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BioMed Research International
Volume 2016, Article ID 3194321, 13 pages
http://dx.doi.org/10.1155/2016/3194321
Review Article

Risks of Mycotoxins from Mycoinsecticides to Humans

1College of Agriculture, South China Agricultural University, Guangzhou 510642, China
2Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Plant Protection Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China

Received 6 September 2015; Accepted 7 December 2015

Academic Editor: Daniel Cyr

Copyright © 2016 Qiongbo Hu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

There are more than thirty mycotoxins produced by fungal entomopathogens. Totally, they belong to two classes, NRP and PK mycotoxins. Most of mycotoxins have not been paid sufficient attention yet. Generally, mycotoxins do not exist in mycoinsecticide and might not be released to environments unless entomogenous fungus proliferates and produces mycotoxins in host insects or probably in plants. Some mycotoxins, destruxins as an example, are decomposed in host insects before they, with the insect’s cadavers together, are released to environments. Many species of fungal entomopathogens have the endophytic characteristics. But we do not know if fungal entomopathogens produce mycotoxins in plants and release them to environments. On the contrary, the same mycotoxins produced by phytopathogens such as Fusarium spp. and Aspergillus spp. have been paid enough concerns. In conclusion, mycotoxins from mycoinsecticides have limited ways to enter environments. The risks of mycotoxins from mycoinsecticides contaminating foods are controllable.

1. Introduction

Entomopathogenic fungi are the important factors to control natural populations of many pest species. Several species have been developed as biological control agents (BCAs) from more than 800 species of fungal entomopathogens in the world. In the BCAs, there are more than 100 mycoinsecticides for commercial use worldwide [1]. And at least 30 mycoinsecticides were registered in China; among them, Beauveria bassiana is the most popular species up to 14 products for control of locust, pine moth and diamond back moth, and so forth; Metarhizium anisopliae and Paecilomyces lilacinus with the 8 and 7 products were registered to application of grubs, corn borer, aphids and whitefly, and so forth (http://www.chinapesticide.gov.cn/hysj/index.jhtml). There is much public interest in the use of fungal biological control agents as alternatives to chemical pesticides. However, there are some concerns about the safety of BCAs to human health. Many researches about the safety of BCAs have been carried on since the 21st century. Through assessing the risks of infections, allergies, and poisoning/toxic effects [24], the most used mycoinsecticides such as B. bassiana and M. anisopliae were verified as safe biocontrol agents [57]. However, many entomopathogens produce mycotoxins which pose risks to humans and the environment; how these mycotoxins affect human health and environment are not clear yet.

Numerous mycotoxins were found from fungal entomopathogens. They can be characterized to lots of classes according to the chemical structure [8]. But briefly, they can be classified as two main classes: nonribosomal peptide (NRP) synthetase mycotoxins and polyketide (PK) synthase mycotoxins according to their biosynthetic pathways.

2. NRP Mycotoxins

Fungal entomopathogens produce various kinds of NRPs that are usually taken as pathogenic factor of these fungi species. Chemically, NRPs are the secondary metabolic compounds mainly composed of specific or modified amino acids and hydroxyl acids. They are synthesized via thiotemplate multienzyme mechanism of multifunctional enzyme complex system other than on ribosome. NRP synthetase gene of fungi is an open reading frame encoding a peptide chain composed of several modules, which activate amino acids and combined with a specific peptide product. Each module has a number of domains, and a specific reaction is catalyzed by one domain. The main domains include adenylation domains (A domains), thiotion domains (T domains), condensation domains (C domains), epimerization domains (E domains), and methylation domains (M domains) [9].

To date, more than twenty kinds of NRPs were isolated and identified from entomogenous fungi genera: Beauveria, Conoideocrella, Cordyceps, Culicinomyces, Hirsutella, Isaria, Metarhizium, Paecilomyces, Verticillium, and so forth. These NRPs include bassianolides, beauvericins, beauverolides, beauveriolides, cicadapeptins, conoideocrellides, cordycommunins, cordyheptapeptides, culicinins, cyclosporin, destruxins, efrapeptins, enniatins, hirsutellides, hirsutides, isariins, isaridins, isarolides, paecilodepsipeptides, and serinocyclins (Table 1, Figures 1 and 2). Every NRP above includes a series of analogues. Based on the molecular structures, the NRPs could be divided into chain peptides (e.g., cicadapeptin and efrapeptin) and cyclic peptides including a subdivision of cyclopeptides and cyclodepsipeptides. Cyclopeptides are cyclic structures built by amino acid residues through peptide bonding (e.g., cyclosporin), while cyclodepsipeptides are lactone compounds consisting of amino acids and hydroxyl acids which are connected by peptide bonds. Most of the NRPs belong to the group of cyclodepsipeptides [10]. To date, destruxins, beauvericins, and enniatins are the best researched NRPs. However, their detailed biosynthesis, biotransformation, and behavior and fate in the environments are not clear yet.

Table 1: NRP mycotoxins of fugal entomopathogens.
Figure 1: The structure of beauvericins (a), destruxins (b), enniatins (c), conoideocrellide (d), cicadapeptins (e), bassianolides (f), beauveriolides (g), neoefrapeptins (h), beauverolides (i), cordycommunin (j), hirsutellide (k), hirsutide (l), and efrapeptins (m).
Figure 2: The structure of isariins (a), isaridins (b), isarolide (c), serinocyclins (d), verticilides A (e), verticilides B1 (f), cyclosporines (g), and cordyheptapeptide (h).

In all NRPs of entomogenous fungi, beauvericin is considered as emerging mycotoxins likely contaminating the foods and products including rice, wheat, maize, follow-up infant formula, and Chinese medicinal herbs [1115]. The fungal entomopathogens of Beauveria spp., Paecilomyces spp., and Isaria spp. produce beauvericins [1618]. Traces of beauvericins were also detected in animal tissues and eggs [19, 20]. However, the cases of contaminations of beauvericins and enniatins are all from the infection of various Fusarium species other than entomogenous fungal species [15, 19, 2125]. Chemically, beauvericins are a kind of cyclic hexadepsipeptide with alternating methyl-phenylalanyl and hydroxy-iso-valeryl residues (Figure 1(a)). Several documents reviewed beauvericins [15, 19, 21]. Totally 11 analogues of beauvericin were found [26]. The insecticidal effects of beauvericins at a microgram level were reported in several insects [21]. The cytotoxicity of beauvericins on human cells and cancer cells was also discovered [2729]. Acetyl coenzyme-A (acyl-CoA: cholesterol acyltransferase, ACAT) is probably the target protein of beauvericins, while some research reports indicated that beauvericins might act as ionophores [30, 31].

Destruxins were isolated from culture medium of entomogenous fungii M. anisopliae and Aschersonia sp., and the fungal phytopathogen Alternaria brassicicola [32] (Figure 1(b)). Among 39 destruxin analogues, destruxins A, B, and E (DA, DB, and DE, resp.) are the most analogues and show substantial bioactivity [33]. However, the linear molecule resulting from the opening of the DA cycle is not toxic and DE would degrade to less toxic DE-diol upon enzymatic action [33]. Destruxins have insecticidal activity against many pests with various mode of action including contact action, gut toxicity, antifeedant effect, and ovicidal and oviposition deterrent activities [34]. Destruxins damage the innate immunity of insects [3537]. Destruxin maybe acts as a kind of calcium ionophore and an inhibitor of V-H+-ATPase [38]. The antiviral, antitumor, and herbicidal activities and cytotoxicity were reported as well [33]. Destruxins were decomposed in host insects before they, with the cadaver, were released to environments, so it is unlikely to contaminate the food chains [39]. In fact, there are no records about residues of destruxins in agricultural products and foods.

Enniatins could be produced by the fungal entomopathogen, Verticillium hemipterigenum BCC 1449 [69]. Enniatins are N-methylated cyclohexadepsipeptides, composed of three units each of N-methylated branched-chain L-amino acid and D-2-hydroxy acid arranged in an alternate fashion (Figure 1(c)). To date, 29 enniatins have been isolated and characterized, either as a single compounds or as mixtures of inseparable analogues [70]. Enniatins have multiactivities including antifungal, antibiotic, and cytotoxic properties. Fusafungine, one drug developed from a mixture of enniatins, is used as a topical treatment of upper respiratory tract infections by oral and/or nasal inhalation. Enniatins inhibit ABC transporters [71]. Enniatins are also a common contaminant in grain-based foods, but they were produced by the fungal species of Fusarium spp. other than entomopathogens [11, 12, 7274].

There is no information about other NRP mycotoxins influencing environments and human health.

3. PK Mycotoxins

Many fungal entomopathogen mycotoxins are polyketides and its derivatives (PKs); more than 20 PKs were discovered (Table 2, Figures 3 and 4). Fungal polyketide biosynthesis typically involves multiple enzymatic steps, and the encoding genes are often found in gene clusters. The enzymatic machinery for the formation of the polyketides consists of different modules characteristic of each fungus (e.g., keto synthases, acyl transferases, carboxylases, cyclases, dehydrases, aromatases, reductases, thioesterases, and laccases) [75].

Table 2: PK mycotoxins of fugal entomopathogens.
Figure 3: The structure of tenellin (a), cytochalasins (b), cryptosporioptide A (c), pinophilin C (d), indigotide A (e), indigotides C-F (f), 13-hydroxyindigotide A (g), 8-O-methylindigotide B (h), indigotide B (i), annullatin A (j), tenuipyrone (k), annullatin E (l), and terreusinone A (m).
Figure 4: The structure of farinosones A (a), paeciloside A (b), and militarinones B (c), isariketide (d), oosporein (e), and bassianin (f).

One of the best characterised fungal polyketide synthesis pathways is that of the tenellin (Figure 3(a)) from the insect pathogen B. bassiana [76, 77]. Tenellin is not involved in insect pathogenesis [76], but tenellin acts as an iron chelator to prevent iron-generated reactive oxygen species toxicity in B. bassiana [78]. This toxin inhibits total erythrocyte membrane ATPase activity probably because of a consequence of membrane disruption, since all pigments caused alterations in erythrocyte morphology and promoted varying degrees of cell lysis [79]. There are no reports about the risk of tenellin as a mycotoxin to contaminate foods.

Oosporein (Figure 4(e)) is the major secondary metabolite excreted by B. bassiana [80] and B. brongniartii [81]. It had a median oral toxicity to 1-day-old cockerels [82]. Oosporein inhibits total erythrocyte membrane ATPase activity in a dose-dependent manner caused alterations in erythrocyte morphology and promoted varying degrees of cell lysis [79]; meanwhile, the toxin also exhibits broad spectrum of antimicrobial, antioxidant, and cytotoxic activities [83]. However, oosporein is a rather strong organic acid; it can be concluded that oosporein can hardly be adsorbed by organisms, so oosporein is unlikely to enter food chains and influence human health [81].

Bssianin (Figure 4(f)) is a PK pigment isolated from B. bassiana. It inhibits total erythrocyte membrane ATPase activity as well [79].

The fungal entomopathogen M. anisopliae produces cytochalasins (Figure 3(b)), a famous PK [84, 85]. Cytochalasins belong to a kind of cytochalasans which comprise diverse group of fungal polyketide-amino acid hybrid metabolites with a wide range of distinctive biological functions [86]. To date, more than 80 cytochalasans have been isolated from other fungi such as Phomosis, Chalara, Hyposylon, Xylaria, Daldinia, Pseudeurotium, and Phoma exigua [75]. Cytochalasans have phytotoxins or virulence factors and exhibit antimicrobial or cytotoxic activities and inhibit cholesterol synthesis or interfere with glucose transport and hormone release. However, the origin of their name is derived from the Greek terms kytos, meaning cell, and chalasis, meaning relaxation, pointing to the best known property of cytochalasans, the capping of actin filaments. As a result, cytokinesis is effectively inhibited while mitosis remains unaffected, thereby generating giant multinucleated or even, at higher concentrations, denucleated cells. These properties are exploited in molecular and cell biology research, especially in cell imaging methods, cytoskeleton, and cell cycle studies [86].

In the entomogenous fungal genus, Cordyceps, many species produce PKs. For example, C. indigotica produces aromatic polyketides, indigotides (Figure 3(f)), 13-hydroxyindigotide A (Figure 3(g)) and 8-O-methylindigotide B (Figure 3(h)) [91, 96]. Terreusinone A (Figure 3(m)), pinophilin C (Figure 3(d)), and cryptosporioptide A (Figure 3(c)) were isolated from C. gracilioides; these three compounds inhibit the activity of protein tyrosine phosphatases [88]. Annullatins (Figures 3(j) and 3(l)) were isolated from C. annullata [87]. Opaliferin, a polyketide with a unique partial structure in which a cyclopentanone and tetrahydrofuran were connected with an external double bond, was isolated from the insect pathogenic fungus Cordyceps sp. NBRC 106954 [93]. However, there is no information about the risks of these PK toxins to human health.

As to Isaria genus, I. tenuipes produces tenuipyrone (Figure 3(k)) [94]. I. felina KMM 4639 produces isariketide Figure 4(d), showing moderate cytotoxicity toward HL-60 cells [99]. Militarinones were isolated from cultures of the Cordyceps-colonizing fungus I. farinosa. It showed significant cytotoxicity against A549 cells [100]. For the Paecilomyces genus, farinosones (Figure 4(a)) were isolated from the strain Paecilomyces farinosus RCEF 0101. They induce outgrowth but cytotoxicity in the PC-12 cell line [89]. Paeciloside A (Figure 4(b)) is isolated from Paecilomyces sp. CAFT156. Paeciloside A displays inhibitory effects on two gram-positive bacteria, Bacillus subtilis and Staphylococcus aureus, and moderate cytotoxicity towards brine shrimp larvae (Artemia salina) [101]. P. militaris produces militarinones (Figure 4(c)) [92]. There is no other information of these PKs.

4. The Fate of Mycoinsecticide and Its Mycotoxins

In mycoinsecticide, the main component is usually the spores of fungal entomopathegen. Some of mycotoxins maybe exist inside of spores other than outside of spores. Mycoinsecticide itself is almost not the resource of mycotoxins. In fact, mycotoxins mainly come from the target pests or host insects infected by fungal entomopathogen of mycoinsecticide. The endophytic entomopathogenic fungus is maybe the other important mycotoxins resources. Of course, if considering the nonmycoinsecticide factors, the crops and products infected by other fungal species such as Fusarium spp., Aspergillus spp. should be the more important resources of mycotoxins.

Totally, mycoinsecticide in its production and application has six fates (Figure 5). The first fate, humans, may be exposed to the risks of directly contacting the fungal entomopathogens. These humans are mainly the persons who long-timely produce and use the mycoinsecticide. There were several reports about fungal spores allergy of workers producing biocontrol agent of Beauveria bassiana and Metarhizium anisopliae [5, 6]. But there are no evidences supporting that the allergy is because of mycotoxins.

Figure 5: The fates of mycoinsecticide and its mycotoxins. → indicating the actually existing pathway, indicating the pathway not found to date.

When mycoinsecticide is used, the important fate is the target insects. The fungal spores of mycoinsecticide adhere insect surface and then start a pathogenic progress. After penetrating the cuticle, the fungus proliferates itself and produces mycotoxins in host insect. At last, the fungal phages and its mycotoxins along with the cadavers of host insects are released to environments. To date, we do not know how many of the mycotoxins enter the environment. However, a few research cases indicate that the mycotoxins from entomopathogens are scarcely released to environments. For example, the amount and type of destruxin produced are dependent upon the fungal strain and insect host and the fact that these compounds decomposed shortly after host death. Destruxin decomposition was presumably due to the activity of hydrolytic enzymes in the cadavers and appeared to be independent of host or soil type and biota. So, destruxins are essentially restricted to the host and pathogen and are unlikely to contaminate the environment or enter the food chain [39].

Plants including target crop and weeds are the important fate of mycoinsecticide (Figure 5). The main fungal resources of plants is from mycoinsecticide application and target pests. Plants maybe hardly receive the fungus from the systems of water, soil, and atmosphere. Fungal entomopathogen is not phytopathogen, and in general, the phages of fungal entomopathogen only deposit the plants surface. However, many species of entomogenous fungi such as B. bassiana, M. anisopliae, and I. fumosorosea have been found the endophytic characteristics [102104]. If so, the detection and management of mycotoxins from fungal entomopathogens are becoming more important, especially for those food crops.

Soil is an important storage bank of fungal entomopathogens. Fungal spores in soil can survive for long time. Through drifting from application and dropping from target pests cadavers, fungal phages and mycotoxins maybe enter the soil system. Beauveria spp., Metarhizium spp., Paecilomyces spp., and Isaria spp. can be often isolated from soil [105] and the entomopathogens in soil can be detected after mycoinsecticide is used [106]. But there are no reports that mycotoxins of fungal entomopathogen are detected in soil.

Water is another fate of mycoinsecticide. Beauvericins were detected in drainage water after Fusarium spp. was inoculated on wheat plants [107]. However, there are no researches indicating mycotoxins from mycoinsecticides entering the water system.

Atmosphere obtains fungal entomopathogens from drifting. Also, fungus might be exchanged between soil, water, and atmosphere systems. But we can not ensure that fungal mycotoxins enter atmosphere.

5. Conclusion

There are more than thirty mycotoxins isolated from fungal entomopathogens. Based on the biosynthesis, they are classified to NRP and PK mycotoxins. Beauvericins, enniatins, destruxins, cytochalasins, and tenellin are given relevantly intensive researches; other mycotoxins have not been paid sufficient attention. Mycotoxins are produced by cells of fungal entomopathogens used as mycoinsecticide. But mycotoxins are generally not in mycoinsecticide. So, mycotoxins might not be released to environments unless fungus proliferates and produces mycotoxins in host insects or probably in plants. To date, we only know little information about if mycotoxins enter environments. For example, destruxins were decomposed in host insects before they, with the cadaver, were released to environments [39]. Although entomopathogenic fungi are generally not the plants pathogens, many of them have the endophytic characteristics. However, we nowadays neither know if fungal entomopathogens produce mycotoxins in plants and release them to environments nor have enough information that the food chains are contaminated by mycotoxins the host insect produced and that human health are influenced by them. On the contrary, the same mycotoxins produced by phytopathogens such as Fusarium spp., Aspergillus spp. have been paid more attention.

In conclusion, mycotoxins from mycoinsecticides have limited ways to enter environments. The risks of mycotoxins from mycoinsecticides contaminating foods are likely controllable.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgment

This work was supported by Guangzhou Science and Technology Program (2014Y2-00513).

References

  1. S. T. Jaronski, “Ecological factors in the inundative use of fungal entomopathogens,” BioControl, vol. 55, no. 1, pp. 159–185, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. B. J. W. G. H. Mensink and J. W. A. Scheepmaker, “How to evaluate the environmental safety of microbial plant protection products: a proposal,” Biocontrol Science and Technology, vol. 17, no. 1, pp. 3–20, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. R. J. Cook, W. L. Bruckart, J. R. Coulson et al., “Safety of microorganisms intended for pest and plant disease control: a framework for scientific evaluation,” Biological Control, vol. 7, no. 3, pp. 333–351, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Strasser and M. Kirchmair, “Potential health problems due to exposure in handling and using biological control agents,” in An Ecological and Societal Approach to Biological Control, J. Eilenberg and H. M. T. Hokkanen, Eds., vol. 2 of Progress in Biological Control, pp. 275–293, Springer, Dordrecht, The Netherlands, 2006. View at Publisher · View at Google Scholar
  5. G. Zimmermann, “Review on safety of the entomopathogenic fungus Metarhizium anisopliae,” Biocontrol Science and Technology, vol. 17, no. 9, pp. 879–920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Zimmermann, “Review on safety of the entomopathogenic fungi beauveria bassiana and beauveria brongniartii,” Biocontrol Science and Technology, vol. 17, no. 6, pp. 553–596, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Zimmermann, “The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control,” Biocontrol Science and Technology, vol. 18, no. 9, pp. 865–901, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Betina, Mycotoxins (Bioactive Molecules), Elsevier Science, Amsterdam, The Netherlands, 1989.
  9. D. Boettger and C. Hertweck, “Molecular diversity sculpted by fungal PKS-NRPS hybrids,” ChemBioChem, vol. 14, no. 1, pp. 28–42, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. Q. Hu and T. Dong, “Non-ribosomal peptides from entomogenous fungi,” in Biocontrol of Lepidopteran Pests, K. S. Sree and A. Varma, Eds., vol. 43 of Soil Biology, chapter 8, Springer, 2015. View at Publisher · View at Google Scholar
  11. F. Nazari, M. Sulyok, F. Kobarfard, H. Yazdanpanah, and R. Krska, “Evaluation of emerging Fusarium mycotoxins beauvericin, enniatins, fusaproliferin and moniliformin in domestic rice in Iran,” Iranian Journal of Pharmaceutical Research, vol. 14, no. 2, pp. 505–512, 2015. View at Google Scholar · View at Scopus
  12. L. Covarelli, G. Beccari, A. Prodi et al., “Biosynthesis of beauvericin and enniatins invitro by wheat Fusarium species and natural grain contamination in an area of central Italy,” Food Microbiology, vol. 46, pp. 618–626, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. A. B. Serrano, G. Meca, G. Font, and E. Ferrer, “Risk assessment of beauvericin, enniatins and fusaproliferin present in follow-up infant formula by invitro evaluation of the duodenal and colonic bioaccessibility,” Food Control, vol. 42, pp. 234–241, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Hu and M. Rychlik, “Occurrence of enniatins and beauvericin in 60 Chinese medicinal herbs,” Food Additives and Contaminants A: Chemistry, Analysis, Control, Exposure and Risk Assessment, vol. 31, no. 7, pp. 1240–1245, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Santini, G. Meca, S. Uhlig, and A. Ritieni, “Fusaproliferin, beauvericin and enniatins: occurrence in food—a review,” World Mycotoxin Journal, vol. 5, no. 1, pp. 71–81, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. J. J. Luangsa-Ard, P. Berkaew, R. Ridkaew, N. L. Hywel-Jones, and M. Isaka, “A beauvericin hot spot in the genus Isaria,” Mycological Research, vol. 113, no. 12, pp. 1389–1395, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. F. R. Champlin and E. A. Grula, “Noninvolvement of beauvericin in the entomopathogenicity of Beauveria bassiana,” Applied and Environmental Microbiology, vol. 37, no. 6, pp. 1122–1126, 1979. View at Google Scholar · View at Scopus
  18. C. Nilanonta, M. Isaka, P. Kittakoop, S. Trakulnaleamsai, M. Tanticharoen, and Y. Thebtaranonth, “Precursor-directed biosynthesis of beauvericin analogs by the insect pathogenic fungus Paecilomyces tenuipes BCC 1614,” Tetrahedron, vol. 58, no. 17, pp. 3355–3360, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Jestoi, “Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin—a review,” Critical Reviews in Food Science and Nutrition, vol. 48, no. 1, pp. 21–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Jestoi, M. Rokka, E. Järvenpää, and K. Peltonen, “Determination of Fusarium mycotoxins beauvericin and enniatins (A, A1, B, B1) in eggs of laying hens using liquid chromatography-tandem mass spectrometry (LC-MS/MS),” Food Chemistry, vol. 115, no. 3, pp. 1120–1127, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. Q. G. Wang and L. J. Xu, “Beauvericin, a bioactive compound produced by fungi: a short review,” Molecules, vol. 17, no. 3, pp. 2367–2377, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Fotso, J. F. Leslie, and J. S. Smith, “Production of beauvericin, moniliformin, fusaproliferin, and fumonisins B1, B2, and B3 by fifteen ex-type strains of Fusarium species,” Applied and Environmental Microbiology, vol. 68, no. 10, pp. 5195–5197, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. M. M. Reynoso, A. M. Torres, and S. N. Chulze, “Fusaproliferin, beauvericin and fumonisin production by different mating populations among the Gibberella fujikuroi complex isolated from maize,” Mycological Research, vol. 108, no. 2, pp. 154–160, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Moretti, G. Mulè, A. Ritieni, and A. Logrieco, “Further data on the production of beauvericin, enniatins and fusaproliferin and toxicity to Artemia salina by Fusarium species of Gibberella fujikuroi species complex,” International Journal of Food Microbiology, vol. 118, no. 2, pp. 158–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Moretti, G. Mulé, A. Ritieni et al., “Cryptic subspecies and beauvericin production by Fusarium subglutinans from Europe,” International Journal of Food Microbiology, vol. 127, no. 3, pp. 312–315, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. Q. Hu and T. Dong, “Non-ribosomal peptides from entomogenous fungi,” in Biocontrol of Lepidopteran Pests, K. S. Sree and A. Varma, Eds., vol. 43 of Soil Biology, chapter 8, pp. 169–206, Springer, Basel, Switzerland, 2015. View at Publisher · View at Google Scholar
  27. Y. W. Tao, Y. C. Lin, Z. G. She, M. T. Lin, P. X. Chen, and J. Y. Zhang, “Anticancer activity and mechanism investigation of beauvericin isolated from secondary metabolites of the mangrove endophytic fungi,” Anti-Cancer Agents in Medicinal Chemistry, vol. 15, pp. 258–266, 2015. View at Google Scholar
  28. W. Wätjen, A. Debbab, A. Hohlfeld, Y. Chovolou, and P. Proksch, “The mycotoxin beauvericin induces apoptotic cell death in H4IIE hepatoma cells accompanied by an inhibition of NF-κB-activity and modulation of MAP-kinases,” Toxicology Letters, vol. 231, no. 1, pp. 9–16, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. X.-F. Wu, R. Xu, Z.-J. Ouyang et al., “Beauvericin ameliorates experimental colitis by inhibiting activated T cells via downregulation of the PI3K/Akt signaling pathway,” PLoS ONE, vol. 8, no. 12, Article ID e83013, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Makrlík, P. Toman, and P. Vaňura, “Extraction and DFT study on the complexation of Zn2+ with beauvericin,” Acta Chimica Slovenica, vol. 60, no. 4, pp. 884–888, 2013. View at Google Scholar · View at Scopus
  31. E. Makrlík, P. Toman, and P. Vaňura, “Complexation of Pb2+ with beauvericin: an experimental and theoretical study,” Monatshefte fur Chemie, vol. 144, no. 10, pp. 1461–1465, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. M. S. C. Pedras, L. Irina Zaharia, and D. E. Ward, “The destruxins: synthesis, biosynthesis, biotransformation, and biological activity,” Phytochemistry, vol. 59, no. 6, pp. 579–596, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. B.-L. Liu and Y.-M. Tzeng, “Development and applications of destruxins: a review,” Biotechnology Advances, vol. 30, no. 6, pp. 1242–1254, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. X. Chen and Q. Hu, “Non-ribosomal peptidic toxins of entomogenous fungi,” Chinese Journal of Biological Control, vol. 29, pp. 142–152, 2013. View at Google Scholar
  35. A. Vey, V. Matha, and C. Dumas, “Effects of the peptide mycotoxin destruxin E on insect haemocytes and on dynamics and efficiency of the multicellular immune reaction,” Journal of Invertebrate Pathology, vol. 80, no. 3, pp. 177–187, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. J.-Q. Fan, X.-R. Chen, and Q.-B. Hu, “Effects of destruxin a on hemocytes morphology of bombyx mori,” Journal of Integrative Agriculture, vol. 12, no. 6, pp. 1042–1048, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Pal, R. J. S. Leger, and L. P. Wu, “Fungal peptide destruxin a plays a specific role in suppressing the innate immune response in Drosophila melanogaster,” The Journal of Biological Chemistry, vol. 282, no. 12, pp. 8969–8977, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. M. J. Vázquez, M. I. Albarrán, A. Espada, A. Rivera-Sagredo, E. Díez, and J. A. Hueso-Rodríguez, “A new destruxin as inhibitor of vacuolar-type H+-ATPase of Saccharomyces cerevisiae,” Chemistry and Biodiversity, vol. 2, no. 1, pp. 123–130, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Skrobek, F. A. Shah, and T. M. Butt, “Destruxin production by the entomogenous fungus Metarhizium anisopliae in insects and factors influencing their degradation,” BioControl, vol. 53, no. 2, pp. 361–373, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. B. Krasnoff, R. F. Reátegui, M. M. Wagenaar, J. B. Gloer, and D. M. Gibson, “Cicadapeptins I and II: new aib-containing peptides from the entomopathogenic fungus Cordyceps heteropoda,” Journal of Natural Products, vol. 68, no. 1, pp. 50–55, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Rivas, G. Howell, and Z. Floyd, “Orgn 441—progress toward the synthesis of two antibacterial heptapeptides: cicadapeptins I and II,” in Proceedings of the 236th ACS National Meeting, Abstracts of Papers of the American Chemical Society, Philadelphia, Pa, USA, August 2008.
  42. F. Rivas, G. Howell, S. Ntrawka, and C. Thakkar, “Synthesis of antibacterial cicadapeptins: a tool to introduce undergraduate students to research,” Biopolymers, vol. 92, p. 362, 2009. View at Google Scholar
  43. H. He, J. E. Janso, H. Y. Yang, V. S. Bernan, S. L. Lin, and K. Yu, “Culicinin D, an antitumor peptaibol produced by the fungus Culicinomyces clavisporus, strain LL-12I252,” Journal of Natural Products, vol. 69, no. 5, pp. 736–741, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. W. Zhang, N. Ding, and Y. X. Li, “An improved synthesis of (2S, 4S)- and (2S, 4R)-2-amino-4-methyldecanoic acids: assignment of the stereochemistry of culicinins,” Journal of Peptide Science, vol. 17, no. 8, pp. 576–580, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. A. E. Papathanassiu, N. J. MacDonald, D. R. Emlet, and H. A. Vu, “Antitumor activity of efrapeptins, alone or in combination with 2-deoxyglucose, in breast cancer in vitro and in vivo,” Cell Stress and Chaperones, vol. 16, no. 2, pp. 181–193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Jost, S. Weigelt, T. Huber et al., “Synthesis and structural and biological studies of efrapeptin C analogues,” Chemistry and Biodiversity, vol. 4, no. 6, pp. 1170–1182, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Fredenhagen, L.-P. Molleyres, B. Böhlendorf, and G. Laue, “Structure determination of neoefrapeptins A to N: peptides with insecticidal activity produced by the fungus Geotrichum candidum,” Journal of Antibiotics, vol. 59, no. 5, pp. 267–280, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Q. Xu, R. Orozco, E. M. K. Wijeratne et al., “Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana,” Fungal Genetics and Biology, vol. 46, no. 5, pp. 353–364, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Logrieco, A. Ritieni, A. Moretti, G. Randazzo, and A. Bottalico, “Beauvericin and fusaproliferin: new emerging fusarium toxins,” Cereal Research Communications, vol. 25, pp. 407–413, 1997. View at Google Scholar
  50. S. Ganassi, A. Moretti, A. Maria Bonvicini Pagliai, A. Logrieco, and M. Agnese Sabatini, “Effects of beauvericin on Schizaphis graminum (Aphididae),” Journal of Invertebrate Pathology, vol. 80, no. 2, pp. 90–96, 2002. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Calò, F. Fornelli, R. Ramires et al., “Cytotoxic effects of the mycotoxin beauvericin to human cell lines of myeloid origin,” Pharmacological Research, vol. 49, no. 1, pp. 73–77, 2004. View at Publisher · View at Google Scholar
  52. M. Isaka, S. Palasarn, S. Supothina, S. Komwijit, and J. J. Luangsa-Ard, “Bioactive compounds from the scale insect pathogenic fungus conoideocrella tenuis BCC 18627,” Journal of Natural Products, vol. 74, no. 4, pp. 782–789, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Isaka, S. Palasarn, S. Lapanun, and K. Sriklung, “Paecilodepsipeptide A, an antimalarial and antitumor cyclohexadepsipeptide from the insect pathogenic fungus Paecilomyces cinnamomeus BCC 9616,” Journal of Natural Products, vol. 70, no. 4, pp. 675–678, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Isaka, S. Palasarn, K. Kocharin, and N. L. Hywel-Jones, “Comparison of the bioactive secondary metabolites from the scale insect pathogens, Anamorph Paecilomyces cinnamomeus, and Teleomorph Torrubiella luteorostrata,” The Journal of Antibiotics, vol. 60, no. 9, pp. 577–581, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. J. Yang, Y. G. Wang, X. F. Liu, and J. Wu, “Synthesis and anti-tumor activity of cyclodepsipeptides paecilodepsipeptide A,” Advanced Materials Research, vol. 643, pp. 92–96, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Haritakun, M. Sappan, R. Suvannakad, K. Tasanathai, and M. Isaka, “An antimycobacterial cyclodepsipeptide from the entomopathogenic fungus Ophiocordyceps communis BCC 16475,” Journal of Natural Products, vol. 73, no. 1, pp. 75–78, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. I. M. Abalis, Biochemical and Pharmacological Studies of the Insecticidal Cyclodepsipeptides Destruxins and Bassianolide Produced by Entomopathogenic Fungi, Cornell University, Ithaca, NY, USA, 1981.
  58. N. Vongvanich, P. Kittakoop, M. Isaka et al., “Hirsutellide A, a new antimycobacterial cyclohexadepsipeptide from the entomopathogenic fungus Hirsutella kobayasii,” Journal of Natural Products, vol. 65, no. 9, pp. 1346–1348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. G. Lang, J. W. Blunt, N. J. Cummings, A. L. J. Cole, and M. H. G. Munro, “Hirsutide, a cyclic tetrapeptide from a spider-derived entomopathogenic fungus, Hirsutella sp.,” Journal of Natural Products, vol. 68, no. 8, pp. 1303–1305, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. V. Sabareesh, R. S. Ranganayaki, S. Raghothama et al., “Identification and characterization of a library of microheterogeneous cyclohexadepsipeptides from the fungus Isaria,” Journal of Natural Products, vol. 70, no. 5, pp. 715–729, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Ravindra, R. S. Ranganayaki, S. Raghothama et al., “Two novel hexadepsipeptides with several modified amino acid residues isolated from the fungus Isaria,” Chemistry & Biodiversity, vol. 1, no. 3, pp. 489–504, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. F.-Y. Du, P. Zhang, X.-M. Li, C.-S. Li, C.-M. Cui, and B.-G. Wang, “Cyclohexadepsipeptides of the isaridin class from the marine-derived fungus beauveria felina EN-135,” Journal of Natural Products, vol. 77, no. 5, pp. 1164–1169, 2014. View at Publisher · View at Google Scholar · View at Scopus
  63. S. B. Krasnoff, I. Keresztes, R. E. Gillilan et al., “Serinocyclins A and B, cyclic heptapeptides from Metarhizium anisopliae,” Journal of Natural Products, vol. 70, no. 12, pp. 1919–1924, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Shiomi, R. Matsui, A. Kakei et al., “Verticilide, a new ryanodine-binding inhibitor, produced by Verticillium sp. FKI-1033,” The Journal of Antibiotics, vol. 63, no. 2, pp. 77–82, 2010. View at Publisher · View at Google Scholar
  65. S. Monma, T. Sunazuka, K. Nagai et al., “Verticilide: elucidation of absolute configuration and total synthesis,” Organic Letters, vol. 8, no. 24, pp. 5601–5604, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. T. Ohshiro, D. Matsuda, T. Kazuhiro et al., “New verticilides, inhibitors of acyl-CoA:cholesterol acyltransferase, produced by Verticillium sp. FKI-2679,” Journal of Antibiotics, vol. 65, pp. 255–262, 2012. View at Google Scholar
  67. M. Isaka, U. Srisanoh, N. Lartpornmatulee, and T. Boonruangprapa, “ES-242 derivatives and cycloheptapeptides from Cordyceps sp. strains BCC 16173 and BCC 16176,” Journal of Natural Products, vol. 70, no. 10, pp. 1601–1604, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. V. Rukachaisirikul, S. Chantaruk, C. Tansakul et al., “A cyclopeptide from the insect pathogenic fungus Cordyceps sp. BCC 1788,” Journal of Natural Products, vol. 69, no. 2, pp. 305–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Supothina, M. Isaka, K. Kirtikara, M. Tanticharoen, and Y. Thebtaranonth, “Enniatin production by the entomopathogenic fungus Verticillium hemipterigenum BCC 1449,” Journal of Antibiotics, vol. 57, no. 11, pp. 732–738, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. A. A. Sy-Cordero, C. J. Pearce, and N. H. Oberlies, “Revisiting the enniatins: a review of their isolation, biosynthesis, structure determination and biological activities,” The Journal of Antibiotics, vol. 65, no. 11, pp. 541–549, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Hiraga, S. Yamamoto, H. Fukuda, N. Hamanaka, and K. Oda, “Enniatin has a new function as an inhibitor of Pdr5p, one of the ABC transporters in Saccharomyces cerevisiae,” Biochemical and Biophysical Research Communications, vol. 328, no. 4, pp. 1119–1125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. Z. F. Wang, X. A. Lin, M. A. Yu, Y. J. Huang, X. M. Qian, and Y. M. Shen, “Wine contamination by mycotoxin enniatin B from Fusarium tricinctum (Corda) Sacc,” Journal: Food, Agriculture and Environment, vol. 9, no. 1, pp. 182–185, 2011. View at Google Scholar
  73. S. Uhlig, M. Torp, and B. T. Heier, “Beauvericin and enniatins A, A1, B and B1 in Norwegian grain: a survey,” Food Chemistry, vol. 94, no. 2, pp. 193–201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. R. Dornetshuber-Fleiss, D. Heilos, T. Mohr et al., “The naturally born fusariotoxin enniatin B and sorafenib exert synergistic activity against cervical cancer in vitro and in vivo,” Biochemical Pharmacology, vol. 93, no. 3, pp. 318–331, 2015. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Bräse, A. Encinas, J. Keck, and C. F. Nising, “Chemistry and biology of mycotoxins and related fungal metabolites,” Chemical Reviews, vol. 109, no. 9, pp. 3903–3990, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. K. L. Eley, L. M. Halo, Z. Song et al., “Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana,” ChemBioChem, vol. 8, no. 3, pp. 289–297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. L. M. Halo, J. W. Marshall, A. A. Yakasai et al., “Authentic heterologous expression of the tenellin iterative polyketide synthase nonribosomal peptide synthetase requires coexpression with an enoyl reductase,” ChemBioChem, vol. 9, no. 4, pp. 585–594, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Jirakkakul, S. Cheevadhanarak, J. Punya et al., “Tenellin acts as an iron chelator to prevent iron-generated reactive oxygen species toxicity in the entomopathogenic fungus Beauveria bassiana,” FEMS Microbiology Letters, vol. 362, no. 2, pp. 1–8, 2015. View at Publisher · View at Google Scholar
  79. L. B. Jeffs and G. G. Khachatourians, “Toxic properties of Beauveria pigments on erythrocyte membranes,” Toxicon, vol. 35, no. 8, pp. 1351–1356, 1997. View at Publisher · View at Google Scholar · View at Scopus
  80. S. H. El Basyouni and L. C. Vining, “Biosynthesis of oosporein in Beauveria bassiana (bals.) vuill,” Canadian journal of biochemistry, vol. 44, no. 5, pp. 557–565, 1966. View at Publisher · View at Google Scholar · View at Scopus
  81. C. Seger, D. Erlebach, H. Stuppner, U. J. Griesser, and H. Strasser, “Physicochemical properties of oosporein, the major secreted metabolite of the entomopathogenic fungus Beauveria brongniartii,” Helvetica Chimica Acta, vol. 88, no. 4, pp. 802–810, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. R. J. Cole, J. W. Kirksey, H. G. Cutler, and E. E. Davis, “Toxic effects of oosporein from Chaetomium trilaterale,” Journal of Agricultural and Food Chemistry, vol. 22, no. 3, pp. 517–520, 1974. View at Publisher · View at Google Scholar · View at Scopus
  83. R. Alurappa, M. R. M. Bojegowda, V. Kumar, N. K. Mallesh, and S. Chowdappa, “Characterisation and bioactivity of oosporein produced by endophytic fungus Cochliobolus kusanoi isolated from Nerium oleander L.,” Natural Product Research, vol. 28, no. 23, pp. 2217–2220, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. D. W. Roberts, “Toxins of entomopathogenic fungi,” in Microhial Control of Pests, H. D. Burges, Ed., pp. 441–464, Academic Press, London, UK, 1981. View at Google Scholar
  85. H. Strasser, A. Vey, and T. M. Butt, “Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species?” Biocontrol Science and Technology, vol. 10, no. 6, pp. 717–735, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. K. Scherlach, D. Boettger, N. Remme, and C. Hertweck, “The chemistry and biology of cytochalasans,” Natural Product Reports, vol. 27, no. 6, pp. 869–886, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Asai, D. Luo, Y. Obara et al., “Dihydrobenzofurans as cannabinoid receptor ligands from Cordyceps annullata, an entomopathogenic fungus cultivated in the presence of an HDAC inhibitor,” Tetrahedron Letters, vol. 53, no. 17, pp. 2239–2243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. P.-Y. Wei, L.-X. Liu, T. Liu, C. Chen, D.-Q. Luo, and B.-Z. Shi, “Three new pigment protein tyrosine phosphatases inhibitors from the insect parasite fungus Cordyceps gracilioides: terreusinone A, pinophilin C and cryptosporioptide A,” Molecules, vol. 20, no. 4, pp. 5825–5834, 2015. View at Publisher · View at Google Scholar
  89. Y. Cheng, B. Schneider, U. Riese, B. Schubert, Z. Li, and M. Hamburger, “Farinosones A-C, neurotrophic alkaloidal metabolites from the entomogenous deuteromycete Paecilomyces farinosus,” Journal of Natural Products, vol. 67, no. 11, pp. 1854–1858, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. Z. Q. Liu, T. Liu, C. Chen et al., “Fumosorinone, a novel ptp1b inhibitor, activates insulin signaling in insulin-resistance hepg2 cells and shows anti-diabetic effect in diabetic kkay mice,” Toxicology and Applied Pharmacology, vol. 285, pp. 61–70, 2015. View at Google Scholar
  91. T. Asai, T. Yamamoto, Y.-M. Chung et al., “Aromatic polyketide glycosides from an entomopathogenic fungus, Cordyceps indigotica,” Tetrahedron Letters, vol. 53, no. 3, pp. 277–280, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. K. Schmidt, U. Riese, Z. Li, and M. Hamburger, “Novel tetramic acids and pyridone alkaloids, militarinones B, C, and D, from the insect pathogenic fungus Paecilomyces militaris,” Journal of Natural Products, vol. 66, no. 3, pp. 378–383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Grudniewska, S. Hayashi, M. Shimizu et al., “Opaliferin, a new polyketide from cultures of entomopathogenic fungus Cordyceps sp. NBRC 106954,” Organic Letters, vol. 16, pp. 4695–4697, 2014. View at Google Scholar
  94. T. Asai, Y.-M. Chung, H. Sakurai et al., “Tenuipyrone, a novel skeletal polyketide from the entomopathogenic fungus, Isaria tenuipes, cultivated in the presence of epigenetic modifiers,” Organic Letters, vol. 14, no. 2, pp. 513–515, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Isaka, P. Chinthanom, S. Supothina, P. Tobwor, and N. L. Hywel-Jones, “Pyridone and tetramic acid alkaloids from the spider pathogenic fungus Torrubiella sp. BCC 2165,” Journal of Natural Products, vol. 73, no. 12, pp. 2057–2060, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Asai, T. Yamamoto, and Y. Oshima, “Aromatic polyketide production in cordyceps indigotica, an entomopathogenic fungus, induced by exposure to a histone deacetylase inhibitor,” Organic Letters, vol. 14, no. 8, pp. 2006–2009, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. B.-Z. Mao, C. Huang, G.-M. Yang, Y.-Z. Chen, and S.-Y. Chen, “Separation and determination of the bioactivity of oosporein from chaetomium cupreum,” African Journal of Biotechnology, vol. 9, no. 36, pp. 5955–5961, 2010. View at Google Scholar · View at Scopus
  98. K. M. Fisch, W. Bakeer, A. A. Yakasai et al., “Rational domain swaps decipher programming in fungal highly reducing polyketide synthases and resurrect an extinct metabolite,” Journal of the American Chemical Society, vol. 133, no. 41, pp. 16635–16641, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. A. N. Yurchenko, O. F. Smetanina, A. I. Kalinovsky et al., “Oxirapentyns F-K from the marine-sediment-derived fungus Isaria felina KMM 4639,” Journal of Natural Products, vol. 77, no. 6, pp. 1321–1328, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. C. Ma, Y. Li, S.-B. Niu, H. Zhang, X.-Z. Liu, and Y. Che, “N-hydroxypyridones, phenylhydrazones, and a quinazolinone from isaria farinosa,” Journal of Natural Products, vol. 74, no. 1, pp. 32–37, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. F. M. Talontsi, T. J. N. Kenla, B. Dittrich, C. Douania-Meli, and H. Laatsch, “Paeciloside A, a new antimicrobial and cytotoxic polyketide from Paecilomyces sp. strain CAFT156,” Planta Medica, vol. 78, no. 10, pp. 1020–1023, 2012. View at Publisher · View at Google Scholar
  102. S. Mantzoukas, C. Chondrogiannis, and G. Grammatikopoulos, “Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides,” Entomologia Experimentalis et Applicata, vol. 154, no. 1, pp. 78–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  103. M. L. Russo, S. A. Pelizza, M. N. Cabello, S. A. Stenglein, and A. C. Scorsetti, “Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales),” Biocontrol Science and Technology, vol. 25, no. 4, pp. 475–480, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. S. Parsa, V. Ortiz, and F. E. Vega, “Establishing fungal entomopathogens as endophytes: towards endophytic biological control,” Journal of Visualized Experiments, no. 74, Article ID e50360, 2013. View at Publisher · View at Google Scholar
  105. Q. B. Hu, S. Y. Liu, F. Yin, S. J. Cai, G. H. Zhong, and S. X. Ren, “Diversity and virulence of soil-dwelling fungi Isaria spp. and Paecilomyces spp. against Solenopsis invicta (Hymenoptera: Formicidae),” Biocontrol Science and Technology, vol. 21, no. 2, pp. 225–234, 2011. View at Publisher · View at Google Scholar
  106. C. Biswas, P. Dey, B. S. Gotyal, and S. Satpathy, “A method of multiplex PCR for detection of field released Beauveria bassiana, a fungal entomopathogen applied for pest management in jute (Corchorus olitorius),” World Journal of Microbiology and Biotechnology, vol. 31, no. 4, pp. 675–679, 2015. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Schenzel, H.-R. Forrer, S. Vogelgsang, K. Hungerbühler, and T. D. Bucheli, “Mycotoxins in the environment. I. Production and emission from an agricultural test field,” Environmental Science and Technology, vol. 46, no. 24, pp. 13067–13075, 2012. View at Publisher · View at Google Scholar · View at Scopus