IntechOpen

Home > Books > Trichoderma - Technology and Uses

Open access peer-reviewed chapter

Using Trichoderma to Manage Sclerotia-Producing Phytopathogenic Fungi

Written By

Jéssica Rembinski, Silvino I. Moreira, Jorge T. De Souza, Alan C.A. Souza, Adriano F. Dorigan, Eduardo Alves, Breno C.M. Juliatti and Fernando C. Julliati

Submitted: 21 December 2021 Reviewed: 03 January 2022 Published: 31 August 2022

DOI: 10.5772/intechopen.102426

Trichoderma IntechOpen
Trichoderma Technology and Uses Edited by Fernando Juliatti

From the Edited Volume

Trichoderma - Technology and Uses

Edited by Fernando Cezar Juliatti

Book Details Order Print

Chapter metrics overview

142 Chapter Downloads

View Full Metrics
Advertisement

Abstract

Sclerotia are resistance structures that allow several soil-borne plant pathogens to survive for extended periods of time. The white mold disease, caused by Sclerotinia sclerotiorum and the stem rot in Allium spp., caused by Stromatinia cepivora are examples of destructive pathogens in which sclerotia are the central survival structure in their life cycle. In this chapter, we explore the information on the use of Trichoderma to manage sclerotia-producing pathogens in Brazil. There are 34 registered commercial products registered in Brazil, and most of them are recommended to manage sclerotia-producing fungi. The mechanisms of action of Trichoderma against these pathogens involve mainly mycoparasitism. The number of species employed as active ingredients of these commercial products is very limited, although many other species have shown a high potential against these pathogens. The white mold pathogen in soybean was taken as an example of field management, where the technical recommendations are detailed. This management involves other practices in addition to the application of Trichoderma in an integrated manner, and they are essential to manage this disease in the field in Brazil.

Keywords

  • biological control
  • white mold
  • white rot
  • resistance structure
  • plant disease management

1. Introduction

Sclerotia are survival melanized structures of different sizes and shapes depending on the fungal species and host plant. They remain viable in soil for long periods of time and are resistant to chemicals, adverse conditions, and biological degradation [1]. Sclerotinia sclerotiorum, Rhizoctonia solani, Athelia rolfsii, Stromatinia cepivora, and Microphomina phaseolina are among the most harmful sclerotia-producing phytopathogenic fungi in agriculture [2, 3, 4, 5, 6]. These pathogens are hard to manage and cause expanding losses in horticultural crops worldwide due to their survival capabilities associated with successive production of the same crop in the field and the lack of safe and efficient soil fumigation methods.

Biological control products formulated with Trichoderma have grown as the best method to manage sclerotia-producing pathogens, once chemicals in soil are often inefficient, too expensive, and too environmentally harmful. All Trichoderma species are able to utilize the cell content of other fungi as a source of nutrients [7, 8, 9]. However, certain species are more adapted to parasitize sclerotia of pathogenic fungi [2, 3, 4, 5, 6, 10, 11, 12]. These species are able to successfully invade, parasitize, and kill sclerotia in soil, meaning that the capacity to survive and compete in this environment is an absolute requirement. Although Trichoderma is one of the most commonly found genera in soil, not all species of the genus are well adapted to survive and thrive in soil [13]. The species adapted to soil need to be equipped with structures such as chlamydospores to ensure their long-term survival.

Trichoderma is a hyper diverse genus, with more than 350 species already described [14]. Only a small fraction of these species were developed into commercial products. This raises the questions which Trichoderma species have potential to be commercialized? Only the limited number of species that is well adapted to the soil environment and frequently are the active ingredients of formulations. Or is there any potential in the unexploited species?

In this chapter, we adopted a more practical view of the use of Trichoderma to control sclerotia-producing fungal plant pathogens. More emphasis is given on the mechanisms employed by Trichoderma, the species used in commercial formulations and the practical use of Trichoderma to control sclerotia producers in the field in Brazil, where products containing these fungi are used by farmers to manage white mold disease in soybean.

Advertisement

2. Plant pathogens capable of producing sclerotia

Sclerotia-producing fungi are very diverse, including saprotrophic, plant, animal and insect pathogens, mycoparasites, endophytes, insect symbionts, ecto- and ericoid-mycorrhizal fungi, and lichenicolous fungi [15]. However, they seem to be exclusively produced by fungi in the phyla Ascomycota and Basidiomycota that comprise the subkingdom Dikarya of the kingdom Fungi [15]. Sclerotia were documented in at least 85 fungal genera and 20 orders [15]. Outside of the kingdom fungi, sclerotia are relatively well studied in the slime molds or Myxomycetes [16], which belong to the kingdom Amoebozoa.

Sclerotia-producing fungi may be found in tropical and temperate regions, although sampling for these structures in natural environments is still scarce [15]. The structure and shape of fungal sclerotia are highly variable. While some are surrounded by much defined melanized ring encircling undifferentiated hyphae, others lack a distinct ring [17]. Some species, such as Athelia rolfsii, produce sclerotia with a round and smooth surface and dark color, whereas other fungi such as Rhizoctonia solani produce sclerotia with an irregular shape and lighter color. Some sclerotia are very small (sometimes smaller than 1 mm) such as the ones produced by Macrophomina phaseolina, Stromatinia cepivora, and Verticillium dahliae, whereas some fungal species, such as Polyporus mylittae, are able to produce giant sclerotia of up to 40 cm in diameter [18]. Fungi, such as Claviceps purpurea, Sclerotinia sclerotiorum, Botrytis cinerea, Monilinia spp., produce apothecia, which are sexual reproductive structures, directly on the sclerotia, whereas Aspergillus flavus produces cleistothecia inside the sclerotia [19].

Garlic and soybean are examples among the economically important crops where Trichoderma has been used to manage sclerotia-producing pathogens, at least under experimental conditions. Garlic cultivation in Brazil is done in the provinces of Goiás, Minas Gerais, Santa Catarina, and Rio Grande do Sul and it reached 118,000 tons in 2018 [20]. High losses have been induced by the white rot disease caused by the fungus Stromatinia cepivora, which is a pathogen specific to plants of the family Alliaceae [21]. Stromatinia cepivora belongs in the Ascomycota phylum, Helotiales order, and Sclerotiniaceae family [22]. The white rot caused in plants of the Alliaceae family presents well characterized symptoms, such as yellowing and death of infected leaves, owing to the root system damage caused by the pathogen. The aerial part of infected plants is easily detached from the soil. In garlic bulbs, the symptoms are soft rot of the tissues and white mycelial on the structural axis of infected plants and production of black microsclerotia on the bulbs [23]. The microsclerotia (ranging from 0.2 to 0.5 mm diameter) can remain dormant and viable in soil for more than 20 years in the absence of suitable host plants [24].

Soybean is an agricultural commodity traded not only in Brazil but is also exported [21]. In this crop, the white mold caused by S. sclerotiorum is considered the second most important disease after soybean rust [24, 25]. Sclerotinia sclerotiorum, which also belongs in the family Sclerotiniaceae, promotes the white mold or sclerotinia stem mold, leading to losses that can reach 70% in productivity. It occurs in approximately 30% of the Brazilian soybean producing area, which is currently more than 35 million ha [26]. The pathogen infects more than 600 plant species and is distributed worldwide. The sclerotia (from 0.5 to 10 mm diameter) are able to survive up to 12 years in soil (50, 51).

Rhizoctonia solani and Athelia rolfsii (syn. Sclerotium rolfsii) are two sclerotia-producing basidiomycetes from the families Ceratobasidiaceae and Atheliaceae, respectively, that cause rots in seeds, roots, stems, leaves, and fruits of a wide range of plant species (52, 53). These pathogens are commonly found in warm climates causing damping-offs, root rots, and wilts. The sclerotia are the only survival structures of these pathogens as they do not reproduce asexually and only rarely reproduce sexually.

These resistance structures are extremely difficult to destroy or inactivate by chemical methods, whereas physical methods such as solarization, inundation, and radiation are not feasible or too expensive to be adopted over large areas. In this context, biological control with antagonistic fungi of the genus Trichoderma is one of the best options available. The advantages of Trichoderma include its mycoparasitic capacity toward these structures, the excellent adaptation of certain species to the soil environment, the safety to humans and animals of the biocontrol species, and the relative ease of mass producing and formulating these agents.

Advertisement

3. Mechanisms employed by Trichoderma against sclerotia producers

The mechanisms of activity present in Trichoderma include mycoparasitism, antibiosis, competition, induction of resistance, and plant growth promotion [27, 28, 29, 30]. Mycoparasitism is the main mechanism employed against sclerotia in soil [31], although the benefits observed in the field probably result from a combination of all mechanisms acting in concert. Mycoparasitism is defined as the ability of organisms to actively parasitize fungi and live at their expense [31]. Mycotrophy, a more inclusive term, may be defined as the ability of organisms to feed on either dead (passive mycotrophy, i.e., saprophytism) or on living fungi (active mycotrophy, i.e., mycoparasitism) [9]. This ability to feed on fungi, either dead or alive, was shown to be the ancestral form of nutrition in all Trichoderma species [13]. Although there are technical differences between mycotrophy and mycoparasitism, the latter term is the only one traditionally employed for Trichoderma in the literature, even in cases where there is no evidence that these fungi killed the host or prey.

Mycoparasitism by Trichoderma involves a sequence of events, including host localization, recognition, direct contact, coiling, formation of hook-shaped structures with appressorium function, penetration, folding, and development of parallel hyphae [29, 31, 32, 33, 34, 35, 36, 37]. It involves a combination of invasive hyphae with secondary metabolites and hydrolytic enzymes in most cases [38]. The wide range of Trichoderma secondary metabolites includes epipolythiodioxopiperazines (ETPs), peptaibols, pyrones, butenolides, pyridines, azaphilones, steroids, anthraquinones, lactones, trichothecenes, and harzianic acid [28]. These compounds can interfere with the metabolic activities of other microorganisms by inhibiting growth and sporulation, reducing spore germination, and weakening the sclerotia. Many Trichoderma species are strong producers of cellulases, chitinases and β-1,3-glucanases, proteases, and lipases, which act in concert with metabolites in the mycoparasitic activity of these fungi [31, 39, 40, 41, 42, 43, 44, 45].

Three distinct strategies of mycoparasitism were described for Trichoderma, which were supported by transcriptomic analyses [7]. These strategies are 1) passive or weak mycoparasitism, where species such as T. reesei have no capacity to stop the growth of fungi, but secrete cell wall degrading enzymes that slowly dissolve the mycelium of the host or prey; 2) strong mycoparasitism occurs in T. atroviride that actively and aggressively grows over the host and parasitizes it swiftly and produces proteases and glucanases; 3) mycoparasitism by lytic enzymes and toxic metabolites, which is observed in T. virens, that first produces metabolites such as gliovirin and gliotoxin that kill the host and later, the mycoparasite moves in and further produces lytic enzymes to digest the mycelium. Probably, strategies 2 and 3 will be more effective against sclerotia producers. There is solid evidence in the literature showing that Trichoderma behaves markedly differently in interactions with different fungal species or Oomycetes [9]. These differences are seen at the phenotypic level and at the gene expression level, where distinct mycoparasitism strategies are employed depending on the host or prey [9].

In this study, scanning electron microscopy observations of in vitro and in soil interactions between Trichoderma spp. and S. sclereotiorum (Tr. × Ssc.) and with Stromatinia cepivora (Tr. × Sce.) were done with scanning electron microscopy (SEM). Colonization of S. sclerotiorum sclerotia and S. cepivora microsclerotia by aerial mycelium of Trichoderma spp. was easily seen with the naked eye 7 days after the inoculation (Figure 1A and I). SEM analysis revealed the Trichoderma aerial mycelia-colonizing sclerotia of Ssc. and Sce. (Figure 1B and J). Conidia and conidiophores of Trichoderma spp. are produced on the surface of the sclerotia (Figure 1C, D, M–O). Cryo-fractures in both Ssc. sclerotia and Sce. microsclerotia evidenced the central medulla enclosed by the outer layer of rind cells free of Trichoderma colonization after 7 and 14 days after the incubation, respectively (Figure 1B and K). Aerial mycelia originated from the sclerotia were efficiently colonized by Trichoderma (Figure 1E–H, M–P). Figure 1G shows decaying hypha of S. sclerotiorum, indicating that cell wall-degrading enzymes acted on the pathogen.

Figure 1.

Scanning electron microscopy (SEM) observations of the interactions between Trichoderma and Sclerotinia sclereotiorum (Tr. × Ssc.) and with Stromatinia cepivora (Tr. × Sce.). A. Photography of Ssc. Sclerotia colonized by Tr. After seven days under 17°C above sterile soil. B–H and J–P: Scanning electron micrographs. B and K. Cryo-fractured Ssc. Sclerotia and Sce. Microsclerotia evidencing the central medulla enclosed by the outer layer of rind cells, respectively. C–D. Trichoderma conidiophores producing conidia above Ssc. Sclerotia surface. E–H. Trichoderma-parasitizing Ssc. Hyphae. I. Photography of Sce. Microsclerotia colonized by Tr. After 14 days under 17°C above sterile soil. J–L. aerial mycelia of Sce. And Trichoderma above Sce. Microsclerotia. M–O. Trichoderma conidia and conidiophores above Sce. Microsclerotial surface. M–P. Trichoderma parasitizing Sce. Hyphae. The hyphae of Ssc. And Sce. were thicker than the hyphae of Trichoderma. a.m. = aerial mycelia; rin. = outer layer of rind cells in sclerotia; c.med. = central medulla enclosed by the rind cells in sclerotia; Tr.con. = Trichoderma conidia; Tr.cdf. = Trichoderma conidiophore; Tr. = Trichoderma; Ssc. = Sclerotinia sclerotiorum; Sce. = Stromatinia cepivora. Scale bars: A and I: 5 cm; B and J: 100 μm; C–H and K–P: 10 μm.

Advertisement

4. Species of Trichoderma employed against sclerotia-producing fungi

In 2014, there were 177 Trichoderma-based fungicides commercially available in the world [46]. These products contained mainly Trichoderma asperellum, T. hamatum, T. harzianum, and T. viride as active ingredients and were recommended mainly for seed and soil treatments [46]. In Brazil, there are currently 34 formulated products with Trichoderma as active ingredients registered in the Ministry of Agriculture, Livestock and Food Supply (MAPA) (Table 1) [39, 47, 48]. These 34 products are based on four species: T. harzianum, T. asperellum, T. koningiopsis, and T. stromaticum. Most products are indicated for sclerotia-producing pathogens, for example, 26 products are recommended for S. sclerotiorum, 23 for R. solani, three for Asclepias rolfsii, and two for Macrophomina phaseolina. Most products are formulated with one strain and only six are combinations of strains. Some of the products are recommended to manage Oomycetes, nematodes, or for Moniliophthora perniciosa, the causative agent of cacao witches’ broom disease (Table 1). No products are available for S. cepivora, even though potential Trichoderma strains are described in the literature [49].

Commercial productActive ingredientStrainOriginTarget pathogen
BF20.001Trichoderma harzianum + Trichoderma asperellum + Bacillus amyloliquefaciensURM 8119 + URM 8120 + CCT 7901Ballagro Agro Tecnologia LTDAColletotrichum lindemuthianum, Sclerotinia sclerotiorum, Rhizoctonia solani
Bio-HulkTrichoderma asperellumBV10Vittia Fertilizantes e Biológicos S.A.Rhizoctonia solani
PardellaTrichoderma harzianum + Trichoderma asperellum + B. amyloliquefaciensURM 8119 + URM 8120 + CCT 7901Ballagro Agro Tecnologia LTDAColletotrichum lindemuthianum, Sclerotinia sclerotiorum, Rhizoctonia solani
QualityTrichoderma asperellumURM 5911Lallemand Soluções Agrobiológicas LtdaFusarium solani f.sp. phaseoli, Sclerotinia sclerotiorum, Rhizoctonia solani
TanusTrichoderma harzianum + Trichoderma asperellum + B. amyloliquefaciensURM 8119 + URM 8120 + CCT 7901Biota Innovations Industria e Comercio de Bioprodutos LtdaColletotrichum lindemuthianum, Sclerotinia sclerotiorum, Rhizoctonia solani
Trichodermax ECTrichoderma asperellumT211Novozymes BioAg Produtos para Agricultura LtdaFusarium solani f.sp. glycines, Sclerotinia sclerotiorum, Rhizoctonia solani
Tricho-GuardTrichoderma asperellumBV10Vittia Fertilizantes e Biológicos S.A.Pratylenchus brachyurus, Rhizoctonia solani, Fusarium oxysporum, Sclerotinia sclerotiorum
Tricho-TurboTrichoderma asperellumBV10Vittia Fertilizantes e Biológicos S.A.Pratylenchus brachyurus, Rhizoctonia solani, Fusarium oxysporum, Sclerotinia sclerotiorum
TríppelTrichoderma asperellumCCT 2165Agrobiológica Sustentabilidade S.A.Rhizoctonia solani, Fusarium oxysporum f.sp. lycopersici
CongreggaTrichoderma asperellumCBMAI 1622Genica Inovação Biotecnologica S.A.Sclerotinia sclerotiorum
TricozakTrichoderma harzianum + Trichoderma asperellum + B. amyloliquefaciensURM 8119 + URM 8120 + CCT 7901Biota Innovations Industria e Comercio de Bioprodutos LtdaColletotrichum lindemuthianum, Sclerotinia sclerotiorum, Rhizoctonia solani
Organic WPTrichoderma asperellumURM 5911Lallemand Soluções Agrobiológicas LtdaFusarium solani f.sp. phaseoli, Rhizoctonia solani
DaytonaTrichoderma harzianumESALQ-1306Koppert do Brasil Holding Ltda.Fusarium solani f.sp. phaseoli, Rhizoctonia solani, Thielaviopsis paradoxa, Pratylenchus zeae, Sclerotinia sclerotiorum
Ecotrich WPTrichoderma harzianumIBLF 006Ballagro Agro Tecnologia LTDASclerotinia sclerotiorum, Rhizoctonia solani, Macrophomina phaseolina, Sclerotium rolfsii
Gaia BioTrichoderma harzianumCCT 7589Simbiose Indústria e Comércio de Fertilizantes e Insumos Microbiológicos Ltda.Sclerotinia sclerotiorum, Rhizoctonia solani
GreenControlTrichoderma harzianumSIMBI T5 (CCT 7589)Simbiose Indústria e Comércio de Fertilizantes e Insumos Microbiológicos Ltda.Sclerotinia sclerotiorum, Fusarium solani f.sp. phaseoli
NatucontrolTrichoderma harzianumBK-Th001Mezfer BR Soluções Agrícolas LtdaSclerotinia sclerotiorum, Fusarium solani f.sp. phaseoli, Rhizoctonia solani
Plant ProtectionTrichoderma harzianumCCT 7589Simbiose Indústria e Comércio de Fertilizantes e Insumos Microbiológicos Ltda.Sclerotinia sclerotiorum, Rhizoctonia solani
PredatoxTrichoderma harzianumIBLF 006Ballagro Agro Tecnologia LTDASclerotinia sclerotiorum, Rhizoctonia solani
ShockerB. amyloliquefaciens + Trichoderma harzianum + B. amyloliquefaciensCPQBA 040-11DRM 01 + CPQBA 040-11DRM 09 + CPQBA 040-11DRM 04Agrivalle Brasil Industria e Comercio de Produtos Agricolas S.A.Sclerotinia sclerotiorum, Rhizoctonia solani
StimucontrolTrichoderma harzianumCCT 7589Simbiose Indústria e Comércio de Fertilizantes e Insumos Microbiológicos Ltda.Sclerotinia sclerotiorum, Rhizoctonia solani
Stimucontrol EvolutionTrichoderma harzianumCCT 7589Simbiose Indústria e Comércio de Fertilizantes e Insumos Microbiológicos Ltda.Sclerotinia sclerotiorum
TorpenoB. amyloliquefaciens + B. amyloliquefaciens + Trichoderma harzianumCPQBA 040-11DRM 01 + CPQBA 040-11DRM 04 + CPQBA 040-11DRM 09Massen Produtos Biologicos S.A.Sclerotinia sclerotiorum, Rhizoctonia solani
Trianum DSTrichoderma harzianumT-22Koppert do Brasil Holding Ltda.Fusarium oxysporum f.sp. lycopersici, Macrophomina phaseolina, Pratylenchus brachyurus, Sclerotinia sclerotiorum, Sclerotium rolfsii
Trianum WGTrichoderma harzianumT-22Koppert do Brasil Holding Ltda.Macrophomina phaseolina, Pratylenchus brachyurus, Sclerotium rolfsii
Trichodermaiz WPTrichoderma harzianumIB19/17Biocontrol Sistema de Controle Biológico LtdaSclerotinia sclerotiorum
Trichodermil SC 1306Trichoderma harzianumESALQ-1306Koppert do Brasil Holding Ltda.Fusarium solani f.sp. phaseoli, Rhizoctonia solani, Thielaviopsis paradoxa, Pratylenchus zeae, Sclerotinia sclerotiorum
Trichodermil Super SC 1306Trichoderma harzianumESALQ-1306Koppert do Brasil Holding Ltda.Fusarium solani f.sp. phaseoli, Thielaviopsis paradoxa, Pratylenchus zeae, Sclerotinia sclerotiorum
Trychonyd FR 25Trichoderma harzianumCCT 6550TZ Biotec LtdaSclerotinia sclerotiorum
WalkerTrichoderma harzianumT-22Koppert do Brasil Holding Ltda.Fusarium oxysporum f.sp. lycopersici, Sclerotinia sclerotiorum
RizodermaTrichoderma harzianumIBLF006Ballagro Agro Tecnologia LTDASclerotinia sclerotiorum, Rhizoctonia solani
TritterTrichoderma harzianumIBLF006Ballagro Agro Tecnologia LTDASclerotinia sclerotiorum, Rhizoctonia solani
Lalnix ResistTrichoderma koningiopsisIBC 56/12Lallemand Soluções Agrobiológicas LtdaMeloidogyne incognita, Pratylenchus brachyurus, Heterodera glycines
TricovabTrichoderma stromaticumCEPLAC 3550CEPLACMoniliophthora perniciosa

Table 1.

Commercial products formulated with Trichoderma strains and registered in the Brazilian Ministry of Agriculture, Livestock and Food Supply [42].

Most commercial products based on Trichoderma are recommended for soil applications. Soil environments have few variations in temperature and humidity than the aerial parts of plants and these biocontrol agents show more potential in more stable niches. In 2020, there were more than 350 described species of Trichoderma in the world [14] and although only a limited number of species (approximately 30) appear to be well adapted to soil environments, the number of species used in commercial products is certainly under-represented. Additionally, it is possible that some of the species listed in Table 1 are not identified correctly at the species level, as shown for members of the T. harzianum species complex [50].

Many species of Trichoderma other than the ones listed in Table 1 were shown to have potential in the inactivation of sclerotia. In vitro assays performed by the first author of this chapter demonstrated the potential of different species of Trichoderma and eight undescribed species to colonize sclerotia of two pathogenic fungi (Table 2). Some of these strains were able to colonize up to 100% of the sclerotia of S. cepivora in soil (Table 2). The sclerotia of S. sclerotiorum appear to be more resistant to colonization than the ones produced by S. cepivora. Some of the novel strains were superior in comparison with a commercial product based on T. harzianum. These data underscore the potential of other than the species that are traditionally commercialized and novel Trichoderma species to be developed into commercial products to control sclerotia-producing plant pathogens. However, this potential has yet to be confirmed in field trials.

StrainSpecies*Colonization (%)
S. cepivoraS. sclerotiorum
Commercial strainT. harzianum7536
TJ01T. nordicum100100
AAUT14T. harzianum69nd**
CX02TR07MTST. harzianum56nd
CX01TR06T. breve55nd
CX01TR02MTNT. breve62nd
CX01TR04T. breve67nd
CX01TRCAMT. atroviride100nd
AAUT7T. orientale71nd
AAUT11T. orientale89nd
CX01TR10Tetramorium camerunense80nd
CB1Trichoderma sp. 154nd
CB7Trichoderma sp. 138nd
CB8Trichoderma sp. 150nd
CX03TR10MTSTrichoderma sp. 293nd
MON10ATrichoderma sp. 310020
MON10BTrichoderma sp. 310038
MON19Trichoderma sp. 310025
MON21Trichoderma sp. 310040
MTS13Trichoderma sp. 410080
CX01TR03Trichoderma sp. 582nd
CX01TR03MTNTrichoderma sp. 587nd
CX01TR4.2MONTrichoderma sp. 569nd
CX02TR18MTSTrichoderma sp. 689nd
CX02TR05MTSTrichoderma sp. 788nd
CX03TR04MTSTrichoderma sp. 788nd
CX01TR4.1MONTrichoderma sp. 890nd
CX01TR02MONTrichoderma sp. 830nd
CX01TR1.2MONTrichoderma sp. 873nd

Table 2.

Colonization of sclerotia of Stromatinia cepivora and Sclerotinia sclerotiorum by strains of Trichoderma.

Sclerotia of the pathogens were placed on the soil surface and sprayed with a suspension of Trichoderma conidia. The boxes containing the sclerotia were incubated at 17°C for S. cepivora and at 25°C for S. sclerotiorum. The evaluations were done at 7 and 14 days after the inoculations. The data are averages of two experiments with five replicates per experiment. * Species identification was done by sequencing the tef-1 fragment. * Not determined.

Advertisement

5. Interaction with other beneficial microorganisms

The combination of more than one biocontrol agent is thought to be advantageous, but it depends on the individual strains compatibility [51]. Six out of the 34 registered products in Brazil are formulated with one or two Trichoderma and Bacillus amyloliquefaciens strains (Table 1). However, it is not known whether these microorganisms are compatible or not or if there is any synergism in their combination. Bacterial genera such as Bacillus and Pseudomonas are potential biocontrol agents of soil-borne pathogens due to the secretion of antibiotics and lytic enzymes in the rhizosphere of plants. Therefore, they are potential agents to be combined with Trichoderma, especially when they do not inhibit each other [51, 52, 53, 54, 55]. However, the compatibility of combinations needs to be evaluated with in vitro and in planta assays [56].

Interactions between Trichoderma and mycorrhyzae are sometimes antagonistic, such as with the ectomycorrhyzal basidiomycetous genus Laccaria spp., where there was clear inhibition of growth, colonization, and spore germination on both partners [57, 58, 59]. However, sometimes these interactions are synergistic, such as with Glomus spp. Although there was an increase in plant biomass in the interaction, microscopical observations clearly showed that Trichoderma was parasitizing this endomycorrhyzal fungus [60]. Trichoderma can parasitize the hyphae of the endomycorrhyzal fungus Glomus irregulare and gain entry into potato roots [61]. On the other hand, endomycorrhyzal species of Rhizophaga use Trichoderma to penetrate into the roots of non-host Brassicaceae, resulting in increased plant productivity [62].

The compatibility and synergism in interactions between Trichoderma and other beneficial microorganisms is so specific that they vary according to the strain of each partner and the host plant. Therefore, determining the outcome of these interactions is crucial for the successful field applications.

Advertisement

6. Field trials and uses in agriculture

Biological control of plant diseases is a reality in the agricultural world, since the abuse and inappropriate use of chemicals have led to major problems to the environment and human health. In view of sustainable agriculture, the use of chemical molecules is becoming unfeasible due to their high cost and toxicity. The use of products based on Trichoderma proved to be effective, especially against root pathogens able to produce resistance structures such as sclerotia [63, 64, 65]. The application of these microorganisms aiming to manage different plant diseases can be performed on seeds before planting, via foliar spraying, in the substrate, in the planting furrow or even in organic matter that will be incorporated before transplanting seedlings [66]. The form of application of products formulated with these microorganisms depends on the target to be controlled, the host crop, the environmental conditions, and the manufacturer’s recommendations.

In Brazil, the control of white mold in soybeans is done by a combination of biological and chemical methods. This system will be used here as a case study to exemplify the application of Trichoderma in the field. White mold is the second most important soybean disease in Brazil and causes between 20 and 30% of losses on average, but under some conditions may reach 70–100% [26, 30, 67]. Approximately 10 million ha of soil is infested by this pathogen in Brazil out of total 35.9 million ha devoted to soybean cultivation in the country [67]. Approximately 5 million ha of soybean is currently treated with Trichoderma-based products in Brazil [67]. A common recommendation for white mold management is one spray application of Trichoderma at the vegetative stage V2 and another application at V4-V6 with concentrations varying from 109 to 1011 CFU/ha, depending on the commercial product adopted. Spray application of Trichoderma should be done on overcast days with high soil humidity and mild temperatures. Since the levels of resistance in commercial cultivars are not satisfactory, the combination of other practices is desirable. No-tillage planting with mulch produced by Urochloa ruziziensis (Syn. Brachiaria) is highly recommended as it stimulates the sexual germination of sclerotia and at the same time functions a barrier for the spread of ascospores produced in apothecia [67, 68]. This mulch will also provide conducive conditions for the colonization of sclerotia and apothecia by Trichoderma [68, 69]. Another practice that must be adopted is the application of fungicides at the reproductive stage R1 and another application 15 days later. The most commonly used fungicides are fluazinam, thiophanate-methyl, procymidone, carbendazim, and trifloxystrobin [26]. Monitoring is essential for fine-tuning these recommendations to specific locations and environmental conditions. Some farmers may adopt the biological seed treatment with Trichoderma on top of the standard chemical seed treatment, as an additional measure to control damping-off, which is caused by many soil-borne pathogens, including S. sclerotiorum.

To verify the efficacy of the biological treatments, some of the manufactures of Trichoderma provide Petri plates with culture medium to farmers. Sclerotia should be collected from soil at the end of the cycle of soybean, but before harvest and plated to determine the percentage of sclerotia colonized by Trichoderma. When the level of colonization of sclerotia in the plates is above 50%, the level of control is considered satisfactory. Although this level of control cannot be directly correlated with success, they serve to show that Trichoderma is present in the treated area at a relatively high rate.

Control of white mold is also dependent on the density of sclerotia in soil. Best results are obtained when the densities are 1–10 sclerotia/kg of soil [30]. Field experiments have shown that Trichoderma spp. as an exclusive control method is not sufficient to reduce the severity of white mold (Table 3). Fungicides normally have to be deployed to complement the activity of Trichoderma. However, in this experiment, where 1 year only was evaluated, two Trichoderma strains used alone were able to maintain the productivity at high levels even in the absence of fungicides. The use of Trichoderma in multiple years is expected to promote the build-up of inoculum in the soil and consequently decrease the levels of sclerotia to acceptable levels [70]. In the long run, the objectives are to maintain the inoculum in equilibrium and increase the plant growth and productivity.

TreatmentsAUDPCIncidence (%)Sclerotia (g)TGW (g)Yield (kg/ha)
Control909.4 B25.5 B6.6 A127.6 B1942.5 C
T. asperellum SF04 (V4/V6)685.0 B9.2 A2.4A147.2 A2890.0 A
T. harzianum IBLF006 (V4/V6)766.9 B10.8 A5.8 A136.4 B2523.3 B
T harzianum ESALQ-1306. (V4/V6)651.2 B9.8 A2.2 A145.8 A2897.5 A
Trichoderma sp. Tricho 656 (V4/V6)656.9 B12.2 A4.6 A144.5 A2452.5 B
ESALQ-1306 (V4/V6) + Tioph. methyl (R1/R2)532.5 A10.5 A2.5 A146.1 A2765.0 A
Thiophanate methyl (R1/R2)658.1 B3.4 A3.4 A143.3 A2945.0 A
FLuazinam (R1/R2)440.6 A1.9 A1.9 A151.5 A3015.0 A

Table 3.

Combination of Trichoderma and fungicides to control Sclerotinia stem rot in soybean.

The experiment was done in the field with four replicates per treatment. Trichoderma was applied at a concentration of 109 CFU/ha at the stages V4 and V6 and the fungicides at the stages R1 and R2. The area under the disease progress curve (AUDPC) was determined by integrating multiple measurements of disease severity; disease incidence was determined by measuring the percentage of infected plants per treatment; the number of sclerotia per ha was determined by separating them from seeds with sieves and weighing; TGW is the total grain weight and yield was determined by weighing. Means followed by different uppercase letters in the same columns are statistically different by the Scott-Knott test (p ≤ 0.05).

Advertisement

7. Conclusion

In Brazil, 34 Trichoderma-based products are currently registered and most of them are recommended to control soil-borne pathogens that produce sclerotia as resistance structures. Relatively few species of the genus Trichoderma were developed into commercial formulations, despite the high number of publications that have shown the potential of many other species. Trichoderma spp. are widely used in Brazil to control white mold in soybean and its use is expected to increase in the near future as only 50% of the infected area is currently treated with these biocontrol agents. Besides providing partial control of white mold, these fungi can also increase plant growth and productivity coupled with a reduction in the use of chemical fungicides.

Advertisement

Acknowledgments

JTS, EA, and FCJ acknowledge CNPq (National Council for Scientific and Technological Development) for his productivity scholarship.

Advertisement

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1. Smolinska U, Kowalska B. Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum. Journal of Plant Pathology. 2018;100:1-12. DOI: 10.1007/s42161-018-0023-0
  2. 2. Sá MNF, Lima JS, Jesus FN, Perez JO, Gava CAT. Effect of Bacillus sp. and Trichoderma sp. on mycelial growth of Sclerotium rolfsii. Acta Brasiliensis. 2019;3:79-81. DOI: 10.22571/2526-4338158
  3. 3. Liang X, Rollins JA. Mechanisms of broad host range necrotrophic pathogenesis in Sclerotinia sclerotiorum. Phytopathology. 2018;108:1128-1140. DOI: 10.1094/PHYTO-06-018-0197-RVW
  4. 4. McCaghey M, Willbur J, Smith DL, Kabbage M. The complexity of the Sclerotinia sclerotiorum pathosystem in soybean: Virulence factors, resistance mechanisms, and their exploitation to control Sclerotinia stem rot. Tropical Plant Pathology. 2019;44:12-22
  5. 5. Bosamia TC, Dodia SM, Mishra GP, Ahmad S, Joshi B, Thirumalaisamy PP, et al. Unraveling the mechanisms of resistance to Sclerotium rolfsii in peanut (Arachis hypogaea L.) using comparative RNA-Seq analysis of resistant and susceptible genotypes. PLoS One. 2021;15(8):e0236823. DOI: 10.1371/journal. pone.0236823
  6. 6. García VG, Onco MAP, Susan VR. Biology and systematics of the form genus Rhizoctonia. Spanish Journal of Agricultural Research. 2006;4(1):55-79
  7. 7. Atanasova L, Le Crom S, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, et al. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics. 2013;14:121. Available from: http://www.biomedcentral.com/1471-2164/14/121
  8. 8. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V. Comparative genome sequence analysis underscores myco- parasitism as the ancestral life style of Trichoderma. Genome Biology. 2021;12:1-15. DOI: 10.1186/gb-2011-12-4-r40
  9. 9. Mukherjee PK, Mendoza-Mendoza A, Zeilinger S, Horwitz BA. Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biology Reviews. 2022;39:15e33. DOI: 10.1016/j.fbr.2021.11.004
  10. 10. Abd-El-Moity TH. The use of Trichodema spp. to control soilborne plant pathogens in Egypt. In: Biological Control of Plant Diseases. Boston, MA: Springer; 1992. pp. 255-258
  11. 11. Ararsa L, Thangavel S. Evaluation of arbuscular mycorrhizal fungi and Trichodema species for the control of onion white rot (Sclerotium cepivorum Berk). Journal of Plant Pathology & Microbiology. 2013;4:1000159. DOI: 10.4172/2157-7471.1000159
  12. 12. Hussain WA, Elzaawely AA, Sheery NI, Ismail AA, El-Zahaby HM. Biological control of onion white rot disease caused by Sclerotium cepivorum. Environment, Biodiversity & Soil Security. 2017;1:101-107. DOI: 10.21608/jenvbs.2017.1547.1008
  13. 13. Chaverri P, Samuels GJ. Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution. 2013;67-10:2823-2837. DOI: 10.1111/evo.12169
  14. 14. Cai F, Druzhinina IS. In honor of John Bissett: Authoritative guidelines on molecular identification of Trichoderma. Fungal Diversity. 2021;107:1-69
  15. 15. Smith ME, Henkel TW, Rollins JA. How many fungi make sclerotia? Fungal Ecology. 2014;13:211-220. DOI: 10.1016/j.funeco.2014.08.010
  16. 16. Chet I, Henis Y. Sclerotial morphogenesis in fungi. Annual Review of Phytopathology. 1975;13:169-192
  17. 17. Willetts HJ. Survival of fungal sclerotia under adverse environmental conditions. Biological Reviews of the Cambridge Philosophical Society. 1971;46:387-407
  18. 18. Macfarlane TD, Kuo J, Hilton RN. Structure of the giant sclerotium of Polyporus mylittae. Transactions of the British Mycological Society. 1978;71:359-365
  19. 19. Horn BW, Sorensen RB, Lamb MC, Sobolev VS, Olarte RA, Worthington CJ, et al. Sexual reproduction in Aspergillus flavus sclerotia naturally produced in corn. Phytopathology. 2014;104:75-85. DOI: 10.1094/PHYTO-05-13-0129-R
  20. 20. IBGE. Instituto Brasileiro de Geografia de Estatística. Produção Agrícola Municipal–PAM [Internet]. 2020. Available from: https://www.ibge.gov.br/estatisticas/economicas/agricultura-e-pecuaria/9117-producao-agricola-municipal-culturastemporarias- e-permanentes.html?=&t=resultados. [Accessed: February 20, 2022]
  21. 21. CONAB. Companhia Nacional de Abastecimento. Alho – Altos Preços, mas Clima Preocupa a Próxima Safra no Sul [Internet]. 2020. Available from: https://www.conab.gov.br/indicadores-da-agropecuaria/item/download/31689_569f5735ff790f58650ce6f2526323e4. [Accessed: February 20, 2022]
  22. 22. Index Fungorum [Internet]. 2021. Available from: http://www.indexfungorum.org/names/names.asp. [Accessed: February 20, 2022]
  23. 23. Domingos LB, Bontempo A, Lopes EA. Podridão-branca do alho e da cebola. In: Avanços Tecnológicos Aplicados à Pesquisa na Produção Vegetal. Universidade Federal de Viçosa [Internet]. 2015. Available from: https://www.researchgate.net/profile/Everaldo_Lopes/publication/283568389_Podridao-branca_do_alho_e_da_cebola/links/563f6ec008aec6f17ddb7ea5.pdf. [Accessed: February 20, 2022]
  24. 24. Coley-Smith JR. White rot disease of allium: Problems of soil-borne diseases in microcosm. Plant Pathology. 1990;39:214-222
  25. 25. Fuga CAG, Lopes EA, Vieira BS. Etiologia, epidemiologia e controle de doenças causadas por Sclerotium rolfsii e S. cepivorum. Revisão Anual de Patologia de Plantas. 2012;20:278-322
  26. 26. Meyer MC, Campos HD, Godoy CV, Utiamada CM, Sato LN, Dias AR, et al. Eficiência de fungicidas para controle de mofo-branco (Sclerotinia sclerotiorum) em soja, na safra 2019/2020: resultados sumarizados dos experimentos cooperativos. Londrina: Embrapa; 2020. p. 10
  27. 27. Adnan M, Islam W, Shabbir A, Khan KA, Ghramh HA, Huang Z, et al. Plant defense against fungal pathogens by antagonistic fungi with Trichoderma in focus. Microbial Pathogenesis. 2019;129:7-18. DOI: 10.1016/j.micpath.2019.01.042
  28. 28. Khan RA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp against phytopathogenic fungi. MDPI Microorganisms. 2020;8:817. DOI: 10.3390/microorganisms8060817
  29. 29. Zhang F, Ge H, Zhang F, Guo N, Wang Y, Chen L, et al. Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean. Plant Physiology and Biochemistry. 2016;100:64-74. DOI: 10.1016/j.plaphy.2015.12.017
  30. 30. Juliatti FC, Rezende AA, Juliatti BC, Morais TP. Trichoderma as a biocontrol agent against Sclerotinia stem rot or white mold on soybeans in Brazil: Usage and technology. In: Shar MM, editor. Trichoderma: The Most Widely Used Fungicide. London, UK: IntechOpen; 2019. pp. 1-23. DOI: 10.5772/intechopen.84544
  31. 31. Troian RF, Steindorff AS, Ramada MHS, Arruda W, Cirano JU. Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: Evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnology Letters. 2014;36:2095-2101. DOI: 10.1007/s10529-014-1583-5
  32. 32. Abdullah MT, Ali NY, Suleman P. Biological control of Sclerotinia sclerotiorum (Lib.) de Bary with Trichoderma harzianum and Bacillus amyloliquefaciens. Crop Protection. 2008;27:1354-1359. DOI: 10.1016/j.cropro.2008.05.007
  33. 33. Silva FF, Castro EM, Moreira SI, Ferreira TC, Lima AE. Alves. Emergência e análise ultraestrutural de plântulas de soja inoculadas com Sclerotinia sclerotiorum sob efeito da aplicação de Trichoderma harzianum. Summa Phytopathologica. 2017;43:41-45. DOI: 10.1590/0100-5405/2212
  34. 34. Marcello CM. Avaliação da expressão e caracterização de uma exo-β-1,3-glucanase envolvida no mecanismo de micoparasitismo de Trichoderma asperellum [thesis]. Brasília: Universidade de Brasília; 2008
  35. 35. Souza ACA, Sousa TP, Cortês MVB, Rodrigues FA, Silva GB, et al. Enzyme induced defense response in the suppression of rice leaf blast (Magnaporthe oryzae) by silicon fertilization and bioagents. International Journal of Research Studies in Bioscience. 2015;3:22-32
  36. 36. Bozzola JJ, Russell LD. Electron Microscopy. Boston: Jones and Bartlett Publishers; 1999. p. 670
  37. 37. Alves E, Lucas GC, Pozza EA, Carvalho Alves M. Scanning electron microscopy for fungal sample examination. In: Laboratory Protocols in Fungal Biology. New York: Springer; 2013. pp. 133-150
  38. 38. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, et al. Trichoderma: The genomics of opportunistic success. Nature Review Microbiology. 2011;9:749-759. DOI: 10.1038/nrmicro2637
  39. 39. Bettiol W, Morandi MAB, Pinto ZV, Paula Junior TJ, Correa EB, Lucon CMM, et al, editors. Produtos Comerciais à Base de Agentes de Biocontrole de Doenças de Plantas. Jaguariúna: Embrapa Meio Ambiente; 2012. p. 155
  40. 40. Dias PP. Controle biológico de fitopatógenos de solo por meio de isolados de fungos do gênero Trichoderma e sua contribuição no crescimento de plantas. 101 f. [thesis]. Seropédica: Universidade Federal Rural do Rio de Janeiro; 2011
  41. 41. Amorim L, JAM R, Bergamin Filho A, editors. Manual de Fitopatologia vol. I–Princípios e Conceitos. 5th ed. Ouro Fino: Agronômica Ceres; 2018. p. 810
  42. 42. Carvalho Filho MR. Relações filogenéticas, identificação e potencial de uso de isolados de Trichoderma no controle do mofo branco e como promotores de crescimento do feijoeiro [thesis]. Brasília: Universidade de Brasília; 2013
  43. 43. Souza JR. Potencialidade de fungicida e agente biológico no controle de requeima do tomateiro [dissertation]. Vitória da Conquista: Universidade Estadual do Sudoeste da Bahia; 2013
  44. 44. Melo IS. Potencialidades da utilização de Trichoderma spp. no controle biológico de doenças de plantas. In: Bettiol W, editor. Controle biológico de doenças de plantas. Jaguariúna: CNPDA/EMBRAPA; 1991. pp. 135-156
  45. 45. Harman GE. The nature and application of biocontrol microbes II: Trichoderma spp. - Overview of mechanisms and uses of Trichoderma spp. Phytopathology. 2005;96:190-194. DOI: 10.1094/PHYTO-96-0190
  46. 46. Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, et al. Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal. 2014;8:271-126
  47. 47. MAPA. Ministério da Agricultura Pecuária e Abastecimento. Agrofit–Sistemas de Agrotóxicos Fitossanitários, Coordenação Geral de Agrotóxicos e Afins [Internet]. 2021. Available from: http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. [Accessed: February 19, 2022]
  48. 48. Lucon CMM, Chaves ALR, Bacilieri S, editors. Trichoderma: o que é, para que serve e como usar corretamente na lavoura. São Paulo: Instituto Biológico; 2014. p. 28
  49. 49. Elshahawy IE, Saied N, Abd-El-Kareem F, Morsy A. Biocontrol of onion white rot by application of Trichoderma species formulated on wheat bran powder. Archives of Phytopathology and Plant Protection. 2017;50(3-4):150-166. DOI: 10.1080/03235408.2016.1276423
  50. 50. Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ. Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia. 2015;107(3):558-590. DOI: 10.3852/14-147
  51. 51. Barbosa LO, Lima JS, Magalhaes VC, Gava CAT, Soares ACF, Marbach PAS, et al. Compatibility and combination of selected bacterial antagonists in the biocontrol of sisal bole rot disease. BioControl. 2018;63(4):595-605. DOI: 10.1007/s10526-018-9872-x
  52. 52. Mishra J, Arora NK. Secondary metabolites of fluorescent pseudomonads in biocontrol of phytopathogens for sustainable agriculture. Applied Soil Ecology. 2017;125:35-45. DOI: 10.1016/j.apsoil.2017.12.004
  53. 53. Pawana G, Badami K, Djunaedy A. Growth and reproduction of Trichoderma sp. in with presence Bacillus sp. or fluorescent pseudomonad. Journal of Physics: Conference Series. 2021;1899:1-7. DOI: 10.1088/1742-6596/1899/1/012021
  54. 54. Pan S, Jash S. Variability in biocontrol potential and microbial interaction of Trichoderma spp. with soil inhabiting antagonistic bacteria Pseudomonas fluorescens. Indian Phytopathology. 2010;63:158-164
  55. 55. Braga AF. Interaction of Trichoderma Asperellum and Biological Control of Bacillus spp. Used in Soybean Diseases [Dissertation]. Instituto Federal Goiano: Rio Verde; 2021
  56. 56. Cruz-Magalhães V, Guimarães RA, Silva JCP, Faria AF, Pedroso MP, Campos VP, et al. The combination of two Bacillus strains suppresses Meloidogyne incognita and fungal pathogens, but does not enhance plant growth. Pest Managment Science. 2021;78(2):722-732. DOI: 10.1002/ps.6685
  57. 57. Summerbell RC. The inhibitory effect of Trichoderma species and other soil microfungi on formation of mycorrhiza by Laccaria bicolor in vitro. New Phytology. 1987;105:437e448. DOI: 10.1111/j.1469-8137.1987.tb00881.x
  58. 58. Werner A, Zadworny M, Idzikowska K. Interaction between Laccaria laccata and Trichoderma virens in co-culture and in the rhizosphere of Pinus sylvestris grown in vitro. Mycorrhiza. 2002;12:139e145. DOI: 10.1007/s00572-002-0159-8
  59. 59. Guo Y, Ghirardo A, Weber B. Trichoderma species differ in their volatile profiles and in antagonism toward ectomycorrhiza Laccaria bicolor. Frontiers in Microbiology. 2019;10:891. DOI: 10.3389/fmicb.2019.00891
  60. 60. Rousseau A, Benhamou N, Chet I, Piche Y. Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology. 1996;86:434e443. DOI: 10.1094/Phyto-86-434
  61. 61. De Jaeger N, Declerck S, De La Providencia IE. Mycoparasitism of arbuscular mycorrhizal fungi: A pathway for the entry of saprotrophic fungi into roots. FEMS Microbiology Ecology. 2010;73:312e322. DOI: 10.1111/j.1574-6941.2010.00903.x
  62. 62. Poveda J, Hermosa R, Monte E, Nicolas C. Trichoderma harzianum favors the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Scientific Reports. 2019;9:1-11. DOI: 10.1038/s41598-019-48269-z
  63. 63. Souza ACA, Filippi MCC, Nascente AS, Prabhu AS, Alves E. Silicon rates and beneficial microorganism on blast suppression and productivity of upland rice. Journal of Plant Science and Phytopathology. 2021;5:20-27. DOI: 10.29328/journal.jpsp.1001057
  64. 64. Caixeta GJ, Nascimento LM, Filippi MCC, Gonçalves FJ, Souza ACA. Use of bioagents in the suppression of Macrophomina phaseolina in the common bean culture. Ipê Agronomic Journal. 2021;5:1-11
  65. 65. Silva NP, Filippi MCC, Gonçalves FJ, Souza ACA. Biocontrol of Macrophomina phaseolina and promoting growth in sunflower culture with the use of Trichoderma sp. and Rhyzobacteria. Ipê Agronomic Journal. 2021;1:1-14
  66. 66. Moscoso MAP, Ramírez IJN, Angarita CC, Rojas ET. In vitro biocontrol activity of macrohongs against different phytopathogenic fungi. Acta Biológica Colombiana. 2020, 2020;25:265-279. DOI: 10.15446/abc.v25n2.75303
  67. 67. Meyer MC, Campos HD, Godoy CV, Utiamada CM. Ensaios cooperativos de controle biológico de mofo branco na cultura da soja—safras 2012 a 2015. Londrina: Embrapa Soja; 2016. p. 49
  68. 68. Görgen CA, Civardi E, Perreto E, Carneiro LC, Silveira Neto AN, Ragagnin V, et al. Controle de Sclerotinia sclerotiorum com o manejo de Brachiaria ruziziensis e aplicação de Trichoderma harzianum. Circular Técnica 81: Embrapa; 2008. p. 4
  69. 69. Silva JC, Meyer MC, Mazaro SM. Trichoderma: uso na agricultura. Brasília, DF: Embrapa; 2019. p. 536
  70. 70. Jaccoud Filho DS, Henneberg L, Grabicoski EMG, editors. Mofo branco. Ponta Grossa: Todapalavra; 2017. p. 520

Written By

Jéssica Rembinski, Silvino I. Moreira, Jorge T. De Souza, Alan C.A. Souza, Adriano F. Dorigan, Eduardo Alves, Breno C.M. Juliatti and Fernando C. Julliati

Submitted: 21 December 2021 Reviewed: 03 January 2022 Published: 31 August 2022

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.0 License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Continue reading from the same book

View All
Chapter 1 Introductory Chapter: Trichoderma the Versatile Fu...

By Fernando Cezar Juliatti and David de Souza Jaccoud...

115 downloads

Chapter 2 Trichoderma: A Biofertilizer and a Bio-Fungicide f...

By Bongani Petros Kubheka and Luwam Weldegabir Ziena

1467 downloads

Chapter 3 Trchoderma Spp.: Their Impact in Crops Diseases Ma...

By Amar Bahadur and Pranab Dutta

357 downloads