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Review

The Genus Clonostachys (Bionectria) as a Potential Tool Against Agricultural Pest and Other Biotechnological Applications: A Review

by
Manuela Reyes-Estebanez
1,* and
Pedro Mendoza-de Gives
2,*
1
Center of Environmental Microbiology and Biotechnology, Autonomous University of Campeche, Calle Agustín Melgar s/n entre Juan de la Barrera y Calle 20, Campeche 24039, Mexico
2
Laboratory of Helminthology, National Center for Disciplinary Research in Animal Health and Innocuity (INIFAP-Mexico), Boulevard Paseo Cuauhnahuac No. 8534, Progreso 62550, Mexico
*
Authors to whom correspondence should be addressed.
Microbiol. Res. 2025, 16(4), 86; https://doi.org/10.3390/microbiolres16040086
Submission received: 19 February 2025 / Revised: 6 April 2025 / Accepted: 16 April 2025 / Published: 19 April 2025
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Abstract

:
The Clonostachys genus is a saprophytic soil microfungus (Ascomycota). It exhibits significant ecological adaptability and plays a crucial role in maintaining the balance of soil microorganisms. Species within this genus are natural antagonists of insects and nematodes, and they also combat phytopathogenic fungi through mycoparasitism. This process involves producing lytic enzymes and competing for space and nutrients. Clonostachys species are effective biocontrol agents in agriculture and have been utilized to manage pests affecting many high-value commercial crops, acting as a natural biopesticide. They inhabit plant tissues, boosting plant defenses and activating genes for water and nutrient uptake, enhancing plant performance. Additionally, they produce enzymes and bioactive metabolites with antimicrobial, antifungal, nematocidal, anticancer, and antioxidant properties. Clonostachys species can degrade plastic waste and remove hydrocarbons from crude oil-contaminated sites when functioning as endophytes, positioning Clonostachys as a promising candidate for reducing environmental pollution. There are still challenges and limitations, such as the continuous surveillance of the safety of Clonostachys species on plants, the establishment of commercial applications, formulation viability, and variability due to field conditions. These issues will have to be addressed. This review provides an overview of Clonostachys ecology, morphology, classification, and biotechnological applications, emphasizing its significance in various fields.

1. Introduction

Pest-affecting crops implicate important economic losses all over the world. It is estimated that 40% of the world’s crop production (USD 220 billion) is lost due to agricultural pests [1].
The primary threats to economically important crops include a variety of soil-borne plant pathogens (bacteria, fungi, viruses, and Oomycetes), harmful organisms (nematodes, phytoplasmas, and protozoa), parasitic plants [2], and herbivorous (phytophagous) insects that feed on plant tissues [3,4] (Figure 1).
Traditionally, the control of these pests is managed through the systematic use of chemically synthesized pesticides [5]. This method helps to reduce the symptoms occasioned by phytopathogenic organisms and promotes an important improvement in the health and productivity of crops [6]. However, there are some worrying disadvantages in this control method that lead to increasing restrictions on the use of these compounds [7].
Below, we address, in a general way, the main problems caused by using chemical pesticides in different areas.

1.1. Public Health Risks of Using Chemical Pesticides

The use of chemical pesticides can pose potential risks to human health. These risks can arise from direct exposure to the chemicals, such as for farmers and applicators, or from consuming food [8,9,10] or drinking water that contain pesticide residues [11]. Additionally, inhalation of airborne contaminants can also lead to exposure. The toxic effects of these pesticides on public health depend on both the dose and frequency of exposure [12], and they can have cumulative effects on the body [13,14,15]. Pesticide contamination can lead to dysbiosis, which is associated with chronic degenerative disorders such as obesity and diabetes [16]. It can also cause various health issues, including pulmonary, fertility, circulatory, neuronal, hormonal, and endocrine dysfunctions [17] as well as cancer, kidney, and liver dysfunctions, among others [18,19].
The control of household pests, such as cockroaches, mosquitoes, flies, and mites, is an important social issue. These pests not only cause discomfort but are also known carriers of various diseases [20,21,22]. Managing these pests typically requires the continuous use of home pesticides, leading to ongoing exposure to these chemicals. Regular applications of pesticides can expose both the individuals applying the products and all residents of the area to potentially harmful substances. This exposure can occur through direct contact or by inhaling toxic pesticide residues lingering in the air [23]. Continuous exposure to low doses of these pesticides is a significant risk factor that could lead to serious health issues, such as childhood leukemia [24].

1.2. Environmental Risks of Using Chemical Pesticides

The release of chemical pesticides into the environment presents significant risks of environmental damage. Of the total amount of pesticide applied to target pests, whether in agriculture or homes, only a small percentage reaches the intended organisms. The majority of pesticides become pollutants, posing a latent threat to humans, animals, and beneficial microorganisms [25]. Pesticide residues can impact a wide range of organisms, including mammals, birds, reptiles, amphibians, fish, insects, and other invertebrates, as well as plants and fungi [26,27,28]. One of the most concerning consequences of using pesticides is the contamination of soil and water bodies. This contamination negatively affects microorganisms in both terrestrial and aquatic ecosystems, including those that comprise their microbiomes [29]. Moreover, the loss of microbial biodiversity due to the toxic effects of pesticide residues leads to soil degradation and a decline in fertility, which can result in soil erosion with ecologically devastating consequences [30]. The effect of harmful chemical residues from pesticides in the environment, in many cases, produces a lethal effect not only on the target organisms but also on non-target organisms [31]. The consequences of this effect occasion the loss of diversity and put under risk the sustainability of the environment and global stability [32].

1.3. Effects of Pesticides on Pollinating Organisms

One significant concern with the use of chemical pesticides, especially in controlling agricultural pests, is their harmful collateral effect on non-target organisms, including essential pollinators such as bats, beetles, ants, insects, birds, and bees. These organisms are crucial for transferring pollen between plants, enabling fertilization and reproduction [33]. Pollinators establish a mutualistic relationship with plants, providing vital ecological functions that support global biodiversity [34].
Wild bees, in particular, play an important role in pollination, enhancing both the production and quality of commercially valuable crops like apples, pears, rapeseed, various berries, and cucumbers [35]. However, the use of pesticides poses a significant threat to pollinator populations and jeopardizes the ecosystem services these beneficial organisms provide [36,37].
Pollinating organisms are highly vulnerable to the harmful effects of pesticides. They can be exposed through direct contact with sprayed surfaces or by ingesting contaminated pollen and nectar. Depending on the dosage, this exposure can lead to neurophysiological and immune system disorders, resulting in disorientation, paralysis, and even death, particularly in honeybees [38]. Furthermore, the toxicity of pesticide residues in honeybees can also contaminate bee products, which may adversely affect the nervous and digestive systems of human consumers [39].

1.4. Pesticide Resistance in Plague Organisms

The improper use of agrochemical pesticides leads to a rapid loss of their effectiveness against pest organisms due to the development of pesticide resistance. This resistance can result from several factors, such as the overuse and misuse of pesticides [40] as well as genetic and adaptive processes. Changes in the pest genome, including mutations in genes associated with detoxification, have also been linked to pesticide resistance [41]. These genetic modifications enable pests to develop mechanisms to counteract the harmful effects of pesticides [42]. Pests may employ various survival strategies to withstand exposure to chemical pesticides, including behavioral, biochemical, physiological, genetic, and metabolic adaptations [43]. As a consequence, these strategies often result in the overexpression of detoxifying enzymes in insects, enhancing their resistance to pesticides. One notable example of an insect that has developed resistance is the diamondback moth (Plutella xylostella Linnaeus, 1758), which has shown resistance to pyrethroids, organophosphates, and other pesticide classes [44]. The white fly (Bemisia tabaci Gennadius, 1889) has recently been reported to exhibit resistance to various pesticides, including pyrethroids, organophosphates, neonicotinoids, and biogenic insecticides [45]. Beyond the emergence of pesticide resistance in agricultural pests, this issue has also extended to pathogens of public health significance, such as Candida auris Saton & Makimura 2009, which has been found to be resistant to fluconazole [46]. Furthermore, the potential contamination of fruits, legumes, and various crops treated with pesticides raises serious public health concerns [47]. The negative implications of chemical pesticide use have prompted researchers around the world to seek alternatives for pest control that do not involve chemically synthesized compounds. Some examples of pathogens affecting crops that have developed resistance to pesticides are shown in Table 1.

1.5. Side Effects on the Environment

Side Effects and Public Health Risks of Using Chemical Pesticides

The use of chemical pesticides can affect soil-beneficial microorganisms, particularly when using high doses of chemicals. High doses of pesticides can trigger an important diminishing of soil microbiota that can lead to diminishing the fertility of agricultural areas, becoming a worrying problem of environmental deterioration [57]. Beyond this, the use of chemical pesticides can provoke the presence of contaminant residues in grains, fruits, and vegetables for human consumption. These contaminants lead to the development of lethal diseases, i.e., cancer, kidney diseases, diabetes, liver dysfunction, eczema, neurological destruction, cardiovascular diseases, and other mortal diseases becoming a worrying problem of public health [58,59]. In this context, it is necessary to explore other control strategies different than the use of chemically synthesized compounds.

1.6. Sustainable Alternative Methods of Control of Plague of Importance in Agriculture

Some alternative methods of control of agricultural pests have been proposed to diminish the symptoms occasioned by pests and enhance crop production. Some examples of such alternatives are crop rotation, planting resistant crop varieties, fallowing, soil amendment, plants with nematocidal activity, and biological control [60,61,62]. During recent decades, the use of natural antagonists of pests has been explored, and there is a group of microorganisms that have established biological associations, i.e., parasitism or predation that include bacteria against nematodes and/or insects, i.e., Pasteuria penetrans (Thorne) Sayre y Starr [63,64] and Bacillus thuringiensis Berliner, 1915 [65,66]; predatory nematodes, i.e., Butlerius butleri Goodey, 1929 [67]; entomopathogenic nematodes, i.e., Heterorhabditis sp. and Steinernema [68,69]; nematophagous mites; i.e., Lasioseius penniciliger Barlese, 1916 [70]; and nematophagous fungi, i.e., Arthrobotrys oligospora Fresen. 1950 [71], Duddingtonia flagrans (Dudd.) R.C. Cooke 1969 [34], and Clonostachys spp. [72].

Clonostachys spp. as an Alternative to the Use of Chemically Synthesized Pesticides

One of the soil saprophytic filamentous fungi that possesses a wide range of biotechnological applications is the genus Clonostachys [73,74]. This genus was first discovered by Corda, 1839 [75]. Species of this genus have motivated researchers in many countries to investigate its extraordinary adaptation to different environments [73,74] where they play an important ecological role as a natural control agent of individuals of different populations [76,77]. The Clonostachys species form part of the natural biota, and it is possible to isolate these fungi from different substrates in nature including soil, plant roots, leaves, and flowers [78,79,80]. Additionally, these fungi can also be isolated from other sources, such as the corpses of infected nematodes and insects.

1.7. Genus Clonostachys

1.7.1. General Aspects

The Clonostachys species are nematophagous and entomopathogenic fungi that are saprophytic organisms of soil and groups of more than a hundred species [81] morphologically typified with asexual reproduction, and they include the following recorded species (Figure 2 and Figure 3):
Most of these species have been identified as playing an important role in nature as plant decomposers, endophytes, and natural antagonists of different organisms, including insects [82,83], nematodes [84,85], and other fungi such as Alternaria alternata (Fr.) Keissl. (1912), Fusarium spp. [86], Rhizoctonia solani J.G. Kühn 1858 [87], and Clonostachys genus, belonging to the family Bionectriaceae.
Clonostachys are parasitic fungi that employ multiple mechanisms to attack and invade their hosts. It forms infective hyphae and produces enzymes that degrade cell walls, enabling the fungi to penetrate and destroy vulnerable organisms. Additionally, it generates antibiotics that inhibit the growth of pathogens [88]. Furthermore, compounds produced through its secondary metabolism demonstrate lethal effects against these hosts [88].
Members of this family are distinct from other genera mainly in their shape and septation of the ascospores and lifestyle [89,90].
The genus Clonostachys belongs to the family Bionectriaceae, and members of this family are characterized by their distinct shapes, the septation of their ascospores, and their lifestyles. Recent studies suggest that the sexual morphs of Clonostachys species should be reclassified under the genus Bionectria.
A list of some species belonging to the Clonostachys genus and their isolation source in different countries worldwide are shown in Table 2.

1.7.2. General Morphological Aspects of Clonostachys Genus

Members of the Bionectriaceae family are characterized by the form and septation of their ascospores, morphology of their ascas, lifestyle, and particularly in their character as anamorphous [99,100]. This genus is characterized by the formation of sporodochia with single or penicilate conidiophores. Conidiophores can be found with two to four verticillate and can be mono- or dimorphic with intercalary hyaline fialides. Fialides can be divergent, smooth, or slightly rough. They can also appear flask-shaped or cylindrical. Conidia can form slimy conidia mass. Conidia can be hyaline smooth, being from globose or subglobose to ellipsoidal, and can form chains [99]. Its teleomorph is the genus Bionectria (Bionectriaceae: Hypocreales), which was described by Spegazzini (1919) [100]. This is an ascomycete that presents a well-developed stroma with grouped perithecia that can be from globose to subglobose shape of yellow to orange color, smooth to verrucose, with octosporic, clavate, hyaline ascas with an apical ring, ascospores from ellipsoidal to fusiform, hyaline with a transversal septum in the medial part [87].
Some of the main general morphological characteristics of Clonostachys genus are shown in Figure 4.
One of the most widely studied species of Clonostachys genus is C. rosea. This species has been found widespread in many kinds of habitats around the world, mainly in soil. This species has developed an important ability to act as a natural enemy against numerous fungal plant pathogens, nematodes, and insects. This wide predator/parasitic behavior is based on activating multiple mechanisms such as secreted cell wall-degrading enzymes, the production of antifungal secondary metabolites, and the induction of plant defense systems [72]. Besides having significant biocontrol activity, C. rosea has also shown several important activities and biotechnological uses.

1.8. Uses and Other Applications of Clonostachys Species

Clonostachys species have shown to possess several potential biotechnological activities, particularly in the control of parasites of importance in agriculture [85,100] and livestock, as mentioned above [83]. Likewise, C. pityrodes living as an endophyte stimulates the growth and flavonoid production in tartary buckwheat sprout cultures [101]. Such capability to act as a promoter of growth plants has been attributed to the activation of genes associated with the production of bioactive enzymes [102], the absorption of water and nutrients, or activating plant self-defense mechanisms against pests [103]. Clonostachys sp. has also been discovered to have an important capability to degrade plastics [104]. Furthermore, an isolate of Clonostachys sp., along with other endophytic fungi inhabiting the stem and leaf tissues of plants, demonstrated a remarkable capacity to remove hydrocarbons from a crude oil-contaminated site in natural springs in Las Minas, Ecuador [105].
Some of the main identified biological activities and potential uses of species of Clonostachys are shown in Figure 5.

1.9. Clonostachys as a Biological Control Agent of Pests of Importance in Agriculture

Clonostachys species possess a long list of biological antagonistic properties against several pests of importance in the agriculture and livestock industries. Such properties provide these fungi with enormous biological flexibility to be used as a potential biological control agent. In the case of pests affecting economically important crops, such as tomato, cucumber, okra, chilly, and many other legumes and crops, several pests including insects, nematodes, and phytopathogenic fungi occasion enormous economic losses [58]. The strategy most commonly used against phytopathogenic pests is based on the frequent use of chemical pesticides that help to reduce, at certain levels, the populations of plague microorganisms. These compounds have triggered some disadvantages in their use, for example, the development of genetic resistance in insects to many chemical pesticides [106].

1.9.1. Entomopathogenic Activity

Clonostachys species have demonstrated an important activity against plague insects, and it has been considered a good prospect to be used as a potential biological control agent for several entomopathogenic microorganisms affecting commercially important crops [3,107,108]. Clonostachys species have demonstrated an important activity against plague insects, and it has been considered a good prospect to be used as a potential biological control agent for several entomopathogenic microorganisms [109]. Entomopathogenic fungi operate through various strategies. They first produce cuticle-degrading proteases, which help them penetrate the outer integument of the insect’s body. Once inside, the fungi use infective hyphae to invade further and absorb the insect’s body fluids through secondary hyphae. Additionally, Clonostachys possesses an enormous capability to produce several compounds derived from its secondary metabolism with a wide range of biological activities with pharmaceutical and agrochemical applications [110]. An isolate of Clonostachys solanum from Slovenia occasioned 56.27% pupae mortality of the cabbage root fly (Delia radicum L. 1758) [109]. Likewise, a suspension containing 4 × 107 spores of an Algerian isolate of Clonostachys sp. was sprayed on tomato crops (Lycopersicum solanum L. 1753) infected with the leaf miner lepidopteran Tuta absoluta, and 100% reduction in the pest population was achieved (72 h post-treatment) [111].
Additionally, a list of C. rosea isolates, their blank insect affecting different crops, and the different experimental conditions and efficacies are shown in Table 3.

1.9.2. Mycoparasitic Activity

Another important biological activity shown by Clonostachys spp. is their potent fungicidal activity, mainly acting as hyperparasitic fungi of phytopathogenic fungi. This property makes these fungi a potential biocontrol agent of different fungi affecting important crops either pre- or post-harvest [114] and even inducing resistance-related proteins in tomato fruits against gray mold disease. Clonostachys genus uses different strategies to attack, kill, and degrade phytopathogenic fungi that include competition for space and nutrients and mycoparasitism. This process involves production of fungal wall-degrading proteases followed by fungal infection through invasive hyphae and the collapse of the surface mycelium of the fungal prey. Additionally, antibiosis by secretion of antifungal compounds, tolerance towards antifungal compounds, and induction of plant disease resistance, among others contribute to plant protection [110]. Recent proteomics and genomics studies have revealed that genes encoding predicted secreted proteins are upregulated in the infection process of Clonostachys on phytopathogenic fungi, i.e., Fusarium graminearum Schwabe 1839 and Helminthosporium solani Durieu & Mont. 1849 [115].
Several key biological functions of Clonostachys species in combating phytopathogenic fungi are linked to various genes. These include ATP-binding cassette (ABC) transporters, polyketide synthases, cytochrome mono-oxygenases, pectin lyases, glucose-methanol-choline oxidoreductases, and lytic polysaccharide mono-oxygenases [116]. Additionally, genes that encode cell wall-degrading enzymes, major facilitator superfamily sugar transporters, anion/cation symporters, and pathways for utilizing alternative carbon sources have been documented [117]. Furthermore, differentially expressed genes (DEGs)—including those that encode ABC transporters, glucanases, and chitinases—have also been reported [118].
In Table 4, some examples of predatory/parasitic activity of species of Clonostachys against fungi affecting different crops are shown.

1.9.3. Nematocidal Activity

Similarly, Clonostachys spp. infect nematodes that affect important crops such as tomatoes. In a recent study, an important M. incognita egg infection rate (higher than 68%) by C. rosea at 6 × 107 conidia/mL was recorded, and more than 65% of juveniles died after 96 h incubation with a fungal spore suspension in potato dextrose broth (PDB) compared to a control. The authors attributed this activity to the production of several biomolecules produced by these fungi [122]. In a study conducted under greenhouse conditions, a C. rosea isolate showed a significant reduction in the number of tomato root galling compared to an untreated group [123]. On the other hand, C. rosea fungal organic extracts reduced the number of galls, eggs, and females of M. incognita in tomato plants, and an improvement in the agronomic characteristics was observed [124]. One of the mechanisms used by C. rosea to penetrate and invade the nematode tissues is associated with a subtilisin-like protease (prC) that acts to degrade the nematode cuticle coat [125]. In a recent study conducted under in vitro conditions, a high nematocidal activity of liquid culture filtrates of C. rosea against juveniles and eggs of M. incognita was recorded, and several secondary metabolites including stearic acid, tetradecanoic acid, dodecanoic acid, and 1-heptadecanol were identified as the responsible for this activity [126].
Some additional reports about the nematocidal activity of Clonostachys against different taxonomic nematodes affecting crops of important commercial values are shown in Table 5.

1.9.4. Clonostachys as a Biological Control Agent of Pests of Importance in the Livestock Industry

There are only a few reports about the nematocidal activity of Clonostachys species against nematodes of importance for the livestock industry. In an experiment, two nematophagous fungi, C. rosea and D. flagrans, were assessed to determine their potential use to reduce the populations of H. contortus infective larvae, one of the most pathogenic parasitic nematodes of ruminants, using microplots with grass maintained under field conditions. Microplots with graminaceous forage plants were infected with an aqueous suspension containing H. contortus infective larvae; after infection, microplots were inoculated with an aqueous suspension containing these fungi at doses of 5 × 106 spores/chlamydospores. After twelve days, larvae were recovered from microplates and a control group without fungi. The results showed larval reductions of 91.5% for D. flagrans and 88.9% for C. rosea after 7 days of interaction [65]. In another study, the in vitro lethal activity of C. rosea against nematodes of different taxa, including H. contortus and free-living nematodes of different species, was assessed; its results showed that the fungi exerted a high nematocidal activity against all nematodes and specifically showed 87.7% lethal activity against H. contortus [83]. In an extensive review of the available literature, the present study’s authors only found one record of an in vivo assay, using C rosea chlamydospores in the control of sheep nematodiasis. In this study, Merino sheep artificially infected with H. contortus received a diet containing a powder at three different doses: 0.25, 0.5, and 1 g of C. rosea chlamydospores per kg of BW. The highest larval reductions in feces were 33, 72, and 89%, respectively [128]. This study opens new perspectives on using C. rosea as a potential biological control agent against sheep nematodiasis, although more studies are necessary to confirm this statement.

1.10. Other Biotechnological Applications of Species of Clonostachys Genus

1.10.1. Endophytic and Anticancer Properties of Clonostachys

It is well known that Clonostachys and other natural nematode-antagonistic fungi can be found as endophytic organisms. This fungus activates genic functions to enhance plant self-defense mechanisms or promote better assimilation of water and nutrients by the plant roots, as mentioned above. A recent study reported the presence of C. rosea in a marine green algae Chaetomorpha antennina (Bory) Kützing, 1847, living as an endophyte organism. This isolate was analyzed, and after an organic extraction using ethyl acetate, authors assessed its potential cytotoxic effect against MCF-7 cells responsible for breast cancer [129]. The authors finally found a high cytotoxic effect against these malignant cells. After GC–MS analysis, many compounds were found such as a major compound identified as chrysin, a molecule previously reported with an important cytotoxic activity. Authors associated this activity of the endophyte C. rosea extract with this compound.

1.10.2. Biological Activities of Secondary Metabolites Identified in Clonostachys Genus

A list of secondary metabolites with important biological activities produced by Clonostachys species is shown in Table 6.

1.11. Undesirable Effects in the Use of Some Clonostachys Strains

It is also important to mention that recent studies in different countries have reported some undesirable effects of autochthonous strains of species of Clonostachys genus that have been identified as responsible for root rot disease. In this regard, in a recent study published in China, a strain of Clonostachys rosea was found to cause root rot in a Leguminosae plant from China Astragalus membranaceus Schischkin [135]. This report mentions that the strain they isolated and identified occasioned important symptoms of disease including cracks in the roots, weak aboveground, followed by yellowing and falling of leaves affecting the quality and yield of the plant [136]. Similar findings were reported in Mexico where an undesirable effect of C. rosea was identified in garlic and in avocado, where it caused root rot [137]. More recently, another Clonostachys species (C. chloroleuca) was identified in Argentina as a novel pathogen of cassava roots causing root rot disease with symptoms such as reduced plant height, chlorosis, and wilting of the leaves among others [93]. These findings alert researchers working with Clonostachys strains to pay special attention to demonstrating the harmless effect of their strains before being released to the field.

1.12. Limitations in the Use of Clonostachys Strains

Even with all the beneficial characteristics that have been demonstrated with the technology-based use of Clonostachys as a potential biotechnological tool in different fields, some limitations will have to be overcome. As mentioned above, the risk of Clonostachys strains with pathogenic effect on some crops is one of the main limitations in its use. Therefore, it is crucial to conduct a comprehensive study of the safety of the strain being used to ensure that it will not harm plants, animals, or humans.
On the other hand, other limitations in the use of this technology are the requirements to establish the development of commercial-based biopesticides. For instance, a viable and stable formulation is required, the generated information will have to be protected by a patent, and the registration of the active ingredient and its formulation will have to be established. Applying for a patent with commercial proposes seems to be a relatively simple process, and a high number of patents have been applied; however, many requirements are needed to protect a product with commercial proposes. For that reason, currently only a few products containing Clonostachys are commercially available. The international regulations to register a microbe-based product are quite too demanding and include many requirements; for instance, the aspects related to the protection of human and environmental safety to specify the active ingredients and formulation, providing details of the active ingredient, identity, and purity, effects on human health, fate, and behavior in the environment, effects on non-target organisms, among many more [138].

1.13. Future Perspectives and Challenges

Since the first identification of the genus Clonostachys more than 200 years ago, this genus has been extensively studied, revealing a wide range of desirable characteristics. These findings suggest that Clonostachys holds significant promise as a potential agent for various biotechnological applications across multiple fields. One of the key advantages of utilizing Clonostachys is its potential to partially replace chemically synthesized compounds, which are often necessary to address many problems in the field. The use of synthetic pesticides can lead to various drawbacks, making the technology reliant on Clonostachys an appealing alternative. However, several challenges must be addressed to maximize the benefits of this technology. Notably, there is substantial variation in the growth, physiological, and metabolic characteristics among different Clonostachys isolates [76]. Identifying the most economically viable strains for mass production, along with ensuring high viability and stability of spores during storage, are critical factors that need to be established for each strain intended for commercialization [76,138]. Additionally, it is important to consider reports of certain Clonostachys strains having pathogenic effects on specific crops. This concern is vital when evaluating Clonostachys as a potential biological control agent and represents a significant limitation in its application [93,135,136]. Therefore, a thorough assessment of Clonostachys isolates must be conducted to confirm their harmlessness to plants, animals, and humans before they can be approved for use as biological control agents that benefit crops.

2. Conclusions

The overuse of chemically synthesized pesticides in various sectors, such as the agriculture and livestock industries, results in the impending pollution of soil and water, posing a threat to public health and animal life. This practice also jeopardizes the microbiome of soils and aquifers.
The microorganisms within the soil ecosystem hold significant potential for addressing a wide range of issues impacting various sectors.
The genus Clonostachys has a wide range of uses and applications that are important across various fields, including public health, agriculture, livestock, pharmacology, environmental sanitation, bioremediation, among others. Its potential applications are undeniable; however, several aspects discussed in this review must be considered for its effective use in practice.

Author Contributions

The two authors of the present review participated in an equal form in the conceptualization, organization, writing—original draft preparation, and writing—review and editing of this manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This review did not receive external funding.

Acknowledgments

Authors wish to express their enormous gratitude to DVM, MSc Enrique Gutiérrez Medina, for his valuable support in the artwork design of figures.

Conflicts of Interest

The authors declare no conflicts of interest.

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Microbiolres 16 00086 g001
Figure 1. Illustrative diagram showcasing key pathogenic groups of organisms contributing to soil-borne diseases in economically significant crops. (a) Leaf deformation of lemon caused by the lepidopteran Phyllocnistis citrella; (b) citrus virus in lemon; (c) fire blight caused by the bacteria Erwinia amylovora in tomato; (d) brown spot of guava caused by the fungus Cercospora psidii; (e) leaf wilt of tomato caused by the protozoan Phytopthota infestans in tomato leaves; and (f) halls on tomato roots parasitized by nematodes.
Figure 1. Illustrative diagram showcasing key pathogenic groups of organisms contributing to soil-borne diseases in economically significant crops. (a) Leaf deformation of lemon caused by the lepidopteran Phyllocnistis citrella; (b) citrus virus in lemon; (c) fire blight caused by the bacteria Erwinia amylovora in tomato; (d) brown spot of guava caused by the fungus Cercospora psidii; (e) leaf wilt of tomato caused by the protozoan Phytopthota infestans in tomato leaves; and (f) halls on tomato roots parasitized by nematodes.
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Microbiolres 16 00086 g002
Figure 2. Circular diagrams showing the species reported for Clonostachys genus worldwide: species reported from 1839 to 2001 (Source: Index Fungorum, 2024) [81].
Figure 2. Circular diagrams showing the species reported for Clonostachys genus worldwide: species reported from 1839 to 2001 (Source: Index Fungorum, 2024) [81].
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Microbiolres 16 00086 g003
Figure 3. Circular diagrams showing the species reported for Clonostachys genus worldwide: species reported from 2007 to 2023 (Source: Index Fungorum, 2024) [81].
Figure 3. Circular diagrams showing the species reported for Clonostachys genus worldwide: species reported from 2007 to 2023 (Source: Index Fungorum, 2024) [81].
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Microbiolres 16 00086 g004
Figure 4. Scheme representative of the main morphological structures of Clonostachys: (A) anamorphic phase showing branches and sub-branched conidiophores, fialides, and conidia and a short conidiophore; (a) ascas (B) teleomorphic phase, showing perithecio, ascas, and ascospores (b) conidiophore.
Figure 4. Scheme representative of the main morphological structures of Clonostachys: (A) anamorphic phase showing branches and sub-branched conidiophores, fialides, and conidia and a short conidiophore; (a) ascas (B) teleomorphic phase, showing perithecio, ascas, and ascospores (b) conidiophore.
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Figure 5. Scheme representing different potential uses of Clonostachys genus.
Figure 5. Scheme representing different potential uses of Clonostachys genus.
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Table 1. Examples of pathogens of different crops that have developed pesticide resistance.
Table 1. Examples of pathogens of different crops that have developed pesticide resistance.
Pathogen/Host CropPesticideResultsAuthor
Phytopathogenic fungi
Botrytis cinerea
(Pers. 1797)/fruit and vegetable pre- and post-harvesting		FenhexamidMulti-resistance[48]
Penicillium digitatum (Pers.) Sacc. 1881/citrusMethyl benzimidazoles
Succinate deshydrogenase inhibitors		High resistance[49]
Sclerotinia sclerotiorum (Lib.) de Bary 1884Boscalid
2-chloro-N-(4’-chloro diphenyl-2-yl) Nicotinamide		High resistance[50]
Botrytis cinerea/GinsengCarbendazim, prodione, and pyrimethanilMulti-resistance[51]
Fusarium seudograminearum O’Donnell & T. Aoki 1999/wheatTebuconazoleLow resistance[52]
Alternaria spp./blueberriesFludioxonil, Fluazinam, Metconazole, and CyprodinilMulti-resistance[53]
Phytoparasitic nematodes
Meloidogyne incognita (Kofoid & Ehite, 1919) Chitwood 1949Carbofuran, carbosulfan, cadusafos, triazophosDevelopment of virulent populations of the parasite[54]
Meloidogyne spp.FuradanLow efficacy[55]
M. incognitaFosthiazate (Organophospate)High resistance[56]
Table 2. Species, isolation sources, and origins reported for Clonostachys genus.
Table 2. Species, isolation sources, and origins reported for Clonostachys genus.
SpeciesIsolation SourceCountryAuthor
Clonostachys agrawaliiDecomposing buffalo horn from animal house floor sweepingsIndia[87]
Clonostachys ambiguaOn barkIndonesia[88]
Clonostachys apocinyDead steam of Apocynum cannabium L. 1753USA[89]
Clonostachys aquaticaSubmerged decaying woodChina[89]
Clonostachys aranearumFrom a spider (Araneae)
Landfill/Australia		China[90]
Clonostachys araucariaFrom an Araucaria tree twigPeru[91]
Clonostachys aureofulvellaBarkAustralia[87]
Clonostachys byssicolaWood and falling leaves
From strawberry fields Fragaria ananassa (Duchesne ex Weston) Duchesne ex Rozier, 1785
From fruits of Annona squamosa L. 1753, A. x atemoya
From different sources: barks, wood, Bryophyte, litter, Pipper nigrum L. 1753, Hemelia sp., Coffea arabica, L. 1753 endophyte stems, wild C. arabica		Venezuela
Brazil
Brazil


Brazil, Venezuela, and Ethiopia		[75]
Clonostachys candelabrumSoilNetherlands[92]
Clonostachys chlorinaSoilBrazil[87]
Clonostachys chloroleucaDifferent sources: Bryophyte, native soil, soil under soybean field, soil under cotton fieldBrazil[93]
Clonostachys
chonggingensis		Decaying rotten from a mountainChina[94]
Clonostachys
compactiuscula		Soil/Germany
On bark of Prunus laurocerasus L. 1753		France[88]
Clonostachys divergensSoil
Soil		Germany
Korea		[87]
[95]
Clonostachys granuligeraOrchid barkSweden[88]
Clonostachys intermediaSoilNetherlands[87]
Clonostachys leptodermaAlnus sp. (tree/bush); rotten barkChina[94]
Clonostachys miodochialisSoilNetherlands[87]
Clonostachys oligosporaDecaying rotten twigChina[94]
Clonostachys pallensOn barkIndonesia[88]
Clonostachys phyllophilaLeaves of mistletoe (Viscum album L. 1753)
Another isolate (Unknown source)		France
Cuba		[87]
Clonostachys
pseudocrholeuca		BarkFrench Guiana[87]
Clonostachys rhizophagaChickpea debries
Culture contaminant
As mycoparasitic fungi from species of a rust Hemileia vastatrix Berck & Broome.
As a mycoparasite in Fusarum oxysporum Schltdl. 1824, native soil and on H. vastatrix, Coffea canephora
Culture contaminant		USA
Chile
Switzerland
Africa Cameroon Ethiopia

Switzerland		[96]



[75]
Clonostachys rogersoniana, Clonostachys roseaSoilBrazil[87]
C. roseaDead rhizome of the perennial plant Hedychium coronarium J. Köning
On bamboo (Phyllostachys bambusoides Sieb. et Zucc. var. aurea (Carr. ex Riv.) Makino (Xie) (=P. reticulata (Rupr.) K. Koch)
Root rot of beet root (Beta vulgaris L. 1753)
Arctic soil
Italy

Japan
USA
Norway
[87]



[97]
Clonostachys rosea f. catenulataSoil
Soil
Soil
Soil
Soil		Ukraine
USA
Germany
USA
Ukraine		[87]


[75]
Clonostachys saulensis,Dead bark on Bauhinia (Fabaceae)French Guiana[98]
Clonostachys setosaTrophis racemose L. (Urb.) (Moraceae)Cuba[87]
Clonostachys solani f. nigrovirensOn egg of Arion ater (Mollusca) and soil
On tuber of potato (Solanum tuberosum L. 1753) and soil 		Germany Netherlands[87]
Clonostachys solani f. solaniOn tuber of Solanum tuberosum
Bark
Rotten fruit of chestnut (Aesculus hippocastrum L. 1753)
Wood
From an unknown source		Netherlands Germany
France
Canada
USA		[87]
Clonostachys
squamulligera		On branch bark of willow (Salix babylonica L. 1753)
On bark of soja (Glycine sinensis Sweet 1826)		Italy
Portugal		[88]
Table 3. Clonostachys rosea isolates assessed against different insects affecting crops under different experimental conditions.
Table 3. Clonostachys rosea isolates assessed against different insects affecting crops under different experimental conditions.
SpeciesTarget PestHostsExperimental Conditions/ResultsAuthors
Clonostachys roseaCarpomya vesuviana A. Costa, 1854 (jujuve fruit fly)Jujube fruitLarval mortality of pupa = 46% using 1010 spore/mL[80]
C. roseaBemisia tabaci
(Whitefly)		Tomato50% mortality of nymphs after 6 days using 4 × 106 spores[45]
C. roseaTrogoderma granarium Everst, 1898
(Coleoptera:
Dermestidae),
Tribolium castaneum Herbst, 1797 (Coleoptera: Tenebrionidae) and Callosobruchus maculatus Fabricius, 1775
(Coleoptera: Chrysomelidae) 		Stored grains of
a number of crops:
wheat, oats, barley, corn, rice		Range of mortality
70.7–75.7%
Under in vitro conditions 		[112]
C. roseaThe mango Hopper Amritodus atkunsoni Lethierry (Hemiptera)Mango3 × 108 spores
Caused 96.67% mortality		[113]
Table 4. Predatory/parasitic activity of Clonostachys spp. against phytopathogenic fungi affecting economically important crops.
Table 4. Predatory/parasitic activity of Clonostachys spp. against phytopathogenic fungi affecting economically important crops.
ClonostachysTarget Pest/DiseaseExperimental Conditions/EfficacyAuthors
Clonostachys epichloëMycoparasite of Epichloë typhina (Pers.) Brockm. 1863 chole disease in grass species Clo G 68.33–85.28 vs. 3 E. typhina and Clo j 75–100% in a pre-colonization experiment[119]
Clonostachys roseaEutypa lata (Pers.) Tul. & C. Tul. 1863
Phaemoniella chlamydospora (W. Gams, Crous, M.J. Wingf. & Mugnai) Crous & W. Gams 2000
Botryosphaeria dothidea (Moug.) Ces. & De Not. 1863, Diaporthe spp.
Grape vine trunk 		In vitro and in vivo, growth inhibition
1.9–54% Phaeomoniella chlamydospora
(Antagonism)

(mycoparasitism)

(diseases)		[120]
C. roseaSclerotinia sclerotiorum
mycoparasite		Root of cabbage 79.63%
Crude extract 97.17% inhibition		[114]
C. roseaBotrytis cinerea tomato plants Efficiency > 90%[71]
C. roseaFusarium graminearum/oatInhibits infection effectively [121]
Table 5. Biological activity of Clonostachys species against phytoparasitic nematodes affecting different crops.
Table 5. Biological activity of Clonostachys species against phytoparasitic nematodes affecting different crops.
ClonostachysBlank Nematode/HostHostExperimental Conditions/EfficacyAuthors
C. roseaPratylenchus spp. Heterodera spp. Tylenchorrhynchus spp. Helicotylenchus spp.
Roptylenchys spp.		Carrots and wheatNematocidal activities:
Pratylenchus spp. = 38%
Heterodera spp. = 4%
Tylenchorhynchus spp. = 6%
Pratylenchys spp. = 5%
Helycotylenchys spp. = 5%
Rotylenchys spp. = 3%		[124]
C. roseaM. incognitaSacha inchiSignificantly reduced the number of root goals (around 75%)[127]
C. roseaM. incognita 2nd state juvenilesTomatoLD50 = 375 μg mL−1[123]
C. roseaM. incognitaTomatoLiquid culture filtrates of C. rosea caused 69.38% parasitized eggs[126]
Table 6. Bioactive secondary metabolites identified in Clonostachys species with potential biotechnological uses.
Table 6. Bioactive secondary metabolites identified in Clonostachys species with potential biotechnological uses.
Clonostachys SpeciesCompoundBiological ActivityAuthor
Clonostachys
compactiuscula		Clonocoprogens A, B and CAnti-malaria[130]
Clonostachys rogersonianaGliocladiosin A and BAnti-bacterial[131]
Clonosytachys byssicolaHolocellulolicic enzymesProduction of prebiotic manno-oligosacharides[72]
Clonostachys
eriocamporessi
C. byssicola		Unidentified compoundsAnti-mosquito Aedes aegypti[132]
Clonostachys roseaPolyketidsAnti-pathogenic fungi[133]
C. roseaDi-peptides
Glycol(-Gly-Phe)		Anticancer [134]
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Reyes-Estebanez, M.; Mendoza-de Gives, P. The Genus Clonostachys (Bionectria) as a Potential Tool Against Agricultural Pest and Other Biotechnological Applications: A Review. Microbiol. Res. 2025, 16, 86. https://doi.org/10.3390/microbiolres16040086

AMA Style

Reyes-Estebanez M, Mendoza-de Gives P. The Genus Clonostachys (Bionectria) as a Potential Tool Against Agricultural Pest and Other Biotechnological Applications: A Review. Microbiology Research. 2025; 16(4):86. https://doi.org/10.3390/microbiolres16040086

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Reyes-Estebanez, Manuela, and Pedro Mendoza-de Gives. 2025. "The Genus Clonostachys (Bionectria) as a Potential Tool Against Agricultural Pest and Other Biotechnological Applications: A Review" Microbiology Research 16, no. 4: 86. https://doi.org/10.3390/microbiolres16040086

APA Style

Reyes-Estebanez, M., & Mendoza-de Gives, P. (2025). The Genus Clonostachys (Bionectria) as a Potential Tool Against Agricultural Pest and Other Biotechnological Applications: A Review. Microbiology Research, 16(4), 86. https://doi.org/10.3390/microbiolres16040086

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