Trichoderma Species as Biocontrol Inoculant in Crop Rhizosphere: Comparison
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Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by M Nazrul Islam.

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. 

  • Trichoderma
  • metabolites
  • root exudates

1. Trichoderma Species as a Commercial Biofungicide

Trichoderma is a filamentous fungus beneficial for its multi-prong action against numerous plant pathogens [27][1]. 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][2]. 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][3]. 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][4]. T. afroharzianum is the mostly reported strain used as an active ingredient in several commercial biocontrol products [30,31][4][5]. 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][6].
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][7]. 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][7]. The dry powder or dust of Trichoderma is used to coat seed for seed treatment just before sowing [34,35][8][9]. 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][10]. 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][10]. For instance, across the globe, several Trichoderma–based commercial bioformulations are used in controlling plant pathogenic fungi are listed in Table 1.
Table 1. Trichoderma–based commercial bioformulations controlling plant pathogenic fungi.
Trichoderma–Based Bioformulation/Tradename Trichoderma Species Target Pathogens Manufacturer References
Agroguard WG™ T. harzianum Phoma, Pythium, Rhizoctonia, Sclerotinia, and Sclerotium Life Systems Technology S.A. (Colombia) [34][8]
Antagon WP™ T. harzianum Botrytis, Ceratocystis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and Sclerotium Bio Ecologico Ltd. (Colombia) [34][8]
Binab TF T. polysporum Fusarium, Pythium, Rhizoctonia, Sclerotinia, and Sclerotium BINAB Bio-Innovation AB (USA) [35][9]
Bioderma H T. harzianum Alternaria, Ascochyta, Cercospora, Colletotrichum, Fusarium, Phytophthora, Pythium, Macrophomina, Myrothecium, and Ralstonia Biotech International Ltd. (India) [34][8]
BioFungo™ T. virens Botrytis cinerea and Sphaerotheca pannosa Orius Biotecnologia (Colombia) [34][8]
ECO-77™ T. harzianum Botrytis and Eutypa Plant Health Products (South Africa) [34][8]
ECO-T™ T. harzianum Fusarium, Phytophthora, Pythium, and Rhizoctonia Plant Health Products (South Africa) [34][8]
Ecoderma T. virens Botrytis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and Sclerotium BigHaat Agro Ltd. (India) [35][9]
Ecotrich ES™ T. harzianum Rhizoctonia solani, Pythium, and Sclerotinia Ballagro Agro Tecnologia Ltd. (Brazil) [34][8]
Esquive T. atroviride Pythium and Rhizoctonia Agrauxine (France) [35][9]
Floragard T. hamatum Fusarium, Pythium, Rhizoctonia solani, and Sclerotinia homeocarpa Sellew Associates LLC (USA) [35][9]
FoliGuard™ T. hamatum Alternaria, Botrytis cinerea, Cladosporium, Oidium, and Sphaeroteca pannosa Live Systems Technology S.A. (Colombia) [34][8]
Lycomax T. viride Soil-borne pathogens Russell IPM (UK) [34][8]
Natibiol™ T. viride Rhizoctonia Probiagro S.A. (Venezuela) [34][8]
PlantShield™/RootShield™ T. harzianum Fusarium, Pythium, Rhizoctonia solani, and Sclerotinia homeocarpa Bioworks (USA) [34][8]
T-Gro T. harzianum Botrytis, Ceratocystis, Fusarium, Pythium, and Rhizoctonia Dagutat Biolab (USA) [35][9]
Trianum™ T. harzianum Soil-borne pathogens Koppert BV (The Netherlands) [34,35][8][9]
Tricho™ T. harzianum Alternaria, Arrmilaria, Botrytis, Fusarium, Pythium, Rhizoctonia, Rosellinia, Sclerotinia, and Sclerotium Orius Biotecnologia (Colombia) [34][8]
Trichodermil™ T. harzianum Botrytis ricini, Fusarium, Phytophthora capsici, Phytophthora palmivora, Rhizoctonia, and Sclerotinia sclerotiorum Itaforte BioProdutos (Brazil) [34][8]
Trichodex T. harzianum Colletotrichum, Fusarium, Phytophthora, and Pythium, Macrophomina Makhteshim chemical works Ltd. (USA) [35][9]
Trichosav T. harzianum Soil-borne pathogens Centros de Reproduccion de Medios Biologicos (Cuba) [34][8]
Trichosoil T. harzianum Fusarium Lage S.A. (Uruguay)  
Tusal T. asperellum Fusarium, Pythium, and Rhizoctonia solani Isagro (USA) [35][9]
Virisan T. asperellum Phytophthora, and Pythium Isagro (USA) [35][9]
VinevaxTM–Trichoprotection™ T. harzianum Armillaria, Botryosphaeria stevensii, Chondrostereum purpureum, Eutypa lata, and Phaeomoniella chlamydospor Agrimm Technologies Ltd. (New Zealand) [34,35][8][9]

2. 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][11]. 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][11]. 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][12]. 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][13]. 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][14].
The exchange of root exudates and other signaling molecules between Trichoderma and plants is complex and not well characterized [40][15]. 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][16]. 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][15]. 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][17]. 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][18].

3. 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][19]. 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][20][21][22] (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][23][24]. 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][18]. 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][25].
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][26]. 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][27]. Therefore, it is expected that the transgenes inserted in the plant-host increase the resistance level against a variety of plant pathogens [53][28]. 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][29].
Table 2.
 A list of metabolites and chemical compounds secreted by 
Trichoderma
 species affects soil pathogenic fungi.
Metabolites Compound Trichoderma Species Target Fungal Pathogens References
Anthraquinones 1,8-dihydroxy-3-methylanthraquinone,

1-hydroxy-3-methylanthraquinone and

6-methyl-1,3,8-trihydroxyanthraquinone		 T. harzianum Fusarium oxysporum, Macrophomina phaseolina, Rizoctonia solani, and Sclerotium rolfsii [55][30]
1,8-dihydroxy-3-methylanthraquinone and

1-hydroxy-3-methylanthraquinone		 T. harzianum Gaeumannomyces graminis var. tritici, and Pythium ultimum [56][31]
Azaphilones Harziphilone, Fleephilone and

T22azaphilone		 T. harzianum G. graminis var. tritici, P. ultimum, and R. solani [57][32]
T22azaphilone T. harzianum Leptosphaeria maculans, and Phytophthora cinnamomi [58][33]
Epipolythiodio-xopiperazines Gliotoxins T. virens M. phaseolina, Pythium aphanidermatum, Pythium deharyanum, Rizoctonia bataticola, R. solani, and S. rolfsii [1][34]
Gliovirin T. longibrachiatum R. solani [1][34]
Gliovirin T. virens P. ultimum [1][34]
Koninginins koninginins A, B, D, E, and G T. aureoviride

T. harzianum and T. koningii		 G. graminis var. tritici [59][35]
koninginins A, B, and D T. koningiopsis F. oxysporum, F. solani, and S. rolfsii [59][35]
koninginin D T. harzianum and T. koningii Bipolaris sorokiniana, F. oxysporum, P. cinnamomi, and Pythium middletonii [6][36]
Lactones aspinolide C T. arundinaceum Fusarium sporotrichioides [60][37]
Cerinolactone T. cerinum Rosellinia necatrix [60][37]
Cremenolide T. cremeum. F. oxysporum and R. solani [60][37]
Peptaibols trichokonins VI, VII, and VIII T. koningii F. oxysporum, R. solani, and Verticillium dahliae [55][30]
Trichokonin VI T. pseudokoningii F. oxysporum, Phytophthora parasitica, and V. dahlia [55][30]
Polyketides Harzianolide and

Dehydro Harzianolide		 T. harzianum F. oxysporum and R. solani [61][38]
6-pentyl-α-pyrone T. harzianum

T. koningii

T. viride and Trichoderma spp.		 R. solani [61][38]
6-pent-1-enyl-α-pyrone T. harzianum and T. viride R. solani [61][38]
Massoilactone δ-decenolactone Trichoderma spp. R. solani and S. rolfsii [61][38]
Koninginia E, B, and A T. harzianum and T. koningii G. graminis var. tritici [57][32]
Koninginin D and

Seco-koninginin		 T. harzianum G. graminis var. tritici [57][32]
Koninginin C T. koningii G. graminis var. tritici [57][32]
Pyridones Harzianopyridone T. harzianum G. graminis var. tritici, L. maculans, P. cinnamomi, P. ultimum, and R. solani [57][32]
Pyrones 6-Pentyl pyrone (6-PP) T. harzianum, T. koningii, and T. viride F. oxysporum and R. solani [62][39]
Viridepyronone T. viride S. rolfsii [62][39]
Steroids Stigmasterol T. harzianum and T. koningii F. oxysporum, M. phaseolina, R. solani, and S. rolfsii, [57][32]
Terpenes

(trichothecenes)		 Trichodermin T. polysporum

T. sporulosum

T. reesei and T. virens		 R. solani [63][40]
Harzianum A T. harzianum F. oxysporum [63][40]
Mycotoxin T2 T. lignorum R. solani and S. rolfsii [63][40]
Terpenes

(triterpenes)

(sterols)		 Ergokonin A T. koningii

T. longibrachiatum and T. viride		 Phoma spp. [64][41]
Viridin T. koningii

T. virens and T. viride		 F. oxysporum and R. solani [64][41]
Trichothecenes Trichodermin T. brevicompactum R. solani [65][42]
Trichodermin T. harzianum F. oxysporum and R. solani [66][43]
Agronomy 12 00900 g001 550
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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