Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
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Entomopathogenic Fungi-mediated Pest Management and R&D Strategy

곤충병원성 진균을 활용한 해충 관리와 개발 전략

  • Lee, Se Jin (Department of Agricultural Life Science, Sunchon National University) ;
  • Shin, Tae Young (Department of Agricultural Biology, Jeonbuk National University) ;
  • Kim, Jong-Cheol (Department of Agricultural Biology, Jeonbuk National University) ;
  • Kim, Jae Su (Department of Agricultural Biology, Jeonbuk National University)
  • 이세진 (국립순천대학교 생명산업과학대학 농생명과학과) ;
  • 신태영 (전북대학교 농업생명과학대학 농생물학과) ;
  • 김종철 (전북대학교 농업생명과학대학 농생물학과) ;
  • 김재수 (전북대학교 농업생명과학대학 농생물학과)
  • Received : 2021.12.29
  • Accepted : 2022.02.21
  • Published : 2022.03.01
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Abstract

Entomopathogenic fungi can be used to control a variety of sucking and chewing insects, with little effect on beneficial insects and natural enemies. Approximately 170 entomopathogenic fungal insecticides have been registered and used worldwide, with the recent focus being on the mode of action and mechanism of insect-fungal interactions. During the initial period of research and development, the industrialization of entomopathogenic fungi focused on the selection of strains with high virulence. However, improvement in productivity, including securing resistance to environmental stressors, is a major issue that needs to be solved. Although conidia are the primary application propagules, efforts are being made to overcome the limitations of blastospores to improve the economic feasibility of the production procedure. Fungal transformation is also being conducted to enhance insecticidal activity, and molecular biology is being used to investigate functions of various genes. In the fungi-based pest management market, global companies are setting up cooperative platforms with specialized biological companies in the form of M&As or partnerships with the aim of implementing a tank-mix strategy by combining chemical pesticides and entomopathogenic fungi. In this regard, understanding insect ecology in the field helps in providing more effective fungal applications in pest management, which can be used complementary to chemicals. In the future, when fungal applications are combined with digital farming technology, above-ground applications to control leaf-dwelling pests will be more effective. Therefore, for practical industrialization, it is necessary to secure clear research data on intellectual property rights.

곤충병원성 진균은 다양한 흡즙형 및 저작형 해충 방제에 적용이 가능하며, 익충과 천적에 낮은 영향을 보여, 화학농약의 대체체로서 관심이 높아지고 있다. 현재까지 전세계적으로 170여개의 제품들이 등록되어 판매되고 있으며, 최근 연구측면에서는 작용기작 및 곤충-진균 상호작용체 구명에 집중하고 있다. 해충 방제를 위한 곤충병원성 진균의 산업화 연구는 초기 살충성이 높은 균주 선발에 집중하였으나, 최근에는 환경 스트레스 인자에 대한 저항성 확보를 포함한 생산성 향상이 해결해야 할 주요 과제이다. 분생포자(conidia)가 주된 처리 형태였지만, 액체배양을 통해 생산되는 아포자(blastospore)의 한계점을 극복하여 대량생산의 경제성을 확보하려는 노력들도 진행되고 있다. 추가로 살충효과를 향상시키기 위해, 형질전환을 비롯한 분자생물학적 연구와 유전자 및 유전체 기능 구명에 집중하고 있다. 해충방제 시장측면에서, 글로벌 작물보호제 기업들은 인수합병 또는 공동 연구개발 형태로 전문 생물농약 기업들과의 협력체계를 구축하고 있으며, 화학농약과 곤충병원성 진균의 tank-mix 전략을 주된 방향성으로 삼고 있다. 현장에서 곤충 생태에 대한 이해를 기반으로 한 생태학적 처리(ecological application)는 곤충병원성 진균의 살충효과를 향상시킬 수 있는 기회가 된다. 앞으로의 디지털팜(digital farming) 기술과 접목된다면, 지상부 해충 방제를 위한 실질적인 적용도 가능하다. 곤충병원성 진균의 산업화를 위해서는 지적재산권 분쟁 해결을 위한 명확한 비교 연구자료 확보도 필요하다. 이와 같은 곤충병원성 진균이 식량생산의 안전성과 경제성을 확보하는 중요한 미생물자원으로 활발히 활용되고 개발되길 기대한다.

Keywords

Acknowledgement

본 연구 성과물(리뷰 논문)은 농촌진흥청 연구사업 (세부과제번호: PJ016297032021)의 지원에 의해 이뤄진 것임.

References

  1. Alkhaibari, A.M., Carolino, A.T., Yavasoglu, S.I., Maffeis, T., Mattoso, T.C., Bull, J.C., Samuels, R.I., Butt, T.M., 2016. Metarhizium brunneum blastospore pathogenesis in Aedes aegypti larvae: attack on several fronts accelerates mortality. PLoS Pathog. 12, e1005715. https://doi.org/10.1371/journal.ppat.1005715
  2. Arthurs, S., Dara, S.K., 2019. Microbial biopesticides for invertebrate pests and their markets in the United States. J. Invertebr. Pathol. 165, 13-21. https://doi.org/10.1016/j.jip.2018.01.008
  3. Avery, P.B., Pick, D.A., Aristizabal, L.F., Kerrigan, J., Powell, C.A., Rogers, M.E., Arthurs, S.P., 2013. Compatibility of Isaria fumosorosea (Hypocreales: Cordycipitaceae) blastospores with agricultural chemicals used for management of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae). Insects 4, 694-711. https://doi.org/10.3390/insects4040694
  4. Beys da Silva, W.O., Santi, L., Correa, A.P., Silva, L.A., Bresciani, F. R., Schrank, A., Vainstein, M.H., 2010. The entomopathogen Metarhizium anisopliae can modulate the secretion of lipolytic enzymes in response to different substrates including components of arthropod cuticle. Fun. Biol. 114, 911-916. https://doi.org/10.1016/j.funbio.2010.08.007
  5. Butt, T.M., Coates, C.J., Dubovskiy, I.M., Ratcliffe, N.A., 2016. Entomopathogenic fungi: new insights into host-pathogen interactions. Adv. Genet. 94, 307-364. https://doi.org/10.1016/bs.adgen.2016.01.006
  6. Chandler, D., 2017. Basic and applied research on entomopathogenic fungi. In: Lacey L.A. (Ed.), Microbial control of insect and mite pests. Academic Press, Amsterdam, pp. 69-89.
  7. Chen, J., Lai, Y., Wang, L., Zhai, S., Zou, G., Zhou, Z., Cui, C., Wang, S., 2017. CRISPR/Cas9-mediated efficient genome editing via blastospore-based transformation in entomopathogenic fungus Beauveria bassiana. Sci. Rep. 7, 1-10. https://doi.org/10.1038/s41598-016-0028-x
  8. Conlon, B.H., Mitchell, J., De Beer, Z.W., Caroe, C., Gilbert, M.T.P., Eilenberg, J., Poulsen, M., Henrik, H., 2017. Draft genome of the fungus-growing termite pathogenic fungus Ophiocordyceps bispora (Ophiocordycipitaceae, Hypocreales, Ascomycota). Data Brief. 11, 537-542. https://doi.org/10.1016/j.dib.2017.02.051
  9. Dara, S.K., 2015. Root aphids and their management in organic celery. CAPCA Advi. 18, 65-70.
  10. Dara, S.K., 2016. IPM solutions for insect pests in California strawberries: efficacy of botanical, chemical, mechanical, and microbial options. CAPCA Advi. 19, 40-46.
  11. Davidson, E.W., 2012. History of insect pathology. In: Vega, F.E., Kaya, H.K. (Eds.), Insect pathology, Elsevier, London, pp. 13-28.
  12. de Bary, A., 1866. Morphologie und Physiologie der Pilze, Flechten und Myxomyceten, Wilhelm Engelmann, Leipzig.
  13. de Faria, M.R., Wraight, S.P., 2007. Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol. control. 43, 237-256. https://doi.org/10.1016/j.biocontrol.2007.08.001
  14. Dietsch, R., Jakobs-Schonwandt, D., Grunberger, A., Patel, A., 2021. Desiccation-tolerant fungal blastospores: from production to application. Curr. Res. Biotechnol. 3, 323-339. https://doi.org/10.1016/j.crbiot.2021.11.005
  15. Ding, J.L., Peng, Y.J., Chu, X.L., Feng, M.G., Ying, S.H., 2018. Autophagy-related gene BbATG11 is indispensable for pexophagy and mitophagy, and contributes to stress response, conidiation and virulence in the insect mycopathogen Beauveria bassiana. Environ. Microbiol. 20, 3309-3324. https://doi.org/10.1111/1462-2920.14329
  16. Engel, M.S., Grimaldi, D.A., 2004. New light shed on the oldest insect. Nature 427, 627-630. https://doi.org/10.1038/nature02291
  17. Fernandes, E.K., Rangel, D.E., Braga, G.U., Roberts, D.W., 2015. Tolerance of entomopathogenic fungi to ultraviolet radiation: a review on screening of strains and their formulation. Curr. Genet. 61, 427-440. https://doi.org/10.1007/s00294-015-0492-z
  18. Gasmi, L., Baek, S., Kim, J.C., Kim, S., Lee, M.R., Park, S.E., Shin, T.Y., Lee, S.J., Parker, B.L., Kim, J.S., 2021. Gene diversity explains variation in biological features of insect killing fungus, Beauveria bassiana. Sci. Report 11, 91. https://doi.org/10.1038/s41598-020-78910-1
  19. Hajek, A.E., 1997. Ecology of terrestrial fungal entomopathogens. In: Jones J.G. (Ed.) Advances in microbial ecology, Springer, Boston, pp. 193-249.
  20. Holder, D.J., Kirkland, B.H., Lewis, M.W., Keyhani, N.O., 2007. Surface characteristics of the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153, 3448-3457. https://doi.org/10.1099/mic.0.2007/008524-0
  21. Holliday, J., Cleaver, M.P., 2008. Medicinal value of the caterpillar fungi species of the genus Cordyceps (Fr.) Link (Ascomycetes). a review. Int. J. Med. Mushrooms 10, 219-234. https://doi.org/10.1615/IntJMedMushr.v10.i3.30
  22. Imoulan, A., Wu, H. J., Lu, W. L., Li, Y., Li, B.B., Yang, R.H., Wang, X.L., Kirk, P.M., Yao, Y.J., 2016. Beauveria medogensis sp. nov., a new fungus of the entomopathogenic genus from China. J. Invertebr. Pathol. 139, 74-81. https://doi.org/10.1016/j.jip.2016.07.006
  23. Jaronski, S.T., Jackson, M.A., 2012. Mass production of entomopathogenic Hypocreales. In: Lacey, L.A. (Ed.) Manual of techniques in invertebrate pathology, Academic Press, San Diego, pp. 257-286.
  24. Jitendra, M., Kiran, D., Ambika, K., Priya, S., Neha, K., Sakshi, D., 2012. Biomass production of entomopathogenic fungi using various agro products in Kota region, India. Int. J. Biol. Sci. 1, 12-16.
  25. Kim, J.C., Baek, S., Park, S.E., Kim, S., Lee, M.R., Jo, M., Im, J.S., Ha, P., Kim, J.S., Shin, T.Y., 2020a. Colonization of Metarhizium anisopliae on the surface of pine tree logs: A promising biocontrol strategy for the Japanese pine sawyer, Monochamus alternatus. Fungal biol. 124, 125-134. https://doi.org/10.1016/j.funbio.2019.12.006
  26. Kim, J.C., Lee, M.R., Kim, S., Lee, S.J., Park, S.E., Baek, S., Gasmi, L., Shin, T.Y., Kim, J.S., 2019. Long-term storage stability of Beauveria bassiana ERL836 granules as fungal biopesticide. J. Asia Pac. Entomol. 22, 537-542. https://doi.org/10.1016/j.aspen.2019.04.001
  27. Kim, J.S., Je, Y.H., Skinner, M., Parker, B.L., 2013. An oil-based formulation of Isaria fumosorosea blastospores for management of greenhousewhitefly Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Pest Manag. Sci. 69, 576-581. https://doi.org/10.1002/ps.3497
  28. Kim, J.S., Kassa, A., Skinner, M., Hata, T., Parker, B.L., 2011. Production of thermotolerant entomopathogenic fungal conidia on millet grain. J. Ind. Microbiol. Biotechnol. 38, 697-704. https://doi.org/10.1007/s10295-010-0850-2
  29. Kim, J.S., Lee, S.J., Skinner, M., Parker, B.L., 2014. A novel approach: Beauveria bassiana granules applied to nursery soil for management of rice water weevils in paddy fields. Pest Manag. Sci. 70, 1186-1191. https://doi.org/10.1002/ps.3817
  30. Kim, S., Kim, J.C., Lee, S.J., Lee, M.R., Park, S.E., Li, D., Baek, S., Shin, T.Y., Kim, J.S., 2020b. Beauveria bassiana ERL836 and JEF-007 with similar virulence show different gene expression when interacting with cuticles of western flower thrips, Frankniella occidentalis. BMC Genomics 21, 836. https://doi.org/10.1186/s12864-020-07253-y
  31. Ko, S.H., Shin, T.Y., Lee, J.Y., Choi, C.J., Woo, S.D., 2021. Screening and evaluation of acaropathogenic fungi against the bulb mite Rhizoglyphus robini. J. Asia Pac. Entomol. 24, 991-996. https://doi.org/10.1016/j.aspen.2021.09.005
  32. Lacey, L.A., Frutos, R., Kaya, H., Vail, P., 2001. Insect pathogens as biological control agents: do they have a future? Biol. control 21, 230-248. https://doi.org/10.1006/bcon.2001.0938
  33. Lacey, L.A., Grzywacz, D., Shapiro-Ilan, D.I., Frutos, R., Brown-bridge, M., Goettel, M.S., 2015. Insect pathogens as biological control agents: back to the future. J. Invertebr. Pathol. 132, 1-41. https://doi.org/10.1016/j.jip.2015.07.009
  34. Lee, J.Y., Woo, R.M., Choi, C.J., Shin, T.Y., Gwak, W.S., Woo, S.D., 2019. Beauveria bassiana for the simultaneous control of Aedes albopictus and Culex pipiens mosquito adults shows high conidia persistence and productivity. AMB Express 9, 1-9. https://doi.org/10.1186/s13568-018-0728-7
  35. Lee, M.R., Kim, J.C., Park, S.E., Lee, S.J., Kim, W.J., Lee, D.H., Kim, J.S., 2021. Interactive gene expression between Metarhizium anisopliae JEF-290 and longhorned tick Haemaphysalis longicornis at early stage of infection. Front. Physiol. 12, 643389. https://doi.org/10.3389/fphys.2021.643389
  36. Lee, M.R., Li, D., Lee, S.J., Kim, J.C., Kim, S., Park, S.E., Baek, S., Shin, T.Y., Lee, D.H., Kim, J.S., 2019. Use of Metarhizum aniopliae sl to control soil-dwelling longhorned tick, Haemaphysalis longicornis. J. Invertebr. Pathol. 166, 107230. https://doi.org/10.1016/j.jip.2019.107230
  37. Lee, S.J., Kim, S., Kim, J.C., Lee, M.R., Hossain, M.S., Shin, T.S., Kim, T.H., Kim, J.S., 2017. Entomopathogenic Beauveria bassiana granules to control soil-dwelling stage of western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae). Biocontrol 62, 639-648. https://doi.org/10.1007/s10526-017-9818-8
  38. Lee, S.J., Lee, M.R., Kim, S., Kim, J.C., Park, S.E., Li, D., Shin, T.Y., Nai, Y.S., Kim. J.S., 2018. Genomic analysis of the insect-killing fungus Beauveria bassiana JEF-007 as a biopesticide. Sci. Report. 8, 12388. https://doi.org/10.1038/s41598-018-30856-1
  39. Lee, W.W., Shin, T.Y., Bae, S.M., Woo, S.D., 2015. Screening and evaluation of entomopathogenic fungi against the green peach aphid, Myzus persicae, using multiple tools. J. Asia Pac. Entomol. 18, 607-615. https://doi.org/10.1016/j.aspen.2015.07.012
  40. Li, D., Park, S.E., Lee, M.R., Kim, J.C., Lee, S.J., Kim, J.S., 2021. Soil application of Beauveria bassiana JEF-350 granules to control melon thrips, Thrips palmi Karny (Thysanoptera: Thripidae). J. Asia-Pacific Entomol. 24, 636-644. https://doi.org/10.1016/j.aspen.2021.05.010
  41. Lohse, R., Jakobs-Schonwandt, D., Vidal, S., Patel, A.V., 2015. Evaluation of new fermentation and formulation strategies for a high endophytic establishment of Beauveria bassiana in oilseed rape plants. Biol. control, 88, 26-36. https://doi.org/10.1016/j.biocontrol.2015.05.002
  42. Lovett, B., St. Leger, R.J., 2017. The insect pathogens. Microbiol. Spectr. 5, 5-2.
  43. Lovett, B., St. Leger, R.J., 2018. Genetically engineering better fungal biopesticides. Pest Manag. Sci. 74, 781-789. https://doi.org/10.1002/ps.4734
  44. Market Research, 2020. Global Beauveria bassiana insecticide market growth (Status and Outlook) 2020-2025, LP Information, Inc., USA. https://www.marketresearch.com/LP-Information-Inc-v4134/Global-Beauveria-Bassiana-Insecticide-Growth-13515169/ (accessed on 22 December, 2020).
  45. Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763-767. https://doi.org/10.1126/science.1257570
  46. Molnar, I., Gibson, D.M., Krasnoff, S.B., 2010. Secondary metabolites from entomopathogenic Hypocrealean fungi. Nat. Prod. Rep. 27, 1241-1275. https://doi.org/10.1039/c001459c
  47. Nishi, O., Sushida, H., Higashi, Y., Iida, Y., 2021. Epiphytic and endophytic colonisation of tomato plants by the entomopathogenic fungus Beauveria bassiana strain GHA. Mycology 12, 39-47. https://doi.org/10.1080/21501203.2019.1707723
  48. Park, S.E., Kim, J.C., Lee, S.J., Lee, M.R., Kim, S., Li, D., Baek, S., Han, J.H., Kim, J.J., Koo, K.B., 2018. Solid cultures of thrips-pathogenic fungi Isaria javanica strains for enhanced conidial productivity and thermotolerance. J. Asia Pac. Entomol. 21, 1102-1109. https://doi.org/10.1016/j.aspen.2018.08.005
  49. Pereira, H., Willeput, R., Detrain, C., 2021. A fungus infected environment does not alter the behaviour of foraging ants. Sci. Rep. 11, 1-13. https://doi.org/10.1038/s41598-020-79139-8
  50. Rana, S., Beer, A., Birkett, R., Pegg, J.R., 2019. Biologicals 2019 - An analysis of corporate, product and regulatory news in 2018/2019. Agrow Agiribusiness Intelligence. https://docplayer.net/136726222-Agribusiness-intelligence-biologicals-an-analysis-of-corporate-product-and-regulatory-developments-in-2018-2019.html (accessed on January, 2021).
  51. Rangel, D.E., Braga, G.U., Fernandes, E.K., Keyser, C.A., Hallsworth, J.E., Roberts, D.W., 2015. Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr. Genet. 61, 383-404. https://doi.org/10.1007/s00294-015-0477-y
  52. Resquin-Romero, G., Garrido-Jurado, I., Delso, C., Rios-Moreno, A., Quesada-Moraga, E., 2016. Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. J. Invertebr. Pathol. 136, 23-31. https://doi.org/10.1016/j.jip.2016.03.003
  53. Ruiu, L., 2018. Microbial biopesticides in agroecosystems. Agronomy 8, 235. https://doi.org/10.3390/agronomy8110235
  54. Santos, M.P., Dias, L.P., Ferreira, P.C., Pasin, L.A., Rangel, D.E., 2011. Cold activity and tolerance of the entomopathogenic fungus Tolypocladium spp. to UV-B irradiation and heat. J. Invertebr. Pathol. 108, 209-213. https://doi.org/10.1016/j.jip.2011.09.001
  55. Sevim, A., Donzelli, B.G., Wu, D., Demirbag, Z., Gibson, D.M., Turgeon, B.G., 2012. Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are differentially expressed and corresponding mutants are decreased in virulence. Curr. Genet. 58, 79-92. https://doi.org/10.1007/s00294-012-0366-6
  56. Shah, P., Pell, J., 2003. Entomopathogenic fungi as biological control agents. Appl. Microbiol. Biotechnol. 61, 413-423. https://doi.org/10.1007/s00253-003-1240-8
  57. Shapiro-Ilan, D.I., Bruck, D.J., Lacey, L.A., 2012. Principles of epizootiology and microbial control. In: Vega, F., Kaya, H.K. (Eds.), Insect pathology. Elsevier, San Diego, pp. 29-72.
  58. Shin, T.Y., Bae, S.M., Kim, D.J., Yun, H.G., Woo, S.D., 2017. Evaluation of virulence, tolerance to environmental factors and antimicrobial activities of entomopathogenic fungi against two-spotted spider mite, Tetranychus urticae. Mycoscience 58, 204-212. https://doi.org/10.1016/j.myc.2017.02.002
  59. Shin, T.Y., Lee, M.R., Park, S.E., Lee, S.J., Kim, W.J., Kim, J.S., 2020. Pathogenesis-related genes of entomopathogenic fungi. Arch. Insect Biochem. Physiol. 105, e21747. https://doi.org/10.1002/arch.21747
  60. Shin, T.Y., Lee, W.W., Ko, S.H., Choi, J.B., Bae, S.M., Choi, J.Y., Lee, K.S., Je, Y.H., Jin, B.R., Woo, S.D., 2013. Distribution and characterisation of entomopathogenic fungi from Korean soils. Biocontrol Sci. Technol. 23, 288-304. https://doi.org/10.1080/09583157.2012.756853
  61. Song, M.H., Yu, J.S., Kim, S., Lee, S.J., Kim, J.C., Nai, Y.S., Shin, T.Y., Kim, J.S., 2019. Downstream processing of Beauveria bassiana and Metarhizium anisopliae-based fungal biopesticides against Riptortus pedestris: solid culture and delivery of conidia. Biocontrol Sci. Technol. 29, 514-532. https://doi.org/10.1080/09583157.2019.1566951
  62. Srinivasan, R., Sevgan, S., Ekesi, S., Tamo, M., 2019. Biopesticide based sustainable pest management for safer production of vegetable legumes and brassicas in Asia and Africa. Pest Manag. Sci. 75, 2446-2454. https://doi.org/10.1002/ps.5480
  63. St Leger, R., Screen, S., 2001. Prospects for strain improvement of fungal pathogens of insects and weeds. In: Butt, T., Jackson, C., Magan, N. (Eds.), Fungi as biocontrol agents: progress, problems and potential. CABI, Walingford, pp. 219-237.
  64. Stork, N.E., 2018. How many species of insects and other terrestrial arthropods are there on Earth?. Annu. Rev. Entomol. 63, 31-45. https://doi.org/10.1146/annurev-ento-020117-043348
  65. Sung, G.H., Poinar Jr, G.O., Spatafora, J.W., 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Mol. Phylogenet. Evol. 49, 495-502. https://doi.org/10.1016/j.ympev.2008.08.028
  66. Valero-Jimenez, C.A., Wiegers, H., Zwaan, B.J., Koenraadt, C.J., van Kan, J.A., 2016. Genes involved in virulence of the entomopathogenic fungus Beauveria bassiana. J. Invertebr. Pathol. 133, 4149.
  67. Vega, F.E., Goettel, M.S., Blackwell, M., Chandler, D., Jackson, M.A., Keller, S., Koike, M., Maniania, N.K., Monzon, A., Ownley, B.H., Pell, J.K., Rangel, D.E.N., Roy, H.E., 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecol. 2, 149-159. https://doi.org/10.1016/j.funeco.2009.05.001
  68. Vega, F.E., Posada, F., Catherine Aime, M., Pava-Ripoll, M., Infante, F., Rehner, S.A., 2008. Entomopathogenic fungal endophytes. Biol. Control. 46, 72-82. https://doi.org/10.1016/j.biocontrol.2008.01.008
  69. Wang, C., St Leger, R.J., 2007. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot. Cell 6, 808-816. https://doi.org/10.1128/EC.00409-06
  70. Wang, C., St. Leger, R.J., 2005. Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot. Cell 4, 937-947. https://doi.org/10.1128/EC.4.5.937-947.2005
  71. Wang, C., Wang, S., 2017. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu. Rev. Entomol. 62, 73-90. https://doi.org/10.1146/annurev-ento-031616-035509
  72. Wei, G., Lai, Y., Wang, G., Chen, H., Li, F., Wang, S., 2017. Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proc. Natl. Acad. Sci. 114, 5994-5999. https://doi.org/10.1073/pnas.1703546114
  73. Xu, C., Zhang, X., Qian, Y., Chen, X., Liu, R., Zeng, G., Zhao, H., Fang, W., 2014. A high-throughput gene disruption methodology for the entomopathogenic fungus Metarhizium robertsii. PLoS ONE 9, e107657. https://doi.org/10.1371/journal.pone.0107657
  74. Yang, Y.T., Lee, S.J., Nai, Y.S., Kim, S., Kim, J.S., 2016. Up-regulation of carbon metabolism-related glyoxylate cycle and toxin production in Beauveria bassiana JEF-007 during infection of bean bug, Riptortus pedestris (Hemiptera: Alydidae). Fun. Biol. 120, 1236-1248. https://doi.org/10.1016/j.funbio.2016.07.008
  75. Yu, J.S., Lee, S.J., Shin, T.Y., Kim, W.J., Kim, J.S., 2020. Enhanced thermotolerance of entomopathogenic Beauveria bassiana and Metarhizium anisopliae JEF-isolates by substrate modification. Int. J. Indus. Entomol. 41, 28-35. https://doi.org/10.7852/IJIE.2020.41.2.28
  76. Zhao, X., Yang, X., Lu, Z., Wang, H., He, Z., Zhou, G., Zhang, Y., 2019. MADS-box transcription factor Mcm1 controls cell cycle, fungal development, cell integrity and virulence in the filamentous insect pathogenic fungus Beauveria bassiana. Environ. Microbiol. 21, 3392-3416. https://doi.org/10.1111/1462-2920.14629
  77. Zimmermann, G., 1993. The entomopathogenic fungus Metarhizium anisopliae and its potential as a biocontrol agent. Pestic. Sci. 37, 375-379. https://doi.org/10.1002/ps.2780370410