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Resistance to fungicides in entomopathogenic fungi: Underlying mechanisms, consequences, and opportunities for progress

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Abstract

Although chemical agents are currently the standard in pest control, entomopathogenic fungi (EPF) are a commercially important biocontrol agent (BCA) and an important long-term alternative to pest extermination. Many agroecosystems around the world rely on EPFs to control arthropod pest populations below economically feasible levels. The complementarity of these BCAs with conventional crop protection measures will make implementation easier. Fungicides are the third most extensively used plant protection chemical in the world, but despite their usefulness in reducing plant pathogenic fungus in a number of agroecosystems, they have major implications for non-targeted EPFs. As a result, combining fungicides with biological controls can impair the efficacy of both. Diverse ways can be used to improve EPF's pesticidal capabilities and reduce the negative effects of fungicides. Fungicides affect the subsequent steps of EPF infection and need strategic augmentation by employing EPF-compatible fungicides, a proper formulation, mutagenesis and artificial selection, and endophytic EPFs in pest management. Developing aggressive and fungicide-tolerant strains of EPFs by conventional and/or genetic approaches can improve the field persistence and efficacy of EPFs in fungicide-treated agro-ecosystems. The current review paper summarises the effect of fungicide on EPF infection stages and techniques to decrease EPF's fungicide sensitivity.

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References

  • Akello J, Dubois T, Coyne D, Kyamanywa S (2008) Effect of endophytic Beauveria bassiana on populations of the banana weevil, Cosmopolites sordidus, and their damage in tissue–cultured banana plants. Entomologia Experimentalis Et Applicata 129:157–165

    Article  Google Scholar 

  • Ali S, Huang Z, Ren S (2013) Effect of fungicides on growth, germination and cuticle-degrading enzyme production by Lecanicillium muscarium. Biocontrol Science and Technology 23:711–723

    Article  Google Scholar 

  • Alves SB, Lecuona RE (1998) Epizootiologia aplicada ao controle microbiano de insetos. In: Alves SB (Ed.) Controle microbiano de insetos (pp. 97–170). Fealq, São Paulo, Brazil

  • Avery PB, Pick DA, Aristizábal LF, Kerrigan J, Powell CA, Rogers ME, Arthurs SP (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

    Article  PubMed  PubMed Central  Google Scholar 

  • Bamisile BS, Akutse KS, Siddiqui JA, Xu Y (2021) Model application of entomopathogenic fungi as alternatives to chemical pesticides: Prospects, challenges, and insights for next-generation sustainable agriculture. Frontiers in Plant Science 12:741804

    Article  PubMed  PubMed Central  Google Scholar 

  • Bandani AR, Esmailpour N (2006). Oil formulation of entomopathogenic fungus, Beauveria Bassiana, against Sunn pest, Eurygaster integriceps puton (Heteroptera: Scutelleridae). Communications in Agricultural and Applied Biological Sciences 2:443–448

  • Batta YA (2003) Production and testing of novel formulations of the entomopathogenic fungus Metarhizium anisopliae (Metschinkoff) Sorokin (Deuteromycotina: Hyphomycetes). Crop Protection 22:415–422

    Article  Google Scholar 

  • Bhoi TK, Samal I, Mahanta DK, Komal J, Jinger D, Sahoo MR, Achary GC, Nayak P, Sunani SK, Saini V, Raghuraman M (2022) Understanding How Silicon Fertilization Impacts Chemical Ecology and Multitrophic Interactions Among Plants, Insects and Beneficial Arthropods. Silicon 16:1–21

    Google Scholar 

  • Bogo MR, Vainstein MH, Aragăo FJ, Rech E, Schrank A (1996) High frequency gene conversion among benomyl resistant transformants in the entomopathgenic fungus Metarhizium anisopliae. FEMS Microbiology Letters 142:123–127

    Article  CAS  PubMed  Google Scholar 

  • Boguś MI, Scheller K (2002) Extraction of an insecticidal protein fraction from the parasitic fungus Conidiobolus coronatus (Entomophthorales). Acta Parasitologica 47:66–72, ISSN 1896–1851

  • Bruck DJ (2009) Impact of fungicides on Metarhizium anisopliae in the rhizosphere, bulk soil and in vitro. BioControl 54:597–606

    Article  CAS  Google Scholar 

  • Campos-Esquivel L, Hanson PE, Escudero-Leyva E, Chaverri P (2022) Virulence of native isolates of entomopathogenic fungi (Hypocreales) against the “sweetpotato whitefly” Bemisia tabaci (Hemiptera: Aleyrodidae), including the effects of temperature and fungicides. Journal of Invertebrate Pathology 192:107787

    Article  PubMed  Google Scholar 

  • Celar FA, Kos K (2020) In vitro compatibility of Beauveria bassiana strain ATCC 74040 with copper fungicides. Journal of Applied Entomology 144:388–395

    Article  CAS  Google Scholar 

  • Celis MT, Garcia-Rubio LH (2008) Characterization of emulsions: A systematic spectroscopy study. Journal of Dispersion Science and Technology 29:20–26

    Article  CAS  Google Scholar 

  • Chandler D, Davidson G (2005) Evaluation of entomopathogenic fungus Metarhizium anisopliae against soil- dwelling stages of cabbage maggot (Diptera: Anthomyiidae) in glasshouse and field experiments and effect of fungicides on fungal activity. Journal of Economic Entomology 98:1856–1862

    Article  CAS  PubMed  Google Scholar 

  • Clifton EH, Jaronski ST, Hodgson EW, Gassmann AJ (2015) Abundance of soil-borne entomopathogenic fungi in organic and conventional fields in the Midwestern USA with an emphasis on the effect of herbicides and fungicides on fungal persistence. PLoS ONE 10:e0133613

    Article  PubMed  PubMed Central  Google Scholar 

  • D’Alessandro CP, Padin S, Urrutia MI, López Lastra CC (2011) Interaction of fungicides with the entomopathogenic fungus Isaria fumosorosea. Biocontrol Science and Technology 21(2):189–197

    Article  Google Scholar 

  • Dara SK (2017) Compatibility of the entomopathogenic fungus Beauveria bassiana with some fungicides used in California strawberry. Open Plant Science Journal 10(1):29–34

    Article  CAS  Google Scholar 

  • de Faria MRd, Wraight SP (2007) Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control 43(3):237–256

    Article  Google Scholar 

  • Demirci F, Muştu M, Bora Kaydan M, Ülgentürk S (2011) Laboratory evaluation of the effectiveness of the entomopathogen; Isaria farinosa, on citrus mealybug, Planococcus citri. Journal of Pest Science 84(3):337–342

    Article  Google Scholar 

  • Dun Y, Feng M, Ying S (2003) Evaluation for enhanced aphidicidal activity of a noval emulsifiable formulation of Beauveria bassiana conidia. Wei Sheng Wu Xue Bao 43:781–787 (Chinese)

    PubMed  Google Scholar 

  • Fiedler Ż, Sosnowska D (2017) Side effects of fungicides and insecticides on entomopathogenic fungi in vitro. Journal of Plant Protection Research 57:355–360

    CAS  Google Scholar 

  • Fitriana Y, Shinohara S, Satoh K, Narumi I, Saito T (2015) Benomyl-resistant Beauveria bassiana (Hypocreales: Clavicipitaceae) mutants induced by ion beams. Applied Entomology and Zoology 50:123–129

    Article  CAS  Google Scholar 

  • Fujimura M, Kamakura T, Inoue H, Inoue S, Yamaguchi I (1992) Sensitivity of Neurospora crassa to benzimidazoles and N-phenylcarbamates: effect of amino acid substitutions at position 198 in β-tubulin. Pesticide Biochemistry and Physiology 44:165–173

    Article  CAS  Google Scholar 

  • Gatarayiha MC, Laing MD, Miller RM (2010) Effects of adjuvant and conidial concentration on the efficacy of Beauveria bassiana for the control of the two spotted spider mite, Tetranychus urticae. Experimental and Applied Acarology 50(3):217–229

    Article  CAS  PubMed  Google Scholar 

  • Goettel MS, Koike M, Kim JJ, Aiuchi D, Shinya R, Brodeur J (2008) Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. Journal of Invertebrate Pathology 98:256–261

  • Gołębiowski M, Urbanek A, Oleszczak A, Dawgul M, Kamysz W, Boguś MI, Stepnowski P (2014) The antifungal activity of fatty acids of all stages of Sarcophaga carnaria L. (Diptera: Sarcophagidae). Microbiological Research 169:279–286

  • Gomes SA, Paula AR, Ribeiro A, Moraes CO, Santos JW, Silva CP, Samuels RI (2015) Neem oil increases the efficiency of the entomopathogenic fungus Metarhizium anisopliae for the control of Aedes aegypti (Diptera: Culicidae) larvae. Parasites and Vectors 8:669

    Article  PubMed  PubMed Central  Google Scholar 

  • Greenfield M, Gómez-Jiménez MI, Ortiz V, Vega FE, Kramer M, Parsa S (2016) Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biological Control: Theory and Applications in Pest Management 95:40–48

    Article  PubMed  Google Scholar 

  • Gul HT, Saeed S, Khan FZA (2014) Entomopathogenic fungi as effective insect pest management tactic: A review. Applied Science Business Economy 1:10–18

    Google Scholar 

  • Hajek AE, St. Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annual Review of Entomology 39:293–322.

  • Hao Y, Shaukat A, Shen M, Ren S, Huang Z (2015) Construction of Isaria fumosorosea blastosporetransforming system by Agrobacterium-mediated transformation with benomyl-resistance gene. Pakistan J Zool 47:943–951

  • Hassan AA (2011) Improvement of antagonism and fungicides tolerance in Iraqi Trichoderma harzianum isolates by UV irradiation. Australian Journal of Basic and Applied Sciences 5:909.e917

    Google Scholar 

  • Hatvani L, Manczinger L, Kredics L, Szekeres A, Antal Z, Vagvolgyi C (2006) Production of Trichoderma strains with pesticide-polyresistance by mutagenesis and protoplast fusion. Ant Leeuw International Journal G 89:387.e393

    Google Scholar 

  • Hedimbi M, Kaaya GP, Singh S, Chimwamurombe PM, Gindin G, Glazer I, Samish M (2008) Protection of Metarhizium anisopliae conidia from ultra-violet radiation and their pathogenicity to Rhipicephalus evertsi evertsi Ticks. Experimental and Applied Acarology 46:149–156

    Article  CAS  PubMed  Google Scholar 

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents. CABI Publishing International, Wallingford UK, pp 23–69

  • Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: Can they promote plant growth? Biocontrol Science and Technology 27:28–41

    Article  Google Scholar 

  • Jackson MA, Dunlap CA, Jaronski ST (2010) Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. BioControl 55:129–145

    Article  Google Scholar 

  • Jaros-Su J, Groden E, Zhang J (1999) Effects of selected fungicides and the timing of fungicide application on Beauveria bassiana-induced mortality of the Colorado potato beetle (Coleoptera: Chrysomelidae). Biological Control 15:259–269

    Article  Google Scholar 

  • Johnson JM, Deepthy KB, Chellappan M (2020) Tolerance of Metarhizium anisopliae Sorokin isolates to selected insecticides and fungicides. Entomon 45:143–148

    Article  Google Scholar 

  • Kassab SO, Loureiro EDS, Rossoni C, Pereira FF, Barbosa RH, Costa DP, Zanuncio JC (2014) Combinations of Metarhizium anisopliae with chemical insecticides and their effectiveness in Mahanarva fimbriolata (Hemiptera: Cercopidae) control on sugarcane. Florida Entomologist 97:146–154

    Article  CAS  Google Scholar 

  • Khun KK, Ash GJ, Stevens MM, Huwer RK, Wilson BA (2021) Compatibility of Metarhizium anisopliae and Beauveria bassiana with insecticides and fungicides used in macadamia production in Australia. Pest Management Science 77:709–718

    Article  CAS  PubMed  Google Scholar 

  • Kidanu S, Hagos L (2020) Research and application of entomopathogenic fungi as pest management option: A review. Environmental Earth Sciences 10:31–39

    Google Scholar 

  • Kim JJ, Song YJ, Han JH, Lee SY (2013) Influence of fungicide on the spore germination and mycelial growth of Beauveria bassiana GHA. Korean Journal of Mycology 41:295–300

    Article  Google Scholar 

  • Klingen I, Haukeland S (2006) The soil as a reservoir for natural enemies of pest insects and mites with emphasis on fungi and nematodes. In: Eilenberg J, Hokkanen HMT (eds) An ecological and societal approach to biological control. Springer, Dordrecht, The Netherlands, pp 145–211

    Chapter  Google Scholar 

  • Kouassi M, Coderre D, Todorova SI (2003) Effects of the timing of applications on the incompatibility of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). Journal of Applied Entomology 127:421–426

    Article  CAS  Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology 132:1–41

    Article  CAS  PubMed  Google Scholar 

  • Lopes RB, Pauli G, Mascarin GM, Faria M (2011) Protection of entomopathogenic conidia against chemical fungicides afforded by an oil-based formulation. Biocontrol Science and Technology 21:125–137

    Article  Google Scholar 

  • Loria R, Galaini S, Roberts DW (1983) Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environmental Entomology 12:1724–1726

    Article  Google Scholar 

  • Mantzoukas S, Chondrogiannis C, Grammatikopoulos G (2015) Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomologia Experimentalis Et Applicata 154:78–87

    Article  Google Scholar 

  • Marzano M, Gallo A, Altomare C (2013) Improvement of biocontrol efficacy of Trichoderma harzianum vs Fusarium oxysporum f sp lycopersici through UV induced tolerance to fusaric acid. Biological Control 67:397–408

    Article  CAS  Google Scholar 

  • Mazza G, Arizza V, Baracchi D, Barzanti GP, Benvenuti C, Francardi V, Cervo R (2011) Antimicrobial activity of the red palm weevil Rhynchophorus ferrugineus. Bulletin of Insectology 64:33–41

    Google Scholar 

  • Miętkiewski RT, Pell JK, Clark SJ (1997) Influence of pesticides use on the natural occurrence of entomopathogenic fungi in arable soils in the UK. Field and laboratory comparisons. Biocontrol Science and Technology 7:565–576

  • Mochi DA, Monteiro AC, De Bortoli SA, Dória HOS, Barbosa JC (2006) Pathogenicity of Metarhizium anisopliae for ceratitis capitata (Wied.) (Diptera: Tephritidae) in soil with different pesticides’. Neotropical Entomology 35:382–389

  • Muştu M, Demirci F, Kaydan MB, Ülgentürk S (2015) Laboratory assay of the effectiveness of the entomopathogenic fungus Isaria farinosa (Holmsk.) Fries (Sordariomycetes: Hypocreales) against the vine mealybug Planococcus ficus (Signoret)(Hemiptera: Pseudococcidae), even under the use of fungicides. International Journal of Pest Management 61:264–271

  • Nelly N, Syahrawati MY, Hamid H, Habazar T, Gusnia DN (2019). Diversity and characterization of entomopathogenic fungi from rhizosphere of maize plants as potential biological control agents. Biodivers J Biol Divers 20:1435–1441

  • Neves PMOJ, Hirose E, Tchujo PT, Moino A Jr (2001) Compatibility of entomopathogenic fungi with neonicotinoid insecticides. Neotropical Entomology 30:263–268

    Article  CAS  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2013) Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 4:357–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Urquiza A, Luo Z, Keyhani NO (2015) Improving mycoinsecticides for insect biological control. Applied Microbiology and Biotechnology 99:1057–1068

    Article  CAS  PubMed  Google Scholar 

  • Paula AR, Ribeiro A, Lemos FJA, Silva CP, Samuels RI (2019) Neem oil increases the persistence of the entomopathogenic fungus Metarhizium anisopliae for the control of Aedes aegypti (Diptera: Culicidae) larvae. Parasites and Vectors 12:163

    Article  PubMed  PubMed Central  Google Scholar 

  • Pelizza SA, Scorsetti AC, Fogel MN, Pacheco-Marino SG, Stenglein SA, Cabello MN, Lange CE (2015) Compatibility between entomopathogenic fungi and biorational insecticides in toxicity against Ronderosia bergi under laboratory conditions. BioControl 60:81–91

    Article  CAS  Google Scholar 

  • Pesticides Global Market Report (2022) https://www.thebusinessresearchcompany.com/report/pesticides-global-market-report

  • Yun HG, Kim DJ, Lee JH, Ma JI, Gwak WS, Woo SD (2017) Comparative evaluation of conidia, blastospores and culture filtrates from entomopathogenic fungi against Tetranychus urticae. International Journal of Industrial Entomology 35:58–62

    Google Scholar 

  • Polar P, Kairo MTK, Moore D, Pegram R, John SA (2005) Comparison of water, oils and emulsifiable adjuvant oils as formulating agents for Metarhizium anisopliae for use in control of Boophilus microplus. Mycopathologia 160:151–157

    Article  CAS  PubMed  Google Scholar 

  • Pu ZL, Li ZZ (1996) Insect mycology. Anhui Publishing House of Science and Technology, Hefei, China, pp 582–591

    Google Scholar 

  • Rajula J, Karthi S, Mumba S, Pittarate S, Thungrabeab M, Krutmuang P (2021) Current status and future prospects of entomopathogenic fungi: a potential source of biopesticides. Recent Adv Microbial Biotechnol 71–98

  • Reddy DS, Chowdary NM (2021) Botanical biopesticide combination concept—A viable option for pest management in organic farming. Egyptian Journal of Biological Pest Control 31:1

    Article  Google Scholar 

  • Roberti R, Righini H, Masetti A, Maini S (2017) Compatibility of Beauveria bassiana with fungicides in vitro and on zucchini plants infested with Trialeurodes vaporariorum. Biological Control 113:39–44

    Article  CAS  Google Scholar 

  • Rodríguez-Gómez D, Loera O, Saucedo-Castañeda G, Viniegra-González G (2009) Substrate inßuence on physiology and virulence of Beauveria bassiana acting on larvae and adults of Tenebrio molitor. World Journal of Microbiology and Biotechnology 25:513–518

    Article  Google Scholar 

  • Rossi-Zalaf LS, Alves SB, Vieira SA (2008) Effect of culture media on virulence of Hirsutella thompsonii (Fischer) (deuteromycetes) to control Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae). Neotrop Entomol 37:312–320

  • Sain SK, Monga D, Kumar R, Nagrale DT, Hiremani NS, Kranthi S (2019) Compatibility of entomopathogenic fungi with insecticides and their efficacy for IPM of Bemisia tabaci in cotton. Journal of Pesticide Science 44:97–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samal I, Bhoi TK, Majhi PK, Murmu S, Pradhan AK, Kumar D, Saini V, Paschapur AU, Raj MN, Ankur MS, Behera PP, Mahanta DK, Komal J, Alam P, Balawi TA (2023) Combatting insects mediated biotic stress through plant associated endophytic entomopathogenic fungi in horticultural crops. Frontiers in Plant Science 13:1098673

    Article  PubMed  PubMed Central  Google Scholar 

  • Samson PR, Milner RJ, Sander ED, Bullard GK (2005) Effect of fungicides and insecticides applied during planning of sugarcane on viability of Metarhizium anisopliae and its efficacy against white grubs. BioControl 50:151–163

    Article  CAS  Google Scholar 

  • Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM (2009) Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocontrol Science and Technology 19:743–753

    Article  Google Scholar 

  • Shapiro-Ilan DI, Reilly CC, Hotchkiss MW, Wood BW (2002) The potential for enhanced fungicide resistance in Beauveria bassiana through strain discovery and artificial selection. Journal of Invertebrate Pathology 81:86–93

    Article  CAS  PubMed  Google Scholar 

  • Shapiro-Ilan DI, Reilly CC, Hotchkiss MW, Wood BW (2011) Comparative impact of artificial selection for fungicide resistance on Beauveria bassiana and Metarhizium brunneum. Environmental Entomology 40:59–65

    Article  PubMed  Google Scholar 

  • Sharma A, Kumar V, Shahzad B, Tanveer M, Sidhu GPS, Handa N, Thukral AK (2019) Worldwide pesticide usage and its impacts on ecosystem. SN Applied Sciences 1:1446

    Article  CAS  Google Scholar 

  • Shoeb MA, Solaiman RHA, Abd-Elgyed AA, Ahmed MM (2021) Compatibility of entomopathogenic fungi, Beauvaria bassiana (Bals.-Criv.) Vuill. and Metarhizium anisopliae (Metchn) Sorokin isolates with different agrochemicals commonly used in vineyards. Egyptian Academic Journal of Biological Sciences à Entomology 14:37–53

  • Silva RAd, Quintela ED, Mascarin GM, Barrigossi JAF, Lião LM (2013) Compatibility of conventional agrochemicals used in rice crops with the entomopathogenic fungus Metarhizium anisopliae. Scientia Agricola 70:152–160

    Article  Google Scholar 

  • Song TT, Ying SH, Feng MG (2012) High resistance of Isaria fumosorosea to carbendazim arises from the overexpression of an ATP-binding cassette transporter (ifT1) rather than tubulin mutation. Journal of Applied Microbiology 112:175–184

    Article  CAS  PubMed  Google Scholar 

  • Song ZY, Jin XF, Zhang WT, Zong ZF (2011) Improvement of fungicide resistance to nonpathogenic Fusarium oxysporum strain Fo47 by protoplast fusion. Acta Agriculturae Boreali-Occidentalis Sinica 20:170.e173

    Google Scholar 

  • Tkaczuk C, Harasimiuk M, Król A, Bereś PK (2015) The effect of selected pesticides on the growth of entomopathogenic fungi Hirsutella nodulosa and Beauveria bassiana. Journal of Ecological Engineering 16:177–183. Retrieved from https://doi.org/10.12911/22998993/2952

  • Tkaczuk C, Krzyczkowski T, Głuszczak B, Król A (2012) Wpływ wybranych środków ochrony roślin na wzrost kolonii i kiełkowanie zarodników owadobójczego grzyba Beauveria bassiana (Bals.) Vuill. [The influence of selected pesticides on the colony growth and conidial germination of the entomopathogenic fungus Beauveria bassiana (Bals.) Vuill]. Progress in Plant Protection 52:969–974. (in Polish)

  • Usha J, Babu MN, Padmaja V (2014) Detection of compatibilty of entomopathogenic fungus Beauveria bassiana (bals.) Vuill. With pesticides, fungicides and botanicals. International Journal of Plant and Animal Enviroment Science 4:613–624

  • Valadares-Inglis MC, Inglis PW (1997) Transformation of the entomopathogenic fungus, Metarhizium flavoviride strain CG423 to benomyl resistance. FEMS Microbiology Letters 155:199–202

    Article  CAS  Google Scholar 

  • Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S (2009) Fungal entomopathogens: New insights on their ecology. Fungal Ecology 2:149–159

    Article  Google Scholar 

  • Wu S, Toews MD, Oliveira-Hofman C, Behle RW, Simmons AM, Shapiro-Ilan DI (2020) Environmental tolerance of entomopathogenic fungi: A new strain of Cordyceps javanica isolated from a whitefly epizootic versus commercial fungal strains. Insects 11:711

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie M, Li Q, Hu XP, Zhang YJ, Peng DL, Li Q, Zhang ZR (2018) Improvement of the propamocarb-tolerance of Lecanicillium lecanii through UV-light radiation-based mutagenesis. Crop Protection 103:81–86

    Article  CAS  Google Scholar 

  • Yang C, Hamel C, Vujanovic V, Gan Y (2011) Fungicide: modes of action and possible impact on nontarget microorganisms. ISRN Ecol 2011:1–8

  • Yin Y, Miao J, Shao W, Liu X, Zhao Y, Ma Z (2023) Fungicide resistance: progress in understanding mechanism, monitoring, and management. Phytopathology® 113(4):707–718

  • Zhai XM, Zhang YJ, Xie M (2013) Effects of ten common pesticides on conidial germination, mycelial growth and sporulation of Verticillium lecanii. Chinese Journal of Biological Control 29:227–231

    Google Scholar 

  • Zhang J, Jin K, Xia Y (2017) Contributions of β-tubulin to cellular morphology, sporulation and virulence in the insect-fungal pathogen, Metarhizium acridum. Fungal Genetics and Biology: FG and B 103:16–24

    Article  CAS  PubMed  Google Scholar 

  • Zhang YJ, Zhao JJ, Xie M, Peng DL (2014) Agrobacterium tumefaciens-mediated transformation in the entomopathogenic fungus Lecanicillium lecanii and development of benzimidazole fungicide resistant strains. Journal of Microbiological Methods 105:168–173

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Lovett B, Fang W (2016) Genetically engineering entomopathogenic fungi. Advances in Genetics 94:137–163

    Article  CAS  PubMed  Google Scholar 

  • Zhou MG, Ye ZY, Liu JF (1994) Progress of fungicide resistance. Journal of Nanjing Agricultural University 17:33–41

    CAS  Google Scholar 

  • Zou G, Ying SH, Shen ZC, Feng MG (2006) Multi-sited mutations of beta-tubulin are involved in benzimidazole resistance and thermotolerance of fungal biocontrol agent Beauveria bassiana. Environmental Microbiology 8:2096–2105

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. ICAR-National Research Centre on Litchi, 842002, Bihar, Muzaffarpur, India

    Ipsita Samal

  2. ICFRE-Arid Forest Research Institute (ICFRE-AFRI), Jodhpur, Rajasthan, India, 342005

    Tanmaya Kumar Bhoi, Vipula Vyas & Sangeeta Singh

  3. Odisha University of Agriculture and Technology (OUAT), 751003, Odisha, Bhubaneswar, India

    Prasanta Kumar Majhi

  4. Dr. Rajendra Prasad Central Agricultural University, 848125, Bihar, India

    Deepak Kumar Mahanta

  5. Navsari Agriculture University, Navsari, Gujarat, India, 396450

    J. Komal

  6. University of Agricultural Sciences, Bengaluru, Karnataka, India, 560065

    P. V Dinesh Kumar

  7. ICAR-National Centre for Integrated Pest Management, 110068, New Delhi, India

    Licon Kumar Acharya

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  1. Ipsita Samal
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Contributions

IS, TKB, PKM, VV, DKM: conceptualization, writing original draft preparation, preparation of tables and supervision; JK, SS, PVDK, LKA: preparation of figures, supervision, review and editing. All authors read and approved the manuscript.

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Correspondence to Ipsita Samal or Tanmaya Kumar Bhoi.

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Ipsita Samal, Tanmaya Kumar Bhoi these authors contributed equally to this work And both should be considered as co-first authors.

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Samal, I., Bhoi, T.K., Vyas, V. et al. Resistance to fungicides in entomopathogenic fungi: Underlying mechanisms, consequences, and opportunities for progress. Trop. plant pathol. 49, 5–17 (2024). https://doi.org/10.1007/s40858-023-00585-6

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