Applications of Trichoderma asperelloides in soybean production: a perspective based on bibliometric and experimental data

Aplicações de Trichoderma asperelloides na produção de soja: uma perspectiva baseada em dados bibliométricos e experimentais

Abstract

With the growing demand for more sustainable agricultural practices, the use of bioinputs has been gaining increasing prominence, especially in large-scale crops such as soybean [Glycine max (L.) Merrill]. Among the microorganisms that are attracting attention, Trichoderma asperelloides stands out not only for its potential in the biological control of diseases but also for its ability to support plant growth. This study was divided into two parts: the first is a bibliometric analysis to understand how T. asperelloides has been applied in agriculture, and the second is a field experiment to assess its effect as a growth promoter in soybeans. The bibliometric analysis revealed a significant increase in publications on this topic in recent years, with Brazil leading the research efforts. The field experiment yielded promising results: when 5 g of T. asperelloides was inoculated directly onto the seeds, a higher yield was achieved (4,486.2 kg ha⁻¹), attributed to improved nodule formation and enhanced root system development. Statistical analyses indicated a positive relationship between root growth, nodule formation, and plant productivity. These findings reinforce the importance of T. asperelloides as a valuable ally in increasing soybean yields in a more sustainable and environmentally friendly manner. Thus, T. asperelloides emerges as a viable alternative, contributing to a more efficient agriculture that aligns with current environmental challenges and global food security needs.

Keywords:
plant growth; bioinputs; sustainability; agriculture

Resumo

Com a crescente demanda por práticas agrícolas mais sustentáveis, o uso de bioinsumos vem ganhando cada vez mais destaque, especialmente em culturas de larga escala, como a soja [Glycine max (L.) Merrill]. Entre os microrganismos que estão atraindo atenção, Trichoderma asperelloides se destaca não apenas por seu potencial no controle biológico de doenças, mas também por sua capacidade de auxiliar o crescimento das plantas. Este estudo foi dividido em duas partes: a primeira é uma análise bibliométrica para entender como T. asperelloides tem sido aplicado na agricultura, e a segunda é um experimento de campo para avaliar seu efeito como promotor de crescimento em soja. A análise bibliométrica revelou um aumento significativo nas publicações sobre este tema nos últimos anos, com o Brasil liderando os esforços de pesquisa. O experimento de campo produziu resultados promissores: quando 5 g de T. asperelloides foram inoculados diretamente nas sementes, um maior rendimento foi alcançado (4.486,2 kg ha⁻¹), atribuído à melhor formação de nódulos e ao desenvolvimento do sistema radicular. Análises estatísticas indicaram uma relação positiva entre o crescimento radicular, a formação de nódulos e a produtividade das plantas. Esses achados reforçam a importância de T. asperelloides como um valioso aliado no aumento da produtividade da soja de forma mais sustentável e ecologicamente correta. Assim, T. asperelloides surge como uma alternativa viável, contribuindo para uma agricultura mais eficiente, alinhada aos atuais desafios ambientais e às necessidades globais de segurança alimentar.

Palavras-chave:
crescimento vegetal; bioinsumos; sustentabilidade; agricultura

1. Introduction

The search for sustainable agricultural systems capable of meeting large-scale production demands while ensuring food security has become a top priority. Soybean (Glycine max (L.) Merrill) is a strategic crop for providing protein and vegetable oils for human and animal consumption, and it also plays a vital role in the agricultural economy. However, it faces significant challenges, including climate variability, soil degradation, and water scarcity—factors that compromise its long-term productivity and sustainability (FAO, 2020; Nagel, 2024). The crop’s high nutritional requirements and dependency on chemical fertilizers and pesticides further highlight the urgent need for sustainable alternatives (Marchi et al., 2024).

Brazil holds approximately 25% of the world's arable land over phosphate-fixing soils, and data from 2005 indicate that between 49% and 62% of Brazil’s farmland is on these soil types (Roy et al., 2016). In general, over 70% of the phosphorus (P) added through fertilizers becomes fixed in the soil in forms that are not readily available to plants. Estimates from 2016 suggest that since 1967, about 33.4 Tg of phosphorus have accumulated in Brazilian soils, representing an economic loss of approximately US$22 billion. By 2050, these figures are projected to reach 106.5 Tg of accumulated phosphorus—equivalent to about US$70 billion (Pavinato et al., 2020). In addition, more than 90% of Brazilian farmers use agrochemicals, with an average annual application rate of 5.94 kg ha⁻¹, accounting for roughly 20% of global consumption. This places Brazil fifth in the global ranking of pesticide use. Soybean tops the charts, with an average of 17.7 kg ha⁻¹ year⁻¹ of pesticides applied (Brovini et al., 2021).

Bioinputs have emerged as a promising solution to mitigate these issues. However, the quality of such products is critical for their agronomic performance and acceptance among farmers. This quality is directly linked to the concentration and viability of the microorganisms involved (Harzevili and Chen, 2015). Parameters such as the minimum count of viable cells or spores, nutrient release efficiency, inoculation effectiveness, shelf life, contamination levels, pH, physical form, and carbon and water content must be strictly controlled (Malusá et al., 2012). Despite advances in research, determining the optimal dosage of spore-based solid inoculants remains a challenge.

According to the Global Catalogue of Microorganisms (GCM, 2025), there are currently 250 registered species of Trichoderma, totaling about 4,567 strains. Trichoderma asperelloides, among them, is maintained in culture collections in countries such as New Zealand, the Netherlands, Hungary, China, Japan, and Chinese Taipei. In Brazil, 114 products containing Trichoderma are currently registered: 92 are classified as microbial fungicides, 10 as nematicides, and 2 as insecticides. As plant growth promoters, three are registered for lettuce (Lactuca sativa L.) and seven for soybean (Brasil, 2025).

Although Trichoderma is primarily used for biological disease control, its functions extend beyond this role, including seed germination promotion and increased crop yields. The fungus also produces substances that stimulate plant growth, particularly by enhancing nutrient uptake—most notably phosphorus (Oliveira et al., 2012). Given its diverse applications, bibliometric analysis serves as a valuable tool to quantitatively assess the evolution and scope of scientific research on the Trichoderma genus. Statistical data from bibliometric studies help evaluate the contribution of scientific knowledge across specific fields and can highlight current research trends and opportunities for future exploration (Su and Lee, 2010).

The global heterogeneity of environmental conditions underscores the need for major crops such as soybean to develop adaptive capacity across diverse ecosystems in order to ensure stable and secure food production. Intensive soil use combined with high fertilizer input has led to significant soil degradation, driving the search for sustainable nutrient sources for crops (Conte et al., 2022). While these conventional practices attempt to compensate for suboptimal growing conditions, they ultimately lead to increased production costs, loss of soil microbiota, and contamination of groundwater. As a result, the use of beneficial microorganisms to promote plant growth and boost crop productivity is becoming a global trend in agriculture. Inoculating soils with fungi such as Trichoderma spp. is considered a viable and effective strategy for improving nutrient management and reducing the use of mineral fertilizers, especially in soils with low fertility (Fiorentino et al., 2018).

Species of the Trichoderma genus are found in a wide range of ecosystems, with the ability to colonize different substrates and tolerate pollutants and agrochemicals, which favors their adaptation to both forest environments and agricultural soils (Zin and Badaluddin, 2020). These microorganisms can improve the biological and chemical properties of the soil, promoting plant growth and microbial balance, especially when compared to the exclusive use of mineral fertilizers (Assigbetsé et al., 2012). In addition, they exhibit antagonistic activity against phytopathogens through the production of hydrolytic enzymes and volatile compounds (López-Bucio et al., 2015), as well as the ability to solubilize phosphates, increasing the availability of micronutrients for plants (Pani et al., 2021).

Most studies involving Trichoderma spp. focus on the biological control of plant diseases (Pedro et al., 2012; Silva et al., 2011; Nascimento et al., 2025). In Cucumis sativus L., Trichoderma asperellum has shown up to an 80% reduction in damage caused by Pseudomonas syringae pv. lachrymans (Yedidia et al., 2003). Trichoderma harzianum is widely used for controlling root pathogens, with proven efficacy against Pythium, Rhizoctonia, Fusarium, Cylindrocladium, and Thielaviopsis (Harman, 2000). On the other hand, studies on T. asperelloides in soybean cultivation are limited, with only one report describing its plant growth-promoting effects (Senger et al., 2023).

This research aimed to: (i) conduct a bibliometric analysis on the scientific applications of T. asperelloides, with emphasis on its agricultural use; and (ii) evaluate the potential of this microorganism as a plant growth promoter in soybean cultivation, in order to determine the most appropriate dosage.

2. Materials and Methods

This research was divided into two stages: the first consisted of a bibliometric analysis, and the second involved a field experiment to evaluate the potential and dosage of the inoculant based on Trichoderma asperelloides in soybean cultivation.

2.1. Bibliometric analysis

A structured search was conducted on April 28, 2025, using the platform lens.org. The term "Trichoderma asperelloides" was searched for in the titles and abstracts of scientific articles, considering the entire period available in the database. From a total of 286,216,314 indexed scientific documents, only 38 articles met the initial search criteria. Among these, 18 articles were clearly related to agronomic fields of knowledge, addressing topics such as fungicide compatibility, drought tolerance, plant diseases, grapevines, biofungicides, growth promotion, soybean, biofilm formation, lettuce, citrus, tomato, biocontrol, strawberry, peanut, melon, aluminum stress, maize, quinoa, and postharvest fruit management.

Based on this dataset, the software VOSviewer (Leiden University's Centre for Science and Technology Studies, version 1.6.20) was used to generate a visual map of keyword co-occurrence networks. Each keyword was considered with a minimum occurrence of one. The size of the circles indicates the frequency of individual keywords (larger icons represent more frequently used terms) and how often the variables appear together.

2.2. Field experiment

The study was conducted during the 2020/21 growing season at the experimental teaching area of the Department of Crop Science (29°42’S, 53°42’W), located at the Federal University of Santa Maria (UFSM), Brazil. The soil in the study area is classified as a sandy-textured dystrophic Red Argisol, corresponding to an Ultisol according to the Soil Taxonomy classification system (USDA, 2014; Santos et al., 2018). The climate in the region is classified as humid subtropical (Cfa) according to Köppen's classification, with an average annual rainfall of 1688 mm. The mean temperature in the warmest month is 24.8 °C, and 14.1 °C in the coldest month (Heldwein et al., 2009; Alvares et al., 2013). The water balance for the study period is presented in Figure 1.

Figure 1
Water balance, showing water surplus (blue) and water deficit (red), with green arrow indicating sowing, blue arrow indicating flowering, and red arrow indicating harvest, during the 2020/2021 growing season in Santa Maria (RS).

On November 17, 2020, the experiment was established using the cultivar NS5959 IPRO, with a seeding density of 13 seeds per linear meter, and the harvest took place on March 30, 2021. The experiment was conducted following a randomized complete block design with four replications. The treatments evaluated were: (i) no inoculation; (ii) co-inoculation on the seed; (iii) co-inoculation in the planting furrow; (iv) co-inoculation in the planting furrow + Trichoderma asperelloides (2 g); (v) co-inoculation in the planting furrow + Trichoderma asperelloides (5 g); (vi) co-inoculation in the planting furrow + Trichoderma asperelloides (10 g); (vii) Trichoderma asperelloides seed treatment (2 g); (viii) Trichoderma asperelloides seed treatment (5 g); and (ix) Trichoderma asperelloides seed treatment (10 g).

Experimental plots consisted of five rows with 7.75 m in length, and row spacing of 0.45 m, resulting in a total area of 17.44 m² and a useful area of 3.87 m² per plot. Soybean co-inoculation was performed using Bradyrhizobium japonicum and Azospirillum brasilense, each at a concentration of 2.0 × 10⁹ colony-forming units per mL (CFU mL⁻¹). For inoculation with Trichoderma asperelloides, a spore-based inoculant was used at a concentration of 2.0 × 10¹⁰ CFU mL⁻¹. Inoculation was applied in the planting furrow according to the treatments. The spray volume was 50 L ha⁻¹. General management and phytosanitary practices were carried out aiming at yields above 4000 kg ha⁻¹ (Martin et al., 2022).

To determine base fertilization, a chemical soil analysis was performed on the 0–10 cm layer, showing the following characteristics: pH in water (1:1) = 5.2; organic matter = 2.2% (w/v); clay = 27% (w/v); available phosphorus (P-Mehlich) = 7.5 mg dm⁻³; potassium = 0.102 cmolc dm⁻³; H+Al = 7.7 cmolc dm⁻³; CTC at pH 7.0 = 14.9 cmolc dm⁻³; base saturation = 48.5%; calcium = 5.0 cmolc dm⁻³; magnesium = 2.1 cmolc dm⁻³; aluminum = 0.8 cmolc dm⁻³; aluminum saturation = 10%; SMP index = 5.5. Based on this analysis, the base fertilization applied was 340 kg ha⁻¹ (P₂O₅ 42% and K₂O 60%).

Weed control was carried out by pre-plant desiccation using diquat 200 g L⁻¹ at 2 L ha⁻¹ and diclosulam 840 g kg⁻¹ at 40 g ha⁻¹. Subsequently, two post-emergence chemical weedings were performed using glyphosate 455 g L⁻¹ at 3 L ha⁻¹ for each application. Pest and disease management included three applications: the first with fungicides containing trifloxystrobin 150 g L⁻¹ and prothioconazole 175 g L⁻¹ at 400 mL ha⁻¹, mancozeb at 1 kg ha⁻¹, and insecticides with beta-cyfluthrin 12.5 g L⁻¹ and imidacloprid 100 g L⁻¹ at 500 mL ha⁻¹. The second application followed the same fungicide and insecticide products and dosages. The third and final application consisted of fungicides trifloxystrobin 375 g L⁻¹ and cyproconazole 160 g L⁻¹ at 200 mL ha⁻¹, mancozeb at 1 kg ha⁻¹, and the insecticide acephate 970 g kg⁻¹ at 1 kg ha⁻¹.

The following variables were evaluated: number of nodules per plant (NNP), dry mass of nodules per plant (DNP), dry mass of roots (DMR), number of plants per linear meter (NPLM), grain yield (GY), and thousand-grain weight (TGW). NNP was determined at phenological stage R1 (beginning of flowering), according to Fehr and Caviness (1977), by randomly collecting four plants per experimental unit. After counting nodules, DNP and DMR were determined. Nodules and roots were washed and dried in a forced-air circulation oven at 60 °C until constant weight, then weighed on a scale with 0.001 g precision. NPLM was obtained by counting plants in a one-meter linear row in each plot. GY (kg ha⁻¹) was determined by harvesting plants with a motorized combine, threshing, cleaning, and weighing samples, correcting moisture content to 13% (dry basis). TGW (g) was obtained by weighing 1000 grains per sample.

The data were submitted to analysis of variance (ANOVA), and when significant at 5%, treatment means were compared using the Scott-Knott test at the 5% significance level. Data analysis was performed using the SASM-Agri® statistical software.

3. Results and Discussion

3.1. Bibliometric analysis

A bibliometric survey conducted on the Lens.org platform using the term “Trichoderma asperelloides” in the title and abstract resulted in the identification of 38 scientific documents published up to April 2025. However, when considering the use of T. asperelloides in agricultural applications, the number reduces to 18 articles (Figure 2). The first record appeared in 2008, but a significant increase in publications occurred from 2018 onward, peaking in 2022 with 9 publications. This recent growth trend reflects the rising interest in biological solutions for phytopathogen control and plant growth promotion, aligned with the search for more sustainable agricultural practices.

Figure 2
Evolution of the number of annual publications (“a” and “d”), frequency of knowledge areas (“b” and “e”), and number of publications by country (“c” and “f”), in all publications using Trichoderma asperelloides (38 articles) and those with agricultural applications (18 articles).

The publications are mainly distributed in journals focused on applied microbiology and phytopathology, with highlights including: Biological Control (Impact Factor: 4.5); Frontiers in Microbiology (Impact Factor: 6.1); and Journal of Applied Microbiology (Impact Factor: 4.0). The set of analyzed documents accumulates more than 520 citations, resulting in an H-index of 11 for the topic “Trichoderma asperelloides”. This means that at least 11 articles have received 11 citations each, reflecting the academic relevance of the subject.

Geographical analysis of scientific production on T. asperelloides reveals strong leadership by Brazil, responsible for approximately 62% of the published articles. Following are India and China, each contributing around 10% of the publications related to the topic. Regarding the most productive institutions, the State University of Londrina and the Federal University of Viçosa, both in Brazil, stand out, along with the Indian Agricultural Research Institute (India). This Brazilian predominance reflects the growing importance of biocontrol agents in the management of strategic agricultural crops for the country.

The thematic analysis revealed that the most frequent knowledge areas in the articles were “biological control,” “plant growth promotion,” “enzyme production,” “induced systemic resistance,” and Sclerotinia sclerotiorum. These results indicate that T. asperelloides is being studied from multiple perspectives, both in pathogen protection and plant development promotion, as well as its ability to modulate induced defenses in different crops.

The data confirm that T. asperelloides is an emerging topic with great potential in the context of sustainable agriculture. The recent increase in publications and the high number of citations demonstrate the growing scientific importance of this microorganism. However, there is a clear need to expand studies to diverse edaphoclimatic conditions and deepen the development of viable commercial formulations, ensuring stability, agronomic efficiency, and environmental safety for large-scale use. Furthermore, it is necessary to establish the doses that maximize crop performance, especially regarding growth promotion.

3.2. Co-occurrence of keywords

The co-occurrence analysis of keywords in 18 articles on the agricultural use of T. asperelloides revealed five thematic clusters (Figure 3a), reflecting the diversity of approaches in the literature.

Figure 3
Formation of five clusters related to keyword co-occurrences.

Cluster 1 (red) highlights terms such as “tomato crop,” “biological protection,” and “antagonist,” indicating the use of Trichoderma as a biological control agent in vegetables, especially tomatoes. This reinforces the well-established role of this genus in phytosanitary protection. Recent studies support this idea, such as the evaluation of a strain of T. asperelloides which showed promising performance in laboratory tests against the fungi Fusarium oxysporum and Alternaria alternata. In these in vitro tests, T. asperelloides exhibited significant mycoparasitic activity by constricting and penetrating the hyphae of the phytopathogenic fungi. Moreover, the isolated application of the agent resulted in a reduction of disease severity in tomato plants by more than 53.8% for A. alternata and 66.7% for F. oxysporum. These results reinforce the potential of T. asperelloides as an effective tool in the biological management of diseases in this crop (Ramírez-Cariño et al., 2020).

Cluster 2 (yellow), centered on “BCAs” (Biological Control Agents), presents a more technical and conceptual approach, focusing on T. asperelloides as part of a broader set of biological control agents, including regulatory and characterization aspects. One study evaluated the potential of T. asperelloides PSU-P1 as a natural alternative to control gummy stem blight in melons (Cucumis melo), caused by the fungus Stagonosporopsis cucurbitacearum. The application of the microorganism stimulated the activation of plant defense-related genes, such as chitinase and β-1,3-glucanase, resulting in a significant increase in the activity of these enzymes and a decrease in disease severity under field conditions. Additionally, the treatment contributed to better plant development and improved fruit characteristics, such as weight and diameter, without compromising post-harvest quality. These results indicate that T. asperelloides PSU-P1 is an efficient and sustainable strategy for managing this disease in melon crops (Intana et al., 2022).

Cluster 3 (purple) relates to “biocontrol agents” and addresses practical applications by comparing the efficacy of different microorganisms in specific agricultural contexts. Ranade et al. (2022) investigated the potential of two microorganisms: T. asperelloides (strain 5R) and Bacillus licheniformis (strain TL-171) as biological control agents against the fungus Cladosporium cladosporioides, which causes damage to Thompson Seedless grapes (Vitis vinifera L.) after harvest. According to the authors, applying these microorganisms before harvest significantly reduced the presence of the fungus, both in laboratory tests and field experiments. Therefore, this strategy helped increase the shelf life of grapes during refrigerated storage.

Cluster 4 (blue) includes terms like “antifungal activity,” “culture filtrates,” and “Trichoderma,” indicating studies on secondary metabolites with antifungal action, mostly in vitro. One study evaluated the use of T. asperelloides SKRU-01 as a biocontrol agent against Peniophora salaccae SKRU002, a fungus that causes rot in Salacca zalacca (Gartn.) Voss fruits. Both laboratory tests and fruit assays showed that this microorganism significantly reduced fungal growth, achieving results comparable to the fungicide Mancozeb®. Moreover, Trichoderma helped preserve fruit quality. The presence of antifungal metabolites in this microorganism supports its potential as an effective and more sustainable alternative for controlling this disease (Boukaew et al., 2025).

Cluster 5 (green), represented by “abiotic stresses,” points to an emerging line of research investigating Trichoderma as an inducer of tolerance to abiotic stresses such as drought and salinity, expanding its use beyond disease control. A recent study evaluated how inoculation with T. asperelloides NT33 affects ‘Jaune Flamme’ tomatoes under water stress conditions. Transcriptomic analysis revealed that water deficit caused significant changes in gene expression in the plants. In contrast, inoculation with the fungus caused more subtle changes, involving only 28 genes with differential expression. Among these were genes related to secondary metabolite production and stress responses, suggesting that NT33 helps plants cope with drought through specific mechanisms without causing major alterations in their genetic profile (Rawal et al., 2023).

Together, these clusters illustrate the multifunctional role of Trichoderma in agriculture, acting both in phytosanitary management and in promoting plant growth and resilience. The overlap between classical and emerging themes signals a growing research field with strong appeal to sustainability.

3.3. Specificity of keyword co-occurrence in each cluster

Figure 3b depicts a keyword co-occurrence cluster associated with the antifungal activity of microorganisms, with an emphasis on Trichoderma. The central keyword, "antifungal activity," connects two main thematic axes. The first involves the interaction of Trichoderma with soil fungi and plant pathogens. Terms such as "soil fungi," "plant pathogen," "VOCs," and "trichoderma" indicate a focus on biocontrol mechanisms, especially the production of volatile organic compounds (VOCs), which act at a distance and stand out as sustainable alternatives to chemical fungicides. Ruangwong et al. (2021) analyzed a strain of T. asperelloides called TSU1, isolated from soil cultivated with the plant Anthurium andraeanum in Thailand. This strain demonstrated significant antifungal activity due to the release of VOCs, which were able to inhibit the growth of five fungi that threaten plants: Corynespora cassiicola, Fusarium incarnatum, Neopestalotiopsis clavispora, Neopestalotiopsis cubana, and Sclerotium rolfsii. The inhibition rate ranged from approximately 39% to 68%. Additionally, the study identified 17 different compounds present in these VOCs using a technique called GC-MS. Among them, fluoro(tinitro)methane accounted for about 18% of the peak area in the analysis, and 2-phenylethanol comprised approximately 10%. When tested individually with a similar commercial compound, 2-phenylethanol showed antifungal effects comparable to the natural VOCs, inhibiting up to 78% of fungal growth (Ruangwong et al., 2021).

The second axis addresses the biochemical characterization of produced metabolites, highlighting terms such as "culture filtrates," "heat stability," and "afb(1) degradation." These studies evaluate the antifungal efficacy of secreted compounds, their thermal stability, and their ability to degrade toxins like aflatoxin B1, expanding the use of Trichoderma beyond agriculture to include food safety and bioremediation. The term "Trichoderma asperelloides skru-01" points to the selection of strains with high antifungal potential, aimed at applications as inoculants or sources of bioinputs. The multifunctional effect of Trichoderma was also evaluated by Senger et al. (2023), who studied the agronomic performance of the FT10 inoculant (T. asperelloides) in four lettuce varieties. Results showed significant increases in plant height, leaf number, dry biomass, and productivity, especially with doses of 0.10 and 0.15 kg ha⁻¹, resulting in yield gains of up to 22%. In summary, this cluster highlights the breadth of studies on the antifungal activity of Trichoderma, with agronomic, industrial, and environmental applications. The production of VOCs, metabolite stability, and mycotoxin degradation reinforce the microorganism’s role as a multifunctional bioinput aligned with sustainable agriculture and the bioeconomy.

The cluster in Figure 3c focuses on the biological protection of tomato crops and gathers terms related to biocontrol of phytopathogens. At the center is "tomato crop biological protection," surrounded by terms such as "antifungal," "phytopathogen microbial control," "phytopathogen mycoparasitism," "induced systemic resistance," and "antagonist," representing different disease control strategies. "Antifungal" refers to the production of compounds that inhibit pathogenic fungi. "Phytopathogen microbial control" involves using beneficial microorganisms to suppress pathogens. "Mycoparasitism" describes fungi attacking other fungi. "Induced systemic resistance" points to the activation of plant defenses by microorganisms. "Antagonist" serves as an umbrella term for all these control agents. This cluster evidences an integrated and sustainable phytosanitary management approach in tomato cultivation, reinforcing the role of bioinputs as alternatives to chemical pesticides. Intana et al. (2023) emphasize the versatility of Trichoderma as a biocontrol agent by developing an emulsion-based formulation of T. asperelloides PSU-P1 to control stem canker in pitaya caused by Neoscytalidium dimidiatum. The formulation, composed of coconut oil, Tween 20, and distilled water (30:10:60), significantly reduced disease severity in vivo, with a lesion area of 0.53 cm² compared to 1.65 cm² in the infected control. Beyond its antifungal efficacy, the study highlighted the importance of the stability and viability of Trichoderma propagative structures in formulations. The mixture stored at 10 °C maintained viability above 70% after six months and showed mycelial inhibition capacity over 75%, demonstrating that bioinput durability can be improved through appropriate formulation technologies. These data contrast with the term "antagonist" in the cluster, which synthesizes the multiple roles these microorganisms play in plant protection. Therefore, including Trichoderma in tomato cultivation, as mentioned in the cluster, has practical evidence such as that provided by Intana et al. (2023). These studies show the fungus is effective even outside the Solanaceae system.

The cluster in Figure 3d addresses postharvest disease management and food safety, complementing the previous one on biological protection in tomato crops. The focus here is postharvest, with sustainable strategies to ensure quality, safety, and shelf life of food products. The central term is "biocontrol agents," biological agents used to inhibit the growth of spoilage fungi in stored or marketed products, directly linked to "fungal inhibition," which aims to prevent pathogenic fungal development. The connection with "postharvest disease management" reflects concern for reducing losses during storage, transport, and marketing. Biocontrol use is also linked to the concept of "food safety" since it eliminates the need for chemical fungicides and their residues in food. The term "shelf-life extension" highlights the primary benefit of postharvest biocontrol: prolonging food shelf life while maintaining sensory and nutritional qualities. This cluster complements the previous one by showing that biocontrol benefits not only cultivation but also the safe storage of foods, directly impacting public health, agricultural economics, and sustainability. Together, the clusters demonstrate the integrated action of beneficial microorganisms—from field protection to postharvest conservation. The results of Ranade et al. (2022) support this cluster approach by demonstrating that preharvest application of T. asperelloides 5R on 'Thompson Seedless' grapes significantly reduced colonization by Cladosporium cladosporioides from 650 to only 30 colony-forming units. This helped increase fruit shelf life from 11 to 15 days. The inhibition of the pathogen at rates above 60% was attributed to volatile and non-volatile metabolites produced by T. asperelloides. These data reinforce the efficiency of biocontrol as a sustainable tool for postharvest preservation, bridging closely with the cluster terms "food safety" and "shelf-life extension."

The cluster in Figure 3e, represented by terms such as "gene expression," "disease resistance," "chitinase," "β-1,3-glucanase," and "BCAs" (biocontrol agents), reveals the molecular and physiological core of the biological control mechanism, providing the scientific basis supporting the effects observed in the other clusters. It connects to the broader picture by highlighting the intracellular and biochemical processes triggered in plants when exposed to biocontrol agents. The presence of chitinase and β-1,3-glucanase indicates activation of plant defense enzymes. These enzymes degrade cell wall components of pathogenic fungi, such as chitin and glucans, representing one of the plant's first lines of defense against infection. Activation of these enzymes often follows recognition of pathogen-associated molecular patterns or BCA action. The term gene expression indicates that BCA use can modulate gene expression in plants, inducing defense-related genes, including those encoding these hydrolytic enzymes. This gene expression is directly associated with increased disease resistance, another central cluster concept, representing strengthened plant immunity against pathogens. The acronym BCAs links this cluster with previous ones, showing that biocontrol agents not only act directly on pathogens but also stimulate systemic defense pathways in plants. This effect, known as induced systemic resistance (ISR), is an ecological and effective strategy that reduces pesticide dependency. Thus, this biological cluster complements the others by elucidating molecular mechanisms explaining observed effects in both field disease control and postharvest preservation. It provides the scientific link connecting practical bioinput use with physiological and genetic responses in plants, consolidating the integrated and sustainable biological control approach in agricultural systems. These cluster components reflect activation of plant defense physiological responses, especially through biocontrol agents. Intana et al. (2022) confirm this dynamic by showing that in the field, T. asperelloides PSU-P1 caused a 7- to 10-fold increase in expression of the chi (chitinase) and glu (β-1,3-glucanase) genes in melons. Additionally, there was a significant increase in enzyme activity, crucial for fungal cell wall degradation. This enzymatic response was also accompanied by a marked reduction in stem gummy disease severity, reinforcing the role of biocontrol agents in activating ISR and connecting physiological effects observed in plants to genetic adjustment promoted by bioinputs.

The cluster in Figure 3f, with terms such as "fungus," "abiotic stresses," "proline," "chlorophylls," and "absolute growth rate," relates to the physiological and biochemical effects on plants under biotic and abiotic stresses, often involving microorganisms, including biocontrol agents. The presence of "fungus" highlights biotic stress caused by pathogenic or symbiotic fungi. This interaction activates physiological responses such as proline production, which helps the plant cope with abiotic stresses like drought and salinity. Proline stabilizes proteins, maintains osmotic potential, and neutralizes free radicals. The term "chlorophylls" indicates that these stresses and interactions affect photosynthesis, with degradation or maintenance of chlorophyll levels serving as an indicator of plant health. Plants that maintain higher chlorophyll levels even under stress generally exhibit better adaptation or are influenced by beneficial microorganisms. "Absolute growth rate" reflects the impact of these biochemical and physiological processes on plant growth. Growth may be reduced by stresses or, in the case of beneficial interactions, even increased, demonstrating the effectiveness of the adaptive response or the action of bioinputs.

This cluster shows how biotic and abiotic stresses affect plant physiology and how biocontrol agents can modulate these responses, impacting plant productivity and resilience. In the study by Rawal et al. (2022), inoculation of T. asperelloides NT33 in tomato plants under water stress led to significant improvements in several physiological aspects. The plants exhibited higher chlorophyll content, increased relative water content, better photosynthesis, and greater photosystem II efficiency. Additionally, there was an increase in the accumulation of proline and phenolic compounds, which aid in stress adaptation. At the molecular level, although only 28 genes were identified as differentially expressed in inoculated plants, they were mainly related to secondary metabolite production, stomatal regulation, and xylem development — all important processes for adapting to water deficit. These results explain why the plants were able to maintain their growth, photosynthetic pigments, and overall health even under water stress, reinforcing the role of T. asperelloides in plant resistance to these challenges. This relationship is reflected in the terms "proline," "chlorophylls," and "absolute growth rate" present in the study’s findings.

Research focused on disease control and abiotic stress is predominant, while studies investigating growth promotion and/or productivity in soybean cultivation are rarer. Laboratory or controlled environment studies are important; however, many authors (Baudson et al., 2023; Cassman and Dobermann, 2022) emphasize that field experiments are essential as they expose microorganisms to real adaptation and survival conditions.

In this context, studies on the genus Trichoderma spp. promoting soybean growth in the field have shown promising results. For example, Sá et al. (2024), when evaluating the growth-promoting potential of Trichoderma in soybean cultivation, found satisfactory results by applying it through seed inoculation and foliar spray, which significantly increased crop productivity. Similarly, Moreira et al. (2024) observed that using a biostimulant combined with Trichoderma spp. for seed treatment resulted in vegetative growth increases in both the aerial parts and root systems of soybean plants. Supporting these observations, Gonçalves et al. (2018) reported significant gains in soybean productivity by applying T. asperellum, with increases ranging from 33% to 34.5% compared to control plants that were not inoculated. These results highlight the potential of the genus Trichoderma spp. as a growth and productivity promoter, underscoring the importance of ongoing research to validate its effectiveness under different edaphoclimatic conditions and agricultural management systems.

3.4. Field experiment

From the bibliometric analysis, only one article was found related to the use of T. asperelloides as a growth promoter in soybean cultivation (Senger et al., 2023). This motivated the submission of the present experimental data for publication, as it is understood that the multifunctionality of T. asperelloides goes beyond plant protection, as previously highlighted. Thus, the analysis of variance (Table 1) showed a significant effect (p < 0.01) of the treatments on all evaluated agronomic variables, with particular emphasis on the impact of the combined use of growth-promoting microorganisms and T. asperelloides on crop performance.

Table 1
Summary of the analysis of variance, represented by the mean squares of the variables: number of nodules per plant (NNP), dry mass of nodules per plant (DNP, g), dry root mass (DRM, g), number of plants per linear meter (NPLM), thousand-grain weight (TGW, g), and grain yield (GY, kg ha⁻¹).

SV	DF	NNP	DNP	DRM	NPLM	TGW	GY
Tratament (T)	8	2560.39*	0.0131*	3.8498*	6.9028*	89.1803*	584431*
Bloc (B)	3	416.62*	0.0032*	1.0492*	0.6667*	54.4944*	40828*
CV (%)		19.31	22.21	12.96	17.94	3.17	5.13
Mean		117.69	0.37	4.56	13.22	168.57	3839.53

• ^*
  Significant at the 1% probability level by the F test; source of variation (SV); degrees of freedom (DF); coefficient of variation (CV).

The separation of means by the Scott-Knott test (p < 0.05) (Table 2) indicated that seed co-inoculation resulted in the highest number of nodules per plant, with an average of 155, statistically higher than the other treatments. In second place, the application of T. asperelloides to the seed at a dose of 5 g stood out, with an average of 150 nodules, followed by in-furrow co-inoculation with 10 g of Trichoderma, which provided 134 nodules. Regarding the nodule dry mass (DNP), the highest value (0.46 g) was observed in the in-furrow co-inoculation with 10 g of Trichoderma, the same treatment that also resulted in the highest root dry mass (DRM), reaching 5.67 g, indicating greater root development. The number of plants per linear meter (NPLM) was higher in the co-inoculation in the furrow without Trichoderma (15.5 plants), followed by the co-inoculation with 10 g of Trichoderma (15.0 plants), suggesting a positive effect of these treatments on the final stand. The highest thousand grain mass (TGW) was obtained in the co-inoculation in the furrow with 5 g of Trichoderma (175.34 g), while the best productive performance (GY) was achieved by the treatment with T. asperelloides in the seed at a dose of 5 g, with a productivity of 4486.2 kg ha⁻¹, significantly higher than the others. Considering the concentration of 2 x 10¹⁰ CFU g⁻¹ and the number of seeds per hectare (288,888.9), the estimated concentration was 346,153.83 CFU seed⁻¹, a value close to that reported by Senger et al. (2023) for T. asperelloides, but lower than the typical concentration of Bradyrhizobium (1.2 x 10⁶ CFU seed⁻¹) (Hungria et al., 2017). These results show that the combination of growth-promoting microorganisms with Trichoderma, especially via seed treatment at a dose of 5 g, has the potential to improve nodulation, root development and, mainly, soybean productivity under field conditions.

Table 2
Number of nodules per plant (NNP), dry mass of nodules per plant (DNP, g), dry root mass (DRM, g), number of plants per linear meter (NPLM), thousand grain weight (TGW, g), and grain yield (GY, kg ha⁻¹).

		NNP	DNP	DRM	NPLM	TGW	GY
Without inoculation	77 i		0.26 i	2.95 i	12.75 e	159.71 i	3245.4 i
Co-inoculação on seed	155 a		0.42 b	5.59 b	12.00 f	178.90 e	3454.8 h
Co-inoculation in the furrow	121 d		0.41 c	3.74 g	15.50 a	167.41 f	4065.6 d
Co-inoculation in furrow + Trichoderma (2g)	103 g		0.38 d	5.17 c	13.50 c	168.96 d	3617.4 g
Co-inoculation in furrow + Trichoderma (5g)	104 f		0.37 e	4.16 d	13.25 d	175.34 a	3822.6 e
Co-inoculation in furrow + Trichoderma (10g)	134 c		0.46 a	5.67 a	15.00 b	172.53 c	4101.0 b
TS Trichoderma (seed treatment with Trichoderma) (2g)	100 h		0.34 g	3.29 h	13.25 d	172.98 b	3685.8 f
TS Trichoderma (seed treatment with Trichoderma) (5g)	150 b		0.35 f	4.13 e	11.75 g	166.03 g	4486.2 a
TS Trichoderma (seed treatment with Trichoderma) (10g)	116 e		0.34 h	3.85 f	12.00 f	165.28 h	4077.0 c

• Means followed by the same letter in the column do not differ statistically from each other according to the Scott-Knott test at the 5% probability level. TS (seed treatment); Doses of Trichoderma asperelloides: grams per each 40 kg of seeds.

In soybean cultivation, inoculation with the microorganism Bradyrhizobium is essential to achieve better biological nitrogen fixation (BNF), which replaces nitrogen fertilizers (N) and reduces production costs (Hungria and Mendes, 2015). Despite the remarkable success of this microorganism for this crop, studies are being developed regarding co-inoculation, involving the addition of another beneficial microorganism (Leite et al., 2024). Studies inoculating T. asperellum and Bradyrhizobium in soybean plants have shown increases in biomass, height, and phosphorus uptake efficiency in greenhouse experiments (Bononi et al., 2020). These results demonstrate the potential for using different microorganisms in soybean co-inoculation, aiming for higher productivity and lower production costs (Leite et al., 2024).

3.5. Correlations

It was observed that root dry mass showed a significant correlation with the number of nodules per plant (r = 0.53; p < 0.001) and with the dry mass of nodules (r = 0.60; p < 0.001), indicating that plants with greater root development tend to have higher nodulation and biomass accumulation in nodules (Figure 4). This result suggests that a more robust root system favors nodule formation and growth, likely by providing a larger infection area and better nutritional support for the establishment of symbiosis.

Figure 4
Pearson correlations for the variables number of nodules per plant (NNP), dry mass of nodules per plant (DNP, g), root dry mass (DRM, g), number of plants per linear meter (NPLM), thousand-grain weight (TGW, g), and grain yield (GY, kg ha⁻¹).

Additionally, the number of nodules per plant was positively correlated with nodule dry mass (r = 0.66; p < 0.001) and grain yield (r = 0.39; p < 0.05). This indicates that higher nodulation is associated with increased nodule biomass and, consequently, may contribute to greater biological nitrogen fixation, positively reflecting on crop productivity. The positive correlation between the number of nodules and grain yield reinforces the importance of efficient symbiosis between the plant and nitrogen-fixing microorganisms for the agronomic performance of legumes.

Fipke et al. (2016) highlighted that co-inoculation with Bradyrhizobium spp. and Azospirillum brasilense significantly increased both nodulation and plant productivity. Furthermore, he found that the use of mineral nitrogen can negatively affect biological nitrogen fixation (BNF), reinforcing the importance of seeking more sustainable alternatives such as bioinputs. Although this study used the fungus T. asperelloides, the positive effects on root growth and nodulation are similar to those promoted by rhizobacteria. This shows that different microorganisms can act synergistically to improve BNF and crop performance.

The positive correlations found between root dry mass, nodule number, and nodule mass reinforce the fundamental role of a well-developed root system in ensuring better efficiency in association with rhizobia and, consequently, good agronomic performance of soybean. This relationship was also observed by Senger et al. (2022), using a T. asperelloides-based inoculant on lettuce cultivars. They reported significant increases in shoot dry mass, productivity, and, in some cases, root weight, especially at doses of 0.10 and 0.15 kg ha⁻¹. Although these are different crops, the authors emphasize that agronomic performance is directly linked to plant biomass accumulation and leaf number, both factors that reflect greater nutrient uptake efficiency. This efficiency may also be related to a larger root area and better rhizosphere colonization, which was also observed in our study.

The positive correlations among root dry mass, nodule number, and nodule mass observed in this study further highlight the importance of a well-developed root system for better symbiotic efficiency. Although the greatest yield gains in lettuce occurred when applications were made in the furrow before transplanting, the positive effects of T. asperelloides on root development and shoot growth are consistent with the results of this work (Senger et al., 2022). In the present study, seed treatment resulted in higher grain yield (4486.2 kg ha⁻¹) and increased nodulation. Finally, the relationship between morphophysiological parameters and productivity observed here is also confirmed by the data from Senger et al. (2023). This reinforces that the use of T. asperelloides as a bioinput can improve symbiotic efficiency, promote healthier plant growth, and increase final crop yield, even under different environmental conditions.

4. Conclusion

The bibliometric analysis revealed an increase in publications about Trichoderma asperelloides, focusing on its agricultural use for controlling phytopathogens, promoting plant growth, and enhancing resistance to abiotic stresses, especially in economically important crops.

The results demonstrated that T. asperelloides acts as a growth promoter in soybean, favoring plant development and increasing productivity, confirming its viability as a bioinput in agricultural systems at a dose of 5 g ha⁻¹.

This research reinforces the role of T. asperelloides as a sustainable alternative to chemical inputs, highlighting the importance of bioinputs in building a more efficient, environmentally responsible agriculture aligned with food security.

Acknowledgements

To the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - Processes 312543/2023-9), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil - Finance code 001, and the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS – Processes 22/2551-0001644-8) for granting scholarships to the authors. To the scholarship students and volunteers for helping in data collection.

• Data Availability Statement
  The dataset analysed or produced in this study can be requested from the corresponding author.

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Edited by

• Editor: Takako Matsumura Tundisi

Data availability

The dataset analysed or produced in this study can be requested from the corresponding author.

Publication Dates

• Publication in this collection
  20 Mar 2026
• Date of issue
  2026

History

• Received
  13 Oct 2025
• Accepted
  29 Dec 2025