Entomopathogenic Fungi: Interactions and Applications: History
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Spiridon Mantzoukas

Entomopathogenic fungi are a special group of soil-dwelling microorganisms that infects and kills insects and other arthropods through cuticle penetration. They are currently used as biocontrol agents against insect plant pests and play a vital role in their management. Regardless that entomopathogenic fungi are currently on the agriculture market, their full potential has not yet been utterly explored. Up to date substantial research has covered the topic revealing numerous uses in pest management but also on their ability as endophytes, assisting the plant host on growth and pathogen resistance. This article addresses the literature on entomopathogenic fungi through the years, noting their mode of action, advantages, potential applications, and prospects.

  • entomopathogenic fungi
  • insects
  • plants
  • endophytes
  • pest management
  • biopesticides
Interestingly, the idea of implementing microorganisms for pest control is not a modern application. The first entomopathogenic fungus was discovered and described by Agostino Bassi (1773–1856) in 1835, causing white muscardine disease in insects and was later named Beauveria bassiana (Balsamo) Vuillemin (Hypocreales, Cordycipitaceae) [1]. Some years later, Elias Metschnikoff (1845–1916) discovered the green muscardine, a fungal disease attacking insects, induced by Metarhizium anisopliae Metschnikoff Sorokin (Hypocreales, Clavicipitaceae) [2]. In the late 19th century, the combination of these discoveries and the groundbreaking knowledge obtained by the father of microbiology Louis Pasteur (1822–1895), led to assays experimenting on fungi as potential microbial control agents [3]. Later, the entrance of chemical insecticides in the market held back the establishment of fungi in pest management. Also, the development of Bacillus thuringiensis (Baciliales, Bacillaceae) Berliner against insects, played an important role on the biological protection research. While it assisted acknowledging the potential use of exploiting microorganisms as pest control agents, it may have detained the advance of biological protection studies, as the scientific community focused on bacterial entomopathogens [4]. Nonetheless, to present, even though entomopathogenic fungi (EPF) have been commercialized in the last years, their broad potential applications have not yet been fully discovered.
The advances in molecular biology and DNA sequencing allowed the collection and classification of organisms and along with the symbiosis theory, provided a better comprehension on the interactions between plants, fungi, and insects. During the last years, because of the concerning environmental implications of the extensive use of synthetic substances, the interests of research was rotated on alternatives of chemical pest management and so the EPF came back on the scene. Up to date, numerous studies and reviews have documented the multifaceted roles of EPF as endophytes that antagonize plant diseases [5][6][7][8][9][10], promote plant growth [11][12][13][14], and benefit the rhizosphere through colonization [15][16][17]. The use of EPF so far has been limited to utilization as inundate biopesticides against insects [18], although the newly emerging attributes open the way to complementary roles as dual agents against both arthropods and plant diseases, as vertically transmitted endophytes, and as biofertilizers [12][19][20]. Some fungal endophytes establish themselves in plants naturally while others are introduced therein artificially [21] (Figure 1).
Figure 1. Applications of entomopathogenic fungi and the main effects.
Many EPF isolates have been recorded and tested throughout the years, some of them with thriving results. The ubiquitous soil-borne fungus, B. bassiana is recorded to infect more than 700 insect species. [22] Other examples of artificially inoculated endophytes are Metarhizium brunneum Petch (Hypocreales, Clavicipitaceae) in broad bean by [12], M. anisopliae in broad bean by Akello and Sikora (2012) [23] and cassava by Greenfield et al. (2016) [24]. Beauveria brognartii Sakkaro Petch was also tested in broad bean by Jaber and Enkerli (2017) [12]. Lastly, Metarhizium robertsii Metschnikoff Sorokin (Hypocreales, Clavicipitaceae) and Isaria fumosorosea Wie Brown and Smith (Hypocreales, Cordycipitaceae) was examined in sweet sorghum by Mantzoukas et al., 2015 [25].
Studies have provided data suggesting that fungal endophytes may act antagonistically against plant diseases, such as Fusarium oxysporum Snyder & Hansen (Hypocreales, Nectriaceae), Botrytis cinerea Pers. (Helotiales, Sclerotiniaceae), Alternaria solani Sorauer (Pleosporales, Pleosporaceae) [26] Fusarium solani f. sp. phaseoli Sacc. (Hypocreales, Nectriaceae) [7] and others. Fungal endophytes effects include mycoparasitism, antagonistic race for nutrition, and antibiosis. The effect on insects occurring upon infection includes physiological and behavioral changes, such as feeding deterrence, inertia, changes in oviposition etc., as possible consequences of the secondary metabolites secreted by fungi themselves [27].

References

  1. Rehner, S.A.; Vega, F.E.; Blackwell, M. Phylogenetics and Insect Pathogenic Genus Beauveria. In Insect–Fungal Associations: Ecology and Evolution; Oxford University Press, Inc.: New York, NY, USA, 2005; pp. 3–25.
  2. Zimmermann, G.; Papierok, B.; Glare, T. Elias Metschnikoff, Elie Metchnikoff or Ilya Ilich Mechnikov (1845–1916): A Pioneer in Insect Pathology, the First Describer of the Entomopathogenic Fungus Metarhizium anisopliae and How to Translate a Russian Name. Biocontrol Sci. Technol. 1995, 5, 527–530.
  3. Lord, J.C. From Metchnikoff to Monsanto and beyond: The path of microbial control. J. Invertebr. Pathol. 2005, 89, 19–29.
  4. Lacey, L.A.; Frutos, R.; Kaya, H.K.; Vail, P. Insect Pathogens as Biological Control Agents: Do They Have a Future? Biol. Control 2001, 21, 230–248.
  5. Ownley, B.H.; Griffin, M.R.; Klingeman, W.; Gwinn, K.D.; Moulton, J.K.; Pereira, R. Beauveria bassiana: Endophytic colonization and plant disease control. J. Invertebr. Pathol. 2008, 98, 267–270.
  6. Goettel, M.S.; Koike, M.; Kim, J.J.; Aiuchi, D.; Shinya, R.; Brodeur, J. Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. J. Invertebr. Pathol. 2008, 98, 256–261.
  7. Sasan, R.K.; Bidochka, M.J. Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can. J. Plant Pathol. 2013, 35, 288–293.
  8. Jaber, L.R.; Salem, N.M. Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Sci. Technol. 2014, 24, 1096–1109.
  9. Jaber, L.R.; Ownley, B. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol. Control 2018, 116, 36–45.
  10. Chang, Y.; Xia, X.; Sui, L.; Kang, Q.; Lu, Y.; Li, L.; Liu, W.; Li, Q.; Zhang, Z. Endophytic colonization of entomopathogenic fungi increases plant disease resistance by changing the endophytic bacterial community. J. Basic Microbiol. 2021, 61, 1098–1112.
  11. Sasan, R.K.; Bidochka, M.J. The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am. J. Bot. 2012, 99, 101–107.
  12. Jaber, L.R.; Enkerli, J. Fungal entomopathogens as endophytes: Can they promote plant growth? Biocontrol Sci. Technol. 2017, 27, 28–41.
  13. Dara, S.K. Non-entomopathogenic roles of entomopathogenic fungi in promoting plant health and growth. Insects 2019, 10, 277.
  14. Bamisile, B.S.; Siddiqui, J.A.; Akutse, K.S.; Aguila, L.C.R.; Xu, Y. General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents. Plants 2021, 10, 2119.
  15. Bruck, D.J. Fungal entomopathogens in the rhizosphere. In The Ecology of Fungal Entomopathogens; Springer: Dordrecht, The Netherlands, 2009; pp. 103–112.
  16. Pava-Ripoll, M.; Angelini, C.; Fang, W.; Wang, S.; Posada, F.J.; Leger, R.S. The rhizosphere-competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology 2011, 157, 47–55.
  17. Nelly, N.; Syahrawati, M.; Hamid, H.; Habazar, T.; Gusnia, D.N. Diversity and characterization of entomopathogenic fungi from rhizosphere of maize plants as potential biological control agents. Biodivers. J. Biol. Divers. 2019, 20, 1435–1441.
  18. De Faria, M.R.; Wraight, S.P. Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol. Control 2007, 43, 237–256.
  19. Quesada-Moraga, E.; López-Díaz, C.; Landa, B.B. The hidden habit of the entomopathogenic fungus Beauveria bassiana: First demonstration of vertical plant transmission. PLoS ONE 2014, 9, e89278.
  20. Lacey, L.A.; Grzywacz, D.; Shapiro-Ilan, D.I.; Frutos, R.; Brownbridge, M.; Goettel, M.S. Insect pathogens as biological control agents: Back to the future. J. Invertebr. Pathol. 2015, 132, 1–41.
  21. Vega, F.E.; Goettel, M.S.; Blackwell, M.; Chandler, D.; Jackson, M.A.; Keller, S.; Koike, M.; Maniania, N.K.; Monzón, A.; Ownley, B.; et al. Fungal entomopathogens: New insights on their ecology. Fungal Ecol. 2009, 2, 149–159.
  22. Inglis, G.D.; Goettel, M.S.; Butt, T.M.; Strasser, H.; Helen, E.R.; Fernando, E.V.; Dave, C.; Mark SGoettel, J.P.; Eric, W. Use of Hyphomycetous Fungi for Managing Insect Pests, Fungi as Biocontrol Agents; Springer: Berlin, Germany, 2001; pp. 23–69.
  23. Akello, J.; Sikora, R. Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biol. Control 2012, 61, 215–221.
  24. Greenfield, M.; Gómez-Jiménez, M.I.; Ortiz, V.; Vega, F.E.; Kramer, M.; Parsa, S. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol. Control 2016, 95, 40–48.
  25. Mantzoukas, S.; Chondrogiannis, C.; Grammatikopoulos, G. Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomol. Exp. Appl. 2015, 154, 78–87.
  26. Kang, S.C.; Bark, Y.G.; Lee, D.G.; Kim, Y.H. Antifungal activities of Metarhizium anisopliae against Fusarium oxysporum, Botrytis cinerea, and Alternaria solani. Korean J. Mycol. 1996, 24, 49–55.
  27. Shahid, A.; Rao, Q.; Bakhsh, A.; Husnain, T. Entomopathogenic fungi as biological controllers: New insights into their virulence and pathogenicity. Arch. Biol. Sci. 2012, 64, 21–42.
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