ultimum and R. solaniCucumber and pea[104]
6-Pentyl pyrone (6-PP)T. virens GL-1, GL-21, GL-23Bacillus subtilis BACT-DR. solaniEggplant[92]
β-1,4 glucanase
3,4-dihydroxycarotane
Viridin		T. virens GL-3Burkholderia cepacia A3R, B. cepacia PHQM 100, Pseudomonas aureofaciens 63-28, and P. aureofaciens AB244 Fusarium graminearum, Pythium aphanidermatum, and P. ultimumBarley, Cucumber, Maize, and wheat[105,106,107,108,109]

8. Challenges and Future Research Directions

8.1. Efficacy of Trichoderma–Based Bioformulations

The compatibility of Trichoderma–based bioformulations needs to be assessed for integrated disease control approaches. Farmers should be encouraged to use Trichoderma–based formulations for environmentally sustainable disease control. To overcome the drawbacks of biological control techniques due to adverse environmental factors, formulations based on Trichoderma strains can be developed that act employ different mechanisms under both abiotic and biotic stresses in different climate zones. The utilization of microencapsulation technology can improve the effectiveness of Trichoderma–based bioformulations, and thus help to protect the pathogens in the field [34,35]. Furthermore, encapsulation is also capable to extend the shelf life of commercial products. This new technology will allow for the development of more effective pathogen control formulations in the pre- and post-harvest periods [34,35]. It is important to highlight the optimization and adjustments of microencapsulation processes employed to produce viable Trichoderma bioformulations for field applications. In this context, the association of the nanotechnology and biologically active compounds derived from Trichoderma on the surface of the nanoparticles can promote additional benefits for the efficient management of phytopathogens. However, it is a new technology, detailed investigation should be conducted to confirm that these nanoparticles do not have adverse effects on non-target organisms or cause any environmental contamination. Moreover, to commercialize these nanotechnological products obtained by the biogenic synthesis route, it is necessary to establish protocols for the standardization of the preparation of these biocontrol agents, as well as methods for scaling up production processes. There is tremendous potential to develop and commercialize novel products for the biological control of plant pathogens based on the genus Trichoderma, especially considering their applications in sustainable agriculture. In this review, we briefly discussed recently identified few commercial strains from the T. harzianum complex, which have been used to formulate biofungicides. We suggest researchers conduct further research to confirm how these commercial strains are effective in combating phytopathogens. Nowadays, silicon–based nanoparticles are also using in controlling microbes that exist in crop rhizosphere [110]. So, to see how Trichoderma bioformulations perform compared to silicon-based nanoparticles, further investigation needs to be assessed.

8.2. Ecological Challenges of Trichoderma Inoculant in Crop Rhizosphere

Metabolites and antibiotics produced by Trichoderma inoculant might affect not only phytopathogens, but also other beneficial or neutral soil microbes. The intensity of such impacts depends upon the inoculation period of biocontrol agents and the concentration of metabolites secreted [76]. The competition for nutrients might also be responsible for the alteration of the microbial population in the soil. The soil enzymatic activities are considered as the indicator for abiotic or biotic stresses with the presence of pathogens increasing their levels. Generally, inoculation of biocontrol agents has been shown to reduce biotic stress (soil pathogens) by decreasing the level of enzyme activities [111]. However, Trichoderma inoculant has certain non-target impacts because of the increase in enzymatic activities. It is highly challenging to monitor how bioinoculants affect non-target soil microbes in the rhizosphere and to understand their functions in the soil ecosystem. Future research is also needed to analyze the ecological consequences on non-target microbes, due to the application of bioinoculants into the crop rhizosphere.

8.2.1. Survival Fitness of Microbial Communities in Crop Rhizosphere

Soil microbes have been shown to play an essential role in soil formation, pathogen suppression, and nutrient solubilization and acquisition [112]. Bioinoculation is the most efficient and successful method for manipulating soil microbial communities [113,114]. However, there is very little evidence that these microbes can compete, develop, and operate since they are not reproducible on a long-term basis in natural agricultural soil. Moreover, a wide range of bioinoculants in agricultural fields is readily attacked by many predators and face nutrient competition from native microbes. The effective bioinoculants must be capable of forming interactions with other neighboring microbes, imitating the strongly structured crosslinks found in the native soil rhizosphere. The goal behind this strategy is to introduce beneficial microbial diversity into the plants, which will enhance the plant functions and provide resistance against phytopathogens [115,116]. A systemic approach is required for the successful engineering of soil microbes in the crop rhizosphere. However, knowledge of the basic mechanism of bioinoculants regarding how they are linked with the rhizosphere is important, it and also would improve sustainable crop production simply by enhancing the beneficial symbiotic associations among the plant–soil–microbial communities [117].

8.2.2. Trichoderma Affects Chemical Signals in Crop Rhizosphere

Interaction between plants and their associated microbes occurs in the soil rhizosphere through the exchange chemicals signals secreted by inoculated Trichoderma [118]. Signaling molecules can influence the metabolomic interactions among the soil microbes in either a positive or a negative way [119]. The interchange of these signaling molecules in Trichoderma–plant relationships is complex and not well characterized. However, in recent years, increased attention has been paid to understanding the chemical composition of Trichoderma–released secondary metabolites and their impacts on plant biochemical and physiological processes with potential applications in the field. Thus, we suggest researchers investigate how these signaling molecules interchange in Trichoderma–plant complex interactions.

8.2.3. Trichoderma Challenges Abiotic and Biotic Factors in Crop Rhizosphere

So far, around 100 compounds (e.g., alcohols, alkanes, amines, arenes, esters, phenols, etc.) have been identified in the rhizosphere soil [120]. Therefore, metabolomic interactions in the microbial community imply that soil chemical ecology might play significant roles in establishing biological inoculants and agroecosystem functions under diverse abiotic and biotic environments, such as soil–plant, pathogen–pathogen, microbe–microbe, microbe–pathogen, and indigenous versus non–indigenous inoculant interactions [18,118,120], which require further investigation to ensure introduced microbial inoculants such as Trichoderma can contribute in an eco-friendly and efficient manner in an agricultural production system (see soil ecological factors in Figure 2).
With the continuous growth of Trichoderma–based bioinoculants, we suggest researchers conduct further research to confirm how these commercial inoculants are effective to combat phytopathogens. To understand this multitalented biocontrol agent, further research should be conducted by which Trichoderma species can act against several lethal fungi as a potential biocontrol agent rather than minimizing the negative impact of Trichoderma on other resident microbes in the rhizosphere. To confirm an acceptable database for safe and sustainable usage of Trichoderma for better ecological balance, the extensive applications of any fungal species and their secondary metabolites for biological control management should be assessed. As a result, Trichoderma genomes can be a valuable source of candidate genes to produce transgenic or genetically modified plants resulting in improved resistance against abiotic and biotic stresses.

9. Conclusions

The successful establishment of biocontrol inoculants is reliant upon the multitrophic interactions including wide-ranging metabolites in the crop rhizosphere that play a vital role in shaping the microbial population, plant defense responses, and pathogen control. The molecular cross-talk among the contributors and understanding of these entire ecosystem processes would result not only in the safe use of biocontrol inoculants, but also expand our knowledge of the developmental process of soil and plant root diseases and their biocontrol mechanisms. The potentiality of the Trichoderma species in controlling soil-borne fungal pathogens is already renowned; however, reviewing this topic, no clear evidence of Trichoderma controlling bacterial plant pathogens in the soil rhizosphere has been found, conceivably an area that warrants further investigation. Future experiments on the mechanisms of possible synergistic actions by Trichoderma, soil microorganisms (pathogenic and non-pathogenic consortia), and environmental interactions should be performed. This could open up a new door for crop plants adapting to the Trichoderma as biological inoculants, minimizing negative impacts or unintended alterations to keystone functional soil microbiomes and crop productivity in diverse agroecosystems.

Author Contributions

M.N.I., S.A.S., C.N.W.C., M.M.I. and S.S. conceived and designed this revised version of the review article. M.N.I., S.A.S., M.A.R., P.K. and J.U. performed the investigation and metanalysis of this subject matter. M.N.I. and S.A.S. prepared the Figure 1 and Figure 2. S.A.S. wrote original draft. M.N.I., S.S. and S.A.S. wrote final draft for journal submission with contributions and reviewing support from C.N.W.C., P.K., M.A.R., M.M.I. and J.U. Funds were awarded to S.S. All authors have read and agreed to the published version of the manuscript.

Funding

We acknowledged the financial support from Universiti Malaysia Sabah Scheme UMS Great code number: GUG0276-2/2018.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Metabolites (antibiotics and enzymes) produced by Trichoderma induce plant defense responses against the pathogens: (A) Trichoderma released antibiotics, enzymes, and secondary metabolites (SMs) through metabolic pathways leading to antagonize the phytopathogens. (B) Signals involved in Trichoderma–plant interaction enhanced the plant defense responses.
Figure 1. Metabolites (antibiotics and enzymes) produced by Trichoderma induce plant defense responses against the pathogens: (A) Trichoderma released antibiotics, enzymes, and secondary metabolites (SMs) through metabolic pathways leading to antagonize the phytopathogens. (B) Signals involved in Trichoderma–plant interaction enhanced the plant defense responses.
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Figure 2. Soil ecological challenges and factors (1. Biotic, 2. Abiotic, and 3. Metabolomics) of Trichoderma bioinoculants’ survival, establishment, and function in crop rhizosphere.
Figure 2. Soil ecological challenges and factors (1. Biotic, 2. Abiotic, and 3. Metabolomics) of Trichoderma bioinoculants’ survival, establishment, and function in crop rhizosphere.
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Table
Table 1. Trichoderma–based commercial bioformulations controlling plant pathogenic fungi.
Table 1. Trichoderma–based commercial bioformulations controlling plant pathogenic fungi.
Trichoderma–Based Bioformulation/TradenameTrichoderma SpeciesTarget PathogensManufacturerReferences
Agroguard WG™T. harzianumPhoma, Pythium, Rhizoctonia, Sclerotinia, and SclerotiumLife Systems Technology S.A. (Colombia)[34]
Antagon WP™T. harzianumBotrytis, Ceratocystis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and SclerotiumBio Ecologico Ltd. (Colombia)[34]
Binab TFT. polysporumFusarium, Pythium, Rhizoctonia, Sclerotinia, and SclerotiumBINAB Bio-Innovation AB (USA)[35]
Bioderma HT. harzianumAlternaria, Ascochyta, Cercospora, Colletotrichum, Fusarium, Phytophthora, Pythium, Macrophomina, Myrothecium, and RalstoniaBiotech International Ltd. (India)[34]
BioFungo™T. virensBotrytis cinerea and Sphaerotheca pannosaOrius Biotecnologia (Colombia)[34]
ECO-77™T. harzianumBotrytis and EutypaPlant Health Products (South Africa)[34]
ECO-T™T. harzianumFusarium, Phytophthora, Pythium, and RhizoctoniaPlant Health Products (South Africa)[34]
EcodermaT. virensBotrytis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and SclerotiumBigHaat Agro Ltd. (India)[35]
Ecotrich ES™T. harzianumRhizoctonia solani, Pythium, and Sclerotinia Ballagro Agro Tecnologia Ltd. (Brazil)[34]
EsquiveT. atroviridePythium and RhizoctoniaAgrauxine (France)[35]
FloragardT. hamatumFusarium, Pythium, Rhizoctonia solani, and Sclerotinia homeocarpaSellew Associates LLC (USA)[35]
FoliGuard™T. hamatumAlternaria, Botrytis cinerea, Cladosporium, Oidium, and Sphaeroteca pannosa Live Systems Technology S.A. (Colombia)[34]
LycomaxT. virideSoil-borne pathogensRussell IPM (UK)[34]
Natibiol™T. virideRhizoctoniaProbiagro S.A. (Venezuela)[34]
PlantShield™/RootShield™T. harzianumFusarium, Pythium, Rhizoctonia solani, and Sclerotinia homeocarpaBioworks (USA)[34]
T-GroT. harzianumBotrytis, Ceratocystis, Fusarium, Pythium, and RhizoctoniaDagutat Biolab (USA)[35]
Trianum™T. harzianumSoil-borne pathogensKoppert BV (The Netherlands)[34,35]
Tricho™T. harzianumAlternaria, Arrmilaria, Botrytis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and SclerotiumOrius Biotecnologia (Colombia)[34]
Trichodermil™T. harzianumBotrytis ricini, Fusarium, Phytophthora capsici, Phytophthora palmivora, Rhizoctonia, and Sclerotinia sclerotiorumItaforte BioProdutos (Brazil)[34]
TrichodexT. harzianumColletotrichum, Fusarium, Phytophthora, and Pythium, MacrophominaMakhteshim chemical works Ltd. (USA) [35]
TrichosavT. harzianumSoil-borne pathogensCentros de Reproduccion de Medios Biologicos (Cuba)[34]
TrichosoilT. harzianumFusariumLage S.A. (Uruguay)
TusalT. asperellumFusarium, Pythium, and Rhizoctonia solaniIsagro (USA)[35]
VirisanT. asperellumPhytophthora, and PythiumIsagro (USA)[35]
VinevaxTM–Trichoprotection™T. harzianumArmillaria, Botryosphaeria stevensii, Chondrostereum purpureum, Eutypa lata, and Phaeomoniella chlamydospor Agrimm Technologies Ltd. (New Zealand)[34,35]
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Shahriar, S.A.; Islam, M.N.; Chun, C.N.W.; Kaur, P.; Rahim, M.A.; Islam, M.M.; Uddain, J.; Siddiquee, S. Microbial Metabolomics Interaction and Ecological Challenges of Trichoderma Species as Biocontrol Inoculant in Crop Rhizosphere. Agronomy 2022, 12, 900. https://doi.org/10.3390/agronomy12040900

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Shahriar SA, Islam MN, Chun CNW, Kaur P, Rahim MA, Islam MM, Uddain J, Siddiquee S. Microbial Metabolomics Interaction and Ecological Challenges of Trichoderma Species as Biocontrol Inoculant in Crop Rhizosphere. Agronomy. 2022; 12(4):900. https://doi.org/10.3390/agronomy12040900

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Shahriar, Saleh Ahmed, M. Nazrul Islam, Charles Ng Wai Chun, Parwinder Kaur, Md. Abdur Rahim, Md. Mynul Islam, Jasim Uddain, and Shafiquzzaman Siddiquee. 2022. "Microbial Metabolomics Interaction and Ecological Challenges of Trichoderma Species as Biocontrol Inoculant in Crop Rhizosphere" Agronomy 12, no. 4: 900. https://doi.org/10.3390/agronomy12040900

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