ABSTRACT:
Soybeans are one of the world’s main commodities, and Brazil is one of the largest producers. Conversely, their cultivation depends on climate, management, and the environment. To improve productivity, soybean grains are inoculated with inoculants based on nitrogen-fixing microorganisms that promote soybean growth. This study evaluated the effect of Trichoderma endophyticum as a promoter of growth and grain yield in soybean crop. Experiments were installed in Ponta Grossa - PR, Paranapanema - SP, Bandeirantes - PR, and Paranavaí - PR, in the 2020/2021 harvest. The tests were conducted using a randomized block experimental design and the treatments were applied via seed. The treatments applied were: 1: Control; 2: Co-Mo Platinum (150 mL.50 kg seeds-1); 3: ICB Nutrisolo Trichoderma (100 mL.ha-1); 4: Endophytus Inoculant (dose 50 g.50 kg seeds-1); 5: Endophytus Inoculant (100 g.50 kg seeds-1); 6: Endophytus Inoculant (150 g. 50 kg seeds-1); and 7: Endophytus Inoculant 200 g.50 kg seeds-1). Results showed that the inoculant Endophytus applied via seed positively impacted the growth of soybean plants and did not cause any symptoms of phytotoxicity. The dose of 200 g. 50 kg seeds-1 presented a more constant result in most of the analyzed variables when compared to controls, in the four places, with gains in the analyzed parameters according to the application of the Endophytus inoculant, providing increases of up to 13.63 % in grain yield compared to the control without inoculation. Given the results presented, it is recommended to use the inoculant Endophytus as a plant growth promoter and increase productivity.
Key words:
Glycine max L. (Merrill); agronomic efficiency; phytotoxicity; inoculant; grain yield.
RESUMO:
A soja é uma das principais commodities do planeta, e o Brasil é um dos maiores produtores. Por outro lado, seu cultivo depende de fatores como clima, manejo e ambiente. Com o intuito de melhorar a produtividade, tem se utilizado a inoculação dos grãos de soja com o inoculantes a base de microrganismos fixadores de nitrogênio que promovem o crescimento da soja. Este trabalho teve como objetivo avaliar o efeito do Trichoderma endophyticum como promotor de crescimento e do rendimento de grãos na cultura da soja. Os experimentos foram instalados nas cidades de Ponta Grossa - PR, Paranapanema - SP, Bandeirantes - PR e Paranavaí - PR, na safra 2020/2021. Os testes foram conduzidos em delineamento experimental de blocos casualizados e os tratamentos foram aplicados via sementes. Os tratamentos aplicados foram: 1: Testemunha; 2: Co-Mo Platinum (150 mL. 50 kg sementes-1); 3: ICB Nutrisolo Trichoderma (100 mL.ha-1); 4: Inoculante Endophytus (dose 50 g. 50 kg sementes-1); 5: Inoculante Endophytus (100 g.50kg sementes-1); 6: Inoculante Endophytus (150 g. 50 kg sementes-1); e 7: Inoculante Endophytus 200 g. 50 kg sementes-1). Os resultados obtidos nas quatro localidades edafoclimáticas mostraram que o inoculante Endophytus aplicado via semente impactou positivamente o crescimento das plantas de soja e não causou sintomas de fitotoxicidade. A dose de 200 g. 50 kg sementes-1 apresentou resultado mais constante na maioria das variáveis analisadas quando comparado aos controles, nos quatro locais, com ganhos nos parâmetros analisados de acordo com a aplicação do inoculante Endophytus, proporcionando incrementos de até 13,63 % no rendimento de grãos em comparação ao controle sem inoculação. Diante dos resultados apresentados, recomenda-se a utilização do inoculante Endophytus como promotor de crescimento vegetal em soja e aumento de produtividade.
Palavras-chave:
Glycinemax L. (Merrill); eficiência agronômica; fitotoxicidade; inoculante; rendimento de grãos.
INTRODUCTION
Soybean is the main oilseed produced and consumed in the world and represents the main product of Brazilian agribusiness and each harvest has increased the use of technologies to improve soybean crop productivity (NOGUEIRA et al., 2018; SEIXAS et al., 2020; SÁ et al., 2024). One of the technologies that have been used is the inoculation of nitrogen-fixing bacteria which promotes biological nitrogen fixation; and consequently, promotes plant growth (NOGUEIRA et al., 2018; ITURRALDE et al., 2020).
Using inoculants considerably reduces the need for nitrogen fertilization in the crop (HUNGRIA & MENDES, 2015). With the results obtained with the inoculation of Bradyrhizobium in soybean crops, the search for microorganisms capable of promoting benefits to plants remains high, as microorganisms interact in different ways with the plant, functioning as a microbiome and providing benefits to host plants (GOMES et al., 2016; NOGUEIRA et al., 2018; ITURRALDE et al., 2020).
Among the new technologies for soybean cultivation, species of fungi of the genus Trichoderma spp. (Hypocreales: Ascomycota) has been widely studied and used as biological agents, and active ingredients in commercial products such as biopesticides, biofertilizers, growth promoters, and resistance inducers in plants (WOO et al., 2014).
Trichoderma species are highly competitive and are present in the soil and environments with large amounts of organic matter, being an excellent decomposer of plant material. Furthermore, it can colonize the rhizosphere of plants, being a key point in this process, to compete for space and nutrients (MONTE et al., 2019). Among the action mechanisms of Trichoderma, the production of extracellular enzymes stands out, which act in the biological control of plant diseases (ELAD et al., 1982), as well as antagonistic activity such as competition, parasitism and antibiosis (CORDIER & ALABOUVETTE, 2009; CHAGAS et al., 2017a).
Studies have demonstrated that fungi in the genus Trichoderma act positively on seed germination and crop development and yield, due to the production of growth-promoting substances and the availability of nutrients for plants, mainly through phosphate solubilization (OLIVEIRA et al., 2012; SILVA et al., 2012; SÁ et al., 2024) and synthesis of indoleacetic acid (CHAGAS et al., 2017b). According to CONTRERAS-CARNEJO et al. (2024), the mechanisms involved in plant growth promoted by Trichoderma species has involved metabolites produced by the fungal and diffused in soil with hormone-like activity.
Trichoderma endophyticum Rocha, Samuels and P. Chaverri, was described as an endophytic fungus present in leaves and stems of trees in the neotropical region, mainly of the genera Theobroma and Hevea (CHAVERRI et al., 2015). To date, there have been few records of the use of T. endophyticum in agriculture. SILVA et al. (2011) demonstrated the beneficial effect of the T. endophyticum (IB42/03) strain in promoting cucumber growth, as well as resistance induction against anthracnose. Thus, this study evaluated the effect of Trichoderma endophyticum as a promoter of growth and grain yield in soybean crop.
MATERIALS AND METHODS
Experimental areas and edaphoclimatic conditions
The experiments were carried out in the field to validate the agronomic efficiency and viability of the Trichoderma endofyticum-based inoculant (trade name of Endophytus) in promoting the growth and development of soybean (Glycine max) in four locations with distinct edaphoclimatic conditions (Table 1). The product is registered under No. PR001371-4.000104. For the experiment development the protocols proposed by MAPA (Ministry of Agriculture, Livestock and Food Supply) for product registration of plant growth-promoting microorganisms were applied, according to the IN 53 (BRASIL, 2013).
The study was conducted in four experimental areas: Ponta Grossa - PR, Paranapanema - SP, Bandeirantes - PR, and Paranavaí - PR. All experimental tests were installed in areas of the partner company 3M Agricultural Experimentation. Information about sowing and harvesting dates is described in table 2.
Information on sowing and harvesting dates (all treatments) of soybean cultivar 58I60 RSF IPRO - BMX LANÇA IPRO. 2020/21 harvest.
Seeding and maintenance applications
Before sowing, the seeds were treated with Standak Top (Pyraclostrobin + Methyl Thiophanate + Fipronil), using a dose of 200 mL.100 kg-1 of seeds, to reflect the current practice used in the field by producers. No inoculants formulated with Bradyrhizobium japonicum were applied.
Soybean was sown with a spacing of 0.50 m between rows and a population density of 300,000 plants per hectare. A basis fertilizer was applied with 380 kg.ha-1 of formula 02-20-20. The soybean cultivar 58I60 RSF IPRO - BMX LANÇA IPRO was used, with medium size, indeterminate growth and maturation group. Requires high soil fertility. The cultivar has very high productive potential, adapts to various climatic regions, and has high branching potential. Regarding diseases, it is resistant to stem canker and Phytophthora, while being susceptible to frogeye spot and bacterial pustule.
Phytosanitary maintenance and cultural treatments for soybeans were carried out under the recommendations for the crop, for each region and following the premise of good agricultural practices. All treatments (Table 3) were applied via seed, using a spray volume of 250 mL for every 50 kg of seeds.
Description of treatments applied to evaluate the effect of the Endophytus inoculant in promoting growth in soybean crop. 2020/21 harvest.
The Co-Mo Platinum product was used as a positive control, using the dose recommended by the manufacturer for soybean crops. This liquid fertilizer for seed application contains cobalt and molybdenum (Table 4), elements that contribute to biological nitrogen fixation and increased protein content in grains. The ICB Nutrisolo Trichoderma product was used as a standard inoculant, using the dose recommended by the manufacturer. This inoculant is indicated as a growth promoter in soybean crops when applied via seed and contains three species of Trichoderma (Table 4).
Climatic data were collected throughout the study in each location, from the first date of the month planted to the last date of the month harvested. Data were obtained from on-site weather stations and/or the nearest weather station.
Experimental design and data analysis
All tests were conducted using a randomized block experimental design with seven treatments and four replications. Each plot had a total area of 24.0 m2 (3.0 m x 8.0 m), with a useful area of 5.0 m2 (2.8 m x 1.8 m).
The data obtained were subjected to analysis of variance with 5 % and 10 % of significance, and compared using the Duncan test, also at the level of 5 % and 10 % of significance. The statistical program used was SASM-Agri® (System for analysis and separation of means in agricultural experiments) (CANTERI et al., 2001).
The means comparison test applied was based on the recommendation of the “Protocol for analyzing the quality and agronomic efficiency of inoculants, strains and other technologies related to the process of biological nitrogen fixation in non-leguminous plants” (HUNGRIA et al., 2007).
The evaluations were carried out at different phenological stages of the crop, coded according to the BBCH scale (2001).
Plant stand: The number of plants that emerged in one meter, in three central lines, was quantified. Assessments were carried out 7 days after emergence (7 DAE BBCH - 11); 10 days after emergence (10 DAE BBCH - 12) and at the time of harvest (BBCH - 96).
Plant vigor: For the vigor analysis, all plants present per plot at 10 DAE were considered. The evaluation was carried out visually, assigning a grade from 1 to 7, where grade 1 was given: vigor much lower than the control grade 2: vigor lower than the control, grade 3: vigor slightly lower than the control, grade 4: vigor close to the control, grade 5: vigor equal to control grade 6: vigor greater than the control and grade 7: vigor much higher than the control.
Nodulation and biomass of the shoot and root: Five complete plants were collected in the central area of the second row of each plot, at the beginning of the flowering stage or the immediately preceding stage, but always between 35 - 40 days after emergence. The roots were collected using a straight shovel, taking care not to damage them and detach the nodules. Then, the roots were washed and the number of nodules in the first two cm depth of the main root was counted. Subsequently, they were placed to dry in an oven at 65 °C. After drying, the dry mass of the nodules was evaluated. The fresh mass of the aerial part and roots was evaluated and then placed to dry in an oven at 65 °C until the weight stabilized, then we evaluated the dry weight of the aerial part and roots
Productivity: It was evaluated in central plants totaling 5 m2 per plot. The grains were cleaned and weighed, correcting the humidity to 13% and transforming the values into kg ha-1. At the time of harvest, the mass of one thousand grains (MMG) was also evaluated.
Phytotoxicity: A possible phytotoxic effect caused to plants by the treatments was evaluated by assigning scores to anomalies when observed. The phytotoxicity scale proposed by the EWRC (1964) was used as a basis. Assessments were carried out at 7 and 15 days after emergence (7 DAE; 15 DAE).
RESULTS AND DISCUSSION
Effect of endophytus inoculant on the stand of soybean plants
In the four locations where Endophytus inoculant was applied via seed, at doses of 150 and 200 g. 50 kg seeds-1, it had a positive impact on germination, at 7 and 10 days after emergence, as well as in the final stand of soybean plants. In the experiment carried out in Ponta Grossa, in the three evaluations, significant statistical differences were observed in comparison with the control (without inoculant).
The Endophytus inoculant at a dose of 200 g. 50 kg seeds-1 showed a greater number of plants at 7 and 10 DAE and at the time of harvest, being statistically different from the control, the positive control (Co-Mo Platinum) and the standard (ICB Nutrisolo Trichoderma) (Table 5), when comparing the means using the Duncan test at a 5% probability. It is important to highlight that the two previous doses also differed statistically from the control.
In the experiment conducted in Paranapanema, it was observed that doses of 100 - 200 g.50 kg seeds-1 differed statistically from the control and positive control in the three evaluations carried out.
The stand observed in the experiment conducted in Bandeirantes showed that doses of 100 - 200 g. 50 kg seeds-1 differed statistically from the control in the three evaluations carried out. Therefore, the highest dose presented the largest number of plants (Table 5). In comparison with the standard (ICB Nutrisolo Trichoderma), it was observed that doses of 150 and 200 g. 50 kg seeds-1 were statistically higher.
In the experiment conducted in Paranavaí, it was found that doses of 150 and 200 g. 50 kg seeds-1 differed statistically from the control and positive control in the four evaluations (Table 5). Although the doses of 50 and 100 g. 50 kg seeds-1 were statistically similar to the control.
According to MELLO et al. (2020), the use of Trichoderma can suppress the growth of phytopathogens, as well as induce systemic resistance (RSI) to diseases and/or promote plant growth, increasing seed germination, branching, and root growth. As observed in the study carried out, significant differences in the application of Endophytus, at dosages of 150 and 200 g. 50 kg seeds-1, showing improvement in promoting germination and stand of soybean plants. Studies have reported that inoculation with Trichoderma in the early stage of the crop maximizes its benefits in terms of root development and nutrient absorption; however, the response in plant growth depends on the specific crop or plant genotype (LÓPEZ-BUCIO et al., 2015).
Growth promotion in plants by Trichoderma spp. can be influenced by gibberellin and auxin production, such as indoleacetic acid, which develops lateral roots. This development increases crop productivity, allowing greater adaptation to abiotic conditions and improving nutrient uptake (CHAGAS JUNIOR et al., 2010).
Another characteristic of endophytic Trichoderma species is the secretion of beneficial secondary metabolites to the host plant, which may be involved in inducing plant resistance (GHAFFARI et al., 2016) and as a result, increasing the plant defense against various causal agents of plant and insect diseases (ZIN & BADALUDDIN, 2020), a characteristic that helps the plant in the early stages of development. At the same time, genomic and metabolic modification in the host plant is triggered by this endophytic fungus during root establishment (GHAFFARI et al., 2016).
Effect of endophytus inoculant on the plant vigor
Regarding plant vigor (Table 6), it was observed in the trial conducted in Ponta Grossa that the doses of 150 and 200 g. 50 kg seeds-1 differed statistically from the control (Co-Mo Platinum).
In Paranapanema, at the dose of 150 g. 50 kg seeds-1, the vigor achieved was 5.75, and in Bandeirantes, the dose of 200 g. 50 kg seeds-1 differed statistically from the control (Co-Mo Platinum), reaching a score of 6.0 in plant vigor. In Paranavaí, no changes were observed regarding plant vigor as a result of Endophytus inoculant application.
In a study, OLIVEIRA et al. (2009) places the seedling emergence percentage and emergence speed tests as the most used to evaluate plant vigor at the field level. Therefore, the evaluations in the study made it possible to verify that the dosages 150 and 200 g. 50 kg seeds-1 differed from the other treatments, especially the control, showing that the vigor tests had a direct influence on the emergence speed with normal and stronger plants due to of Endophytus dosage.
Effect of endophytus inoculant on nodulation of soybean plants
The Endophytus inoculant did not interfere in the nodulation process of soybean plants. On the contrary, application via seed had a positive impact on nodulation when comparing the treatments which received inoculant with the control plots (Table 4). In the study developed in Ponta Grossa, it was observed that the highest dose showed the greatest nodulation (Table 4), and all doses differed statistically from the control and positive control when comparing the means using the Duncan test. at the 5 % probability level. Regarding nodule weight, the doses of 150 and 200 g. 50 kg seeds-1 differed from the control.
For the experiment conducted in Paranapanema, doses of 100 - 200 g. 50 kg seeds-1 showed the highest number of nodules (Table 4), being the dose of 150 g. 50 kg seeds-1 the treatment that presented the highest number of nodules. As well as, the study conducted in Bandeirantes, also showed that doses of 100 - 200 g. 50 kg seeds1 had the highest number of nodules, being statistically different from the control.
Conversely, in the experiment carried out in Paranavaí, the two highest doses of the Endophytus inoculant presented the highest number of nodules, statistically differing from the control. The highest dose presented the highest nodule weight value (Table 4). It is important to highlight that the Endophytus inoculant is at doses of 150 and 200 g. 50 kg seeds-1 showed a greater number of nodules compared to the standard product ICB Nutrisolo, in the four locations evaluated.
The application of Endophytus inoculant also had a positive effect on soybean nodulation, with an increase in the number and dry weight of nodules. Similar results were reported with the inoculation of other Trichoderma species such as T. harzianum (MWEETWA et al., 2016; ITURRALDE et al., 2020) and T. asperellum (MACENA et al., 2020), which when applied via seed, showed a positive effect on increasing soybean nodulation, as well as increasing root and shoot biomass (MACENA et al., 2020). The application of Trichoderma increases root development, proliferation of secondary roots, fresh mass of seedlings, as well as leaf area (HARMAN, 2000). The phytostimulatory effect of Trichoderma is attributed to several direct and indirect effects, including the release of auxins and homologous substances such as indole-3-acetaldehyde, indole-3-carboxaldehyde and indole-3-ethanol (CONTRERAS-CORNEJO et al., 2009).
Effect of endophytus inoculant on dry mass of the root
The application of the Endophytus inoculant also had a positive impact on root biomass, with an increase in dry weight observed in plots that were inoculated via seed (Table 7). In Ponta Grossa, it was observed that doses of 100 - 200 g. 50 kg seeds-1 differed statistically from the control. In Paranapanema, the two highest doses differed from the control. It is important to highlight that the dose of 150 g. 50 kg seeds-1 presented the highest root biomass in this location (Table 7), like the results obtained in the emergence and final stand of plants (Table 5).
In a study using Trichoderma spp. concluded a positive increase in fresh and dry mass of passion fruit plants, corroborating the importance of using the inoculant Trichoderma based (SANTOS et al., 2010).
In Bandeirantes and Paranavaí, the highest dose of Endophytus inoculant presented higher dry root weight, statistically differing from the control; however, doses of 100 and 150 g. 50 kg seeds-1 were also statistically different from the control (Table 7), and in comparison, with the positive control, the Endophytus inoculant presented greater biomass in the four locations.
Compared to the standard product (ICB Nutrisolo Trichoderma), doses of 150 and 2000 g. 50 kg seeds-1 showed a similar or higher biomass. In general, the results indicated that the application of the Endophytus inoculant has a positive effect on the development of the roots of soybean plants. Corroborating with VINALE et al. (2008) and CONTRERAS-CORNEJO et al. (2009) who observed in their studies that Trichoderma species promotes the growth of the aerial part of plants and that it produces auxins and metabolites that favor root development. JESUS et al. (2011) also showed a positive effect on the increase in root, shoot, and total biomass, as well as an increase in the efficiency of phosphorus absorption when using Trichoderma asperellum as a substrate conditioner to produce coffee seedlings.
The positive effects of Trichoderma inoculation may be related to root exudation. Evidence of this relationship has been reported in other legumes such as common beans, where inoculation with Trichoderma promoted crop growth (HOYOS-CARVAJAL et al., 2009; PEDRO et al., 2012), partly in response to bean root exudation, which is a source of L-tryptophan, a precursor of auxin synthesis (JUNIOR et al., 2019).
Effect of endophytus inoculant on dry mass of the aerial part
The Endophytus inoculant had a positive effect on increasing the biomass of the aerial part of soybean plants (Table 8). Using Trichoderma asperellum UFT 201 CHAGAS et al. (2017b) present positive results in biomass accumulation for soybean, cowpea, rice, and corn crops.
The average weight dry mass of the aerial part and variation in values about the control V(%), in evaluations carried out at the beginning of flowering (BBCH - 51) in the soybean crop. 2020/21 harvest.
In the experiment conducted in Ponta Grossa and Paranapanema, the greatest increase in dry mass was observed in the plots that received the Endophytus inoculant at doses of 100 and 200 g. 50 kg seeds-1, presenting an average weight statistically higher than the obtained in the control and positive control, when the means were compared using the Duncan test at 5 % probability.
In Bandeirantes, the highest dose of Endophytus was the only one that statistically differed from the control. Conversely, in the Paranavaí experiment, it was observed that the application of doses of 150 and 200 g. 50 kg seeds-1 presented an average weight statistically higher than the control plots (Table 8).
In bean cultivation, CARVALHO et al. (2011) tested the effect of Trichoderma spp. and observed that they provided increases in the dry matter mass of the aerial part of the plants. As well as in SILVA (2011), which the inoculation of Trichoderma harzianum (IB42/03) in cucumber culture promoted gains in the dry mass of the aerial part. Supporting the results obtained in this study, since evaluations of the application of Endophytus at a dosage of 200 g. 50 kg seeds-1 also provided increases in mass as a function of growth.
Effect of endophytus inoculant on productivity
The positive effects in promoting soybean growth provided by the application of different doses of the Endophytus inoculant were reflected in the increase in productivity as well as the increase in the mass of one thousand grains (Table 9). In general terms, the average productivity of the treatments that received doses of 100 - 200 g. 50 kg seeds-1, presented an average yield statistically higher than the control and the positive control, a yield that was similar or higher than that obtained in the plots that were treated with ICB Nutrisolo Trichoderma. In the experiment conducted in Ponta Grossa, the highest dose statistically differed from the control in the mass of one thousand grains and grain yield. It is noteworthy that the two previous doses also promoted an increase in yield of up to 10.58 % compared to the control (Table 9).
In Paranapanema, the two highest doses differed statistically from the control and the positive control, in the evaluations of mass of one thousand grains and productivity, in the dose of 150 g. 50 kg seeds-1 and 7, 8 % at a dose of 200 g. 50 kg seeds-1 (Table 9). In the experiment conducted in Bandeirantes, the dose of 200 g. 50 kg seeds-1 stood out among the treatments and differed statistically from the control, promoting an increase in grain (Table 9). VERGARA et al. (2019) obtained results in which inoculated plants show better performance in physiological processes and growth indicators, resulting in greater productivity.
The average productivity obtained in Paranavaí in treatments that received doses of 100 - 200 g. 50 kg seeds-1 differed statistically from the control and the positive control, with the dose of 200 g. 50 kg seeds-1 being the one that presented the highest yield. Similar results were found by CHAGAS JUNIOR et al. (2010), in studies evaluating soybean productivity depending on inoculation, where they observed an increase of up to 10 %.
GONÇALVES et al. (2018) used inoculation with Trichoderma and obtained increases of more than 30 % in productivity compared to non-inoculated soybeans, demonstrating the importance of using adequate form and dosages of the inoculant. Highlighting the importance and relevance of the study applied in different soil and climatic conditions, it shows the contribution of Endophytus in specific doses of 150 and 200 g. 50 kg seeds-1 in soybean cultivation to improve productivity without affecting environmental conditions.
Phytotoxic effect
No phytotoxicity effects that may have been caused by the formulation of the Endophytus inoculant (Trichoderma endophyticum 1 x 109 UFC.g-1) were observed in the evaluations carried out 7 and 15 days after emergence, with the soybean plants showing normal development, reaching grade 1 (without damage) according to the scale proposed by EWRC (1964). Although, Trichoderma spp. infect roots, they are not generally plant pathogens, with only a few strains reported to cause disease in crops.
Although, research is restricted to verifying the effect of T. endophyticum in promoting the growth of crops of agricultural interest, the results obtained in the present research highlighted the positive effect on emergence and final stand, nodulation, and biomass of plants, which were reflected in the increase in soybean productivity.
CONCLUSION
The Endophytus inoculant based on Trichoderma endophyticum applied via seed had a positive impact on promoting the growth of soybean plants and did not cause any symptoms of phytotoxicity. Inoculation using the dose of 200 g. 50 kg seeds-1 showed a more constant result in most of the variables analyzed (germination and final plant stand, number of nodules, biomass of the shoot and root), in the four locations under study in different soil and climate regions. The gains in the analyzed parameters provided by the Endophytus inoculant application were reflected in high productivity values, with the dose of 200 g. 50 kg seeds-1.
ACKNOWLEDGEMENTS
We would like to thank the 3M Agricultural Experimentation for the partnership for the field tests. And was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasil - Finance code 001.
REFERENCES
- BBCH-ESTÁDIOS DE CULTURAS. Código decimal para a descrição dos estádios de desenvolvimento de plantas. PF/Pesquisa. 2001.
- BRASIL. Instrução Normativa Nº 1, de 2 de fevereiro de 2012. Diário Oficial da União, Brasília, DF, 07 fev. 2012, Seção 1 e 08 fev. 2012, Seção 1.
- BRASIL. Ministro de estado da agricultura, pecuária e abastecimento. Instrução normativa nº 53, de 23 de outubro de 2013. Que estabelece critérios de registro e produção de inoculantes. Diário oficial da União: seção 1, 24 de outubro de 2013.
-
CANTERI, M. G. et al. SASM - Agri: System for analysis and mean separation in agricultural assays using Scott-knott, Tukey and Duncanmethods. Revista Brasileira de Agrocomputação, v.1, n.2, p.18-24, 2001. Available from: <Available from: https://agrocomputacao.deinfo.uepg.br/dezembro_2001/Arquivos/RBAC_01_02.pdf >. Accessed: Aug. 01, 2021.
» https://agrocomputacao.deinfo.uepg.br/dezembro_2001/Arquivos/RBAC_01_02.pdf -
CARVALHO, D. D. C. et al. Biocontrol of seed pathogens and growth promotion of common bean seedlings by Trichoderma harzianum Pesquisa Agropecuária Brasileira, Brasília-DF, v.46, n.8, p.822-828, 2011. Availablefrom: <Availablefrom: https://www.scielo.br/j/pab/a/RxqNb8mYbDsqm97LQVyQKMG/?lang=en# >. Accessed: Jan. 22, 2024. doi: 10.1590/S0100-204X2011000800006.
» https://doi.org/10.1590/S0100-204X2011000800006.» https://www.scielo.br/j/pab/a/RxqNb8mYbDsqm97LQVyQKMG/?lang=en# -
CHAGAS, L. F. B. et al. Trichoderma na promoção do crescimento vegetal. Revista de Agricultura Neotropical, v.4, n.3, p.97-102, 2017a. Available from: <Available from: https://periodicosonline.uems.br/index.php/agrineo/article/view/1529 >. Accessed: Jan. 10, 2024. doi: 10.32404/rean.v4i3.1529.
» https://doi.org/10.32404/rean.v4i3.1529.» https://periodicosonline.uems.br/index.php/agrineo/article/view/1529 -
CHAGAS, L. F. B. et al. Trichoderma asperellum efficiency in soybean yield components. Comunicata Scientiae, v.08, n.1, p.165-169, 2017b. Available from: <Available from: https://www.comunicatascientiae.com.br/comunicata/article/view/1754 >. Accessed: Jan. 22, 2024. doi: 10.14295/cs.v8i1.1754.
» https://doi.org/10.14295/cs.v8i1.1754.» https://www.comunicatascientiae.com.br/comunicata/article/view/1754 -
CHAGAS JUNIOR, J. R. et al. Eficiência agronômica de estirpes de rizóbio inoculadas em feijão-caupi no Cerrado, Gurupi-TO. Revista Ciência Agronômica, v.41, n.4, p.709-714, 2010. Available from: <Available from: https://www.scielo.br/j/rca/a/SHqXkDNwQQd7sHrfYC5zk8k/ >. Accessed: Dec. 02, 2023. doi: 10.1590/S1806-66902010000400027.
» https://doi.org/10.1590/S1806-66902010000400027.» https://www.scielo.br/j/rca/a/SHqXkDNwQQd7sHrfYC5zk8k/ -
CHAVERRI, P. et al. Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia, v.107, n.3, p.558-590, 2015. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4885665/pdf/emss-60079.pdf >. Accessed: Aug. 12, 2024. doi: 10.3852/14-147.
» https://doi.org/10.3852/14-147.» https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4885665/pdf/emss-60079.pdf -
CONTRERAS-CORNEJO, H. A. et al. Trichoderma virens, a plant-beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiology, v.149, p.1579-1592, 2009. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2649400/ >. Accessed: Jan. 10, 2024. doi: 10.1104/pp.108.130369.
» https://doi.org/10.1104/pp.108.130369.» https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2649400/ -
CONTRERAS-CORNEJO, H. A. et al. Mechanisms for plant growth promotion activated by Trichoderma in natural and managed terrestrial ecosystems. Microbiological Research, v.281, 2024. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S0944501324000223 >. Accessed: Aug. 10, 2024. doi: 10.1016/j.micres.2024.127621.
» https://doi.org/10.1016/j.micres.2024.127621.» https://www.sciencedirect.com/science/article/abs/pii/S0944501324000223 -
CORDIER, C.; ALABOUVETTE, C. Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non target soil micro-organisms. European Journal of Soil Biology, v.45, n.3, p.267-274, 2009. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S1164556308001556 >. Accessed: Mar. 04, 2024. doi: 10.1016/j.ejsobi.2008.12.004.
» https://doi.org/10.1016/j.ejsobi.2008.12.004.» https://www.sciencedirect.com/science/article/abs/pii/S1164556308001556 -
ELAD, Y. et al. Degradation of plant pathogenic fungi by Trichoderma harzianum Canadian Journal of Microbiology, v.28, p.719-725, 1982. Available from: Available from: https://cdnsciencepub.com/doi/10.1139/m82-110 >. Accessed: Mar. 04, 2024. doi: 10.1139/m82-110.
» https://doi.org/10.1139/m82-110.» https://cdnsciencepub.com/doi/10.1139/m82-110 - EUROPEAN WEED RESEARCH COUNCIL - EWRC. Report of 3rd and 4th meetings of - committee of methods in weed research. Weed Research, v.4, n.1, p.88, 1964.
-
GHAFFARI, M. R. et al. Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant Molecular Biology, v.90, p.699-717, 2016. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/26951140/ >. Accessed: Mar. 04, 2024. doi: 10.1007/s11103-016-0461-z.
» https://doi.org/10.1007/s11103-016-0461-z.» https://pubmed.ncbi.nlm.nih.gov/26951140/ -
GOMES, E. A. et al. Microrganismos Promotores do Crescimento de Plantas. Sete Lagoas: Embrapa Milho e Sorgo. 2016. 51 p. Available from: <Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1063799 >. Accessed: Mar. 11, 2024.
» https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1063799 -
GONÇALVES, A. H. et al., Trichoderma efficiency in the maintenance and productivity of soybean plants in producing savanna regions, Tocantins, Brazil. Revista de Ciências Agrárias, v.41, n.1, p.175-181, 2018. Available from: <Available from: https://revistas.rcaap.pt/index.php/rca/article/view/16637 >. Accessed: Jan. 22, 2024. doi: 10.19084/RCA17079.
» https://doi.org/10.19084/RCA17079.» https://revistas.rcaap.pt/index.php/rca/article/view/16637 -
HARMAN, G. E. Myths and dogmas of biocontrol - changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis., v.84, p.377-393, 2000. Available from: <Available from: https://apsjournals.apsnet.org/doi/abs/10.1094/PDIS.2000.84.4.377?url_ver=Z39.88-2003𝔯_id=ori:rid:crossref.org𝔯_dat=cr_pub%20%200pubmed >. Accessed: Jan. 22, 2024. doi: 10.1094/PDIS.2000.84.4.377.
» https://doi.org/10.1094/PDIS.2000.84.4.377.» https://apsjournals.apsnet.org/doi/abs/10.1094/PDIS.2000.84.4.377?url_ver=Z39.88-2003𝔯_id=ori:rid:crossref.org𝔯_dat=cr_pub%20%200pubmed -
HOYOS-CARVAJAL, L. et al. Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biological Control, v.51, n.3, p.409-416, 2009. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S1049964409001960 >. Accessed: Jan. 22, 2024. doi: 10.1016/j.biocontrol.2009.07.018.
» https://doi.org/10.1016/j.biocontrol.2009.07.018.» https://www.sciencedirect.com/science/article/pii/S1049964409001960 -
HUNGRIA, M.; MENDES, I. C. Nitrogen fixation with soybean: the perfect symbiosis? In: DE BRUIJN, F. J. (Ed.). Biological nitrogen fixation, v.2. Hoboken, New Jersey: John Wiley & Sons, Inc., p.1009-1023, 2015. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S1049964409001960?via%3Dihub >. Accessed: Dec. 15, 2023. doi: 10.1016/j.biocontrol.2009.07.018.
» https://doi.org/10.1016/j.biocontrol.2009.07.018.» https://www.sciencedirect.com/science/article/abs/pii/S1049964409001960?via%3Dihub -
ITURRALDE, E. T. et al. Coinoculation of soybean plants with Bradyrhizobium japonicum and Trichoderma harzianum: Coexistence of both microbes and relief of nitrate inhibition of nodulation. Biotechnology Reports, v.26, e00461, 2020. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S2215017X19303790 >. Accessed: Dec. 02, 2023. doi: 10.1016/j.btre.2020.e00461.
» https://doi.org/10.1016/j.btre.2020.e00461.» https://www.sciencedirect.com/science/article/pii/S2215017X19303790 -
JESUS, E. P. et al. Avaliação do potencial de Trichoderma asperellum como condicionador de substrato para a produção de mudas de café. Cerrado Agrociência, Patos de Minas, MG, v.2, n.2, p.7-19, 2011. Available from: <Available from: https://revistas.unipam.edu.br/index.php/cerradoagrociencias/article/view/4177/1842 >. Accessed: Feb. 19, 2024.
» https://revistas.unipam.edu.br/index.php/cerradoagrociencias/article/view/4177/1842 -
JUNIOR, L. M. et al. Uso de Trichoderma na cultura do feijão-comum. In: MEYER, M. C. et al. Trichoderma uso na agricultura. Brasília: Embrapa, 2019, 538 p. Available from: <Available from: http://www.alice.cnptia.embrapa.br/alice/handle/doc/1117296 >. Accessed: Jan. 22, 2024.
» http://www.alice.cnptia.embrapa.br/alice/handle/doc/1117296 - KÖPPEN, W.; GEIGER, R. Klimate der Erde. Gotha: Verlag Justus Perthes. 1928.
-
LÓPEZ-BUCIO, A. J. et al. Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Scientia Horticulturae, v.196, p.109-123, 2015. Available from: <Available from: http://www.sciencedirect.com/science/journal/03044238 >. Accessed: Feb. 19, 2024. doi: 10.1016/j.scienta.2015.08.043.
» https://doi.org/10.1016/j.scienta.2015.08.043.» http://www.sciencedirect.com/science/journal/03044238 -
MACENA, A. M. F. et al. Antagonism of Trichoderma-based biofungicides against Brazilian and North American isolates of Sclerotinia sclerotiorum and growth promotion of soybean. BioControl, v.65, p.235-246, 2020. Available from: <Available from: https://link.springer.com/article/10.1007/s10526-019-09976-8 >. Accessed: Jan. 22, 2024. doi: 10.1007/s10526-019-09976-8.
» https://doi.org/10.1007/s10526-019-09976-8.» https://link.springer.com/article/10.1007/s10526-019-09976-8 -
MELLO, S. C. M. et al. Controle de Doenças de Plantas. In: FONTES, E. M. G, VALADARES-INGLIS, M. C. Controle Biológico de Pragas da Agricultura. 1ed. Brasília: Embrapa , p.291-325, 2020. Available from: <Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/1121825/1/CBdocument.pd >. Accessed: Mar. 11, 2024.
» https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/1121825/1/CBdocument.pd -
MONTE, E. et al. Trichoderma e seus mecanismos de ação para o controle de doenças de plantas In: MEYER, M. C. et al. Trichoderma uso na agricultura. Brasília: Embrapa , 2019, 538 p. Available from: <Available from: http://www.alice.cnptia.embrapa.br/alice/handle/doc/1117296 >. Accessed: Feb. 08, 2024.
» http://www.alice.cnptia.embrapa.br/alice/handle/doc/1117296 -
MWEETWA, A. M. et al. Nodulation, nutrient uptake and yield of common bean Inoculated with Rhizobia and Trichoderma in an acid soil. Journal of Agricultural Science, v.8, n.12, 2016. Available from: <Available from: https://ccsenet.org/journal/index.php/jas/article/view/62757#:~:text=Inoculating%20common%20bean%20with%20Rhizobia,subsequent%20biomass%20or%20grain%20yields >. Accessed: Feb. 19, 2024. doi: 10.5539/jas.v8n12p61.
» https://doi.org/10.5539/jas.v8n12p61.» https://ccsenet.org/journal/index.php/jas/article/view/62757#:~:text=Inoculating%20common%20bean%20with%20Rhizobia,subsequent%20biomass%20or%20grain%20yields -
NOGUEIRA, M. A. et al. Ações de transferência de tecnologia em inoculação/coinoculação com Bradyrhizobium e Azospirillum na cultura da soja na safra 2017/18 no estado do Paraná. Embrapa Soja: Circular Técnica N. 143. Londrina, BR, 2018, 16 p. Available from: <Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1095314 >. Accessed: Jan. 12, 2024.
» https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1095314 -
OLIVEIRA, A. G. et al. Potencial de solubilização de fosfato e produção de AIA por Trichoderma spp. Revista Verde de Agroecologia e Desenvolvimento Sustentável, v.7, n.3, p.149-155, 2012. Available from: <Available from: https://dialnet.unirioja.es/descarga/articulo/7419841.pdf >. Accessed: Mar. 04, 2024.
» https://dialnet.unirioja.es/descarga/articulo/7419841.pdf - OLIVEIRA, A. C. S. et al. Testes de vigor em sementes baseados no desempenho de plântulas. Inter Science Place, 21 p.2009.
-
PEDRO, E. A. S. et al. Promoção do crescimento do feijoeiro e controle da antracnose por Trichoderma spp. Pesquisa Agropecuária Brasileira, v.47, n.11, p.1589-1595, 2012. Available from: <Available from: https://www.scielo.br/j/pab/a/zyPkc5pmTsLQQLxYqdhH36C/abstract/?lang=pt >. Accessed: Mar. 11, 2024. doi: 10.1590/S0100-204X2012001100005.
» https://doi.org/10.1590/S0100-204X2012001100005.» https://www.scielo.br/j/pab/a/zyPkc5pmTsLQQLxYqdhH36C/abstract/?lang=pt -
HUNGRIA, M. et al. Protocolo para análise da qualidade e da eficiência agronômica de inoculantes, cepas e outras tecnologias relacionada ao processo de fixação biológica do nitrogênio em leguminosas. In: CAMPO, R. J.; HUNGRIA, M. Anais da XIII Reunião da Rede de Laboratórios para Recomendação, Padronização e Difusão de Tecnologia de inoculantes Microbianos de interesse Agrícola (RELARE). - Londrina: Embrapa Soja, 2007. 212p. Available from: <Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1044383 >. Accessed: Jan. 12, 2024.
» https://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1044383 -
SÁ, R. A. et al. Trichodermana promoção de crescimento da cultura da soja na região oeste do Paraná. Contribuciones a Las Ciencias Sociales, v.17, n.1, p.1194-1208, 2024. Available from: <Available from: https://ojs.revistacontribuciones.com/ojs/index.php/clcs/article/view/3380/26 >. Accessed: Mar. 04, 2024. doi: 10.55905/revconv.17n.1-065.
» https://doi.org/10.55905/revconv.17n.1-065.» https://ojs.revistacontribuciones.com/ojs/index.php/clcs/article/view/3380/26 - SANTOS, H. A. et al. Associação de isolados de Trichoderma spp. e ácido indol-3-butírico (AIB) na promoção de enraizamento de estacas e crescimento de maracujazeiro. Bioscience Journal, v.26, n.6, p.966-972, 2010. Available from: <https://seer.ufu.br/index.php/biosciencejournal/article/view/7212>. Accessed: Feb. 08, 2024.
-
SEIXAS, C. D. S. et al. Tecnologias de produção de soja. Londrina: Embrapa Soja , 2020. Avaiable from: < Avaiable from: http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1123928 >. Accessed: Feb. 19, 2024.
» http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1123928 -
SILVA, J. C. et al. Rice sheath blight biocontrol and growth promotion by Trichoderma isolates from the Amazon. Amazonian Journal of Agricultural and Environmental Sciences, v.55, n.4, p.243-250, 2012. Available from: <Available from: http://www.periodicos.ufra.edu.br/index.php/ajaes/article/view/731/262 >. Accessed: Mar. 04, 2024. doi: 10.4322/rca.2012.078.
» https://doi.org/10.4322/rca.2012.078.» http://www.periodicos.ufra.edu.br/index.php/ajaes/article/view/731/262 -
SILVA, V. N. et al. Growth promotion and resistance induction against anthracnose in cucumber using Trichoderma spp. Pesquisa agropecuária brasileira, v.46, n.12. p.1609-1618, 2011. Available from: <Available from: https://www.scielo.br/j/pab/a/KKPwCh9KBsbPfXQsGTKqKfj/?lang=pt >. Accessed: Dec. 08, 20024. doi: 10.1590/S0100-204X2011001200005.
» https://doi.org/10.1590/S0100-204X2011001200005.» https://www.scielo.br/j/pab/a/KKPwCh9KBsbPfXQsGTKqKfj/?lang=pt -
VERGARA, C. et al. Dark septate endophytic fungi increase the activity of proton pumps, efficiency of 15N recovery from ammonium sulphate, N content, and micronutrient levels in rice plants. Brazilian Journal of Microbiology, v.9, p.613, 2019. Available from: <Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6863334/ >. Accessed: Jan. 22, 2024. doi: 10.1007/s42770-019-00092-4.
» https://doi.org/10.1007/s42770-019-00092-4.» https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6863334/ -
VINALE, F. et al. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiological and Molecular Plant Pathology, v.72, n.1-3, p.80-86, 2008. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S0885576508000568 >. Accessed: Dec. 02, 2023. doi: 10.1016/j.pmpp.2008.05.005.
» https://doi.org/10.1016/j.pmpp.2008.05.005.» https://www.sciencedirect.com/science/article/abs/pii/S0885576508000568 -
WOO, S. L. et al. Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal, v.8, p.71-126, 2014. Available from: <Available from: https://benthamopen.com/ABSTRACT/TOMYCJ-8-71 >. Accessed: Jan. 10, 2024. doi: 10.2174/1874437001408010071.
» https://doi.org/10.2174/1874437001408010071.» https://benthamopen.com/ABSTRACT/TOMYCJ-8-71 -
ZIN, N. A.; BADALUDDIN, N. A. Biological functions of Trichoderma spp. for agriculture applications. Annals of Agricultural Sciences, v.65, p.168-178, 2020. Available from: <Available from: https://www.sciencedirect.com/science/article/pii/S0570178320300415 >. Accessed: Mar. 04, 2024. doi: 10.1016/j.aoas.2020.09.003.
» https://doi.org/10.1016/j.aoas.2020.09.003.» https://www.sciencedirect.com/science/article/pii/S0570178320300415
Edited by
-
Editors
Alessandro Dal’Col Lúcio (0000-0003-0761-4200) Diego Follmann (0000-0002-7351-7022)
Publication Dates
-
Publication in this collection
24 Mar 2025 -
Date of issue
2025
History
-
Received
26 Mar 2024 -
Accepted
14 Oct 2024 -
Reviewed
31 Jan 2025
