Abstract
Plant pathogens with their abundance are harmful and cause huge damage to different agricultural crops and economy of a country as well as lead towards the shortage of food for humans. For their management, the utilization of entomopathogenic fungi is an eco-friendly technique, sustainable to the environment, safe for humans and has promising effect over chemical-based pesticides. This process requires a biochemical mechanism, including the production of enzymes, toxins, and other metabolites that facilitate host infection and invasion. Essential enzymes such as chitinase, proteinase, and lipase play a direct role in breaking down the host cuticle, the primary barrier to EPF (Entomopathogenic Fungi) infection. Additionally, secondary metabolites such as destruxins in Metarhizium, beauvericin in Beauveria, hirsutellides in Hirsutella, isarolides in Isaria, cordyols in Cordyceps, and vertihemipterins in Verticillium, among others, act both directly and indirectly to disable the defense mechanisms of insect hosts, thereby accelerating the EPF infection process. The chemical composition of these secondary metabolites varies, ranging from simple non-peptide pigments such as oosporine to highly complex piperazine derivatives such as vertihemiptellides. The biocontrol efficacy of EPF is extensively studied, with numerous fungal strains commercially available on a large scale for managing arthropod pests. This review emphasizes the role of proteins and enzymes against crop pathogens, detailing their mode of action, and describing the metabolites from entomopathogenic fungi and their biological activities. In doing so, these findings contribute to establishing a symbiotic equilibrium between agricultural productivity and environmental conservation.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Any data related to this manuscript can be accessed on reasonable request to corresponding author.
References
Abd El-Wahab ASED, Nada MS, El- MA, Galal A, Amin HA (2023) Effect of the entomopathogenic fungus, Beauveria bassiana inhibiting whitefly transmission of squash leaf curl virus infecting squash. Egypt J Biol Pest Control 33(1):64. https://doi.org/10.1186/s41938-023-00694
Abdellaoui K, Miladi M, Mkhinini M, Boughattas I, Hamouda AB, Hajji-Hedfi L, Acheuk F (2020) The aggregation pheromone phenylacetonitrile: joint action with the entomopathogenic fungus Metarhizium anisopliae var. acridum and physiological and transcriptomic effects on Schistocerca gregaria nymphs. Pesticide Biochem Physiol 167:104594
Abdelsattar AM, Elsayed A, El-Esawi MA, Heikal YM (2023) Enhancing Stevia rebaudiana growth and yield through exploring beneficial plant-microbe interactions and their impact on the underlying mechanisms and crop sustainability. Plant Physiol Biochem 198:107673
Ahsan H, Islam SU, Ahmed MB, Lee YS, Sonn JK (2020) Significance of green synthetic chemistry from a pharmaceutical perspective. Curr Pharm Des 26(45):5767–5782
Ajvad FT, Madadi H, Michaud JP, Zafari D, Khanjani M (2020) Combined applications of an entomopathogenic fungus and a predatory mite to control fungus gnats (Diptera: Sciaridae) in mushroom production. Biol Control 141:104101. https://doi.org/10.1016/j.biocontrol.2019.104101
Akram S, Ahmed A, He P, He P, Liu Y, Wu Y, He Y (2023) Uniting the role of endophytic fungi against plant pathogens and their interaction. J Fungus 9(1):72. https://doi.org/10.3390/jof9010072
Al Khoury C, Nemer N, Bernigaud C, Fischer K, Guillot J (2021) First evidence of the activity of an entomopathogenic fungus against the eggs of Sarcoptes scabiei. Vet Parasitol 298:109553
Al Khoury C, Bashir Z, Tokajian S, Nemer N, Merhi G, Nemer G (2022) In silico evidence of beauvericin antiviral activity against SARS-CoV-2. Comput Biol Med 141:105171. https://doi.org/10.1016/j.compbiomed.2021.105171
Altinok HH, Altinok MA, Koca AS (2019) Modes of action of entomopathogenic fungi. Curr Trends Nat Sci 8(16):117–124
Alves EA, Schmaltz S, Tres MV, Zabot GL, Kuhn RC, Mazutti MA (2020) Process development to obtain a cocktail containing cell-wall degrading enzymes with insecticidal activity from Beauveria bassiana. Biochem Eng J 156:107484. https://doi.org/10.1016/j.bej.2019.107484
Amobonye A, Bhagwat P, Singh S, Pillai S (2021) Enhanced xylanase and endoglucanase production from Beauveria bassiana SAN01, an entomopathogenic fungal endophyte. Fungal Biol 125(1):39–48. https://doi.org/10.1016/j.funbio.2020.10.003
Andrioli WJ, Lopes AA, Cavalcanti BC, Pessoa C, Nanayakkara NPD, Bastos JK (2017) Isolation and characterization of 2-pyridone alkaloids and alloxazines from Beauveria bassiana. Nat Prod Res 31(16):1920–1929. https://doi.org/10.1080/14786419.2016.1269091
Arunthirumeni M, Vinitha G, Shivakumar MS (2023) Antifeedant and larvicidal activity of bioactive compounds isolated from entomopathogenic fungi Penicillium sp. for the control of agricultural and medically important insect pest (Spodoptera litura and Culex quinquefasciatus). Parasitol Int 92:102688
Awan UA, **a S, Meng L, Raza MF, Zhang Z, Zhang H (2021) Isolation, characterization, culturing, and formulation of a new Beauveria bassiana fungus against Diaphorina citri. Biol Control 158:104586
Ayudya DR, Herlinda S, Suwandi S (2019) Insecticidal activity of culture filtrates from liquid medium of Beauveria bassiana isolates from South Sumatra (Indonesia) wetland soil against larvae of Spodoptera litura. Biodiversitas J Biol Diversity. https://doi.org/10.13057/biodiv/d200802
Baja F, Poitevin CG, Araujo ES, Mirás-Avalos JM, Zawadneak MA, Pimentel IC (2020) Infection of Beauveria bassiana and Cordyceps javanica on different immature stages of Duponchelia fovealis Zeller (Lepidoptera: Crambidae). Crop Prot 138:105347. https://doi.org/10.1016/j.cropro.2020.105347
Bamisile BS, Siddiqui JA, Akutse KS, Ramos Aguila LC, Xu Y (2021) General limitations to endophytic entomopathogenic fungi use as plant growth promoters, pests and pathogens biocontrol agents. Plants 10(10):2119
Batool, R., Umer, M. J., Wang, Y., He, K., Zhang, T., Bai, S., Wang, Z. 2020. Synergistic effect of Beauveria bassiana and Trichoderma asperellum to induce maize (Zea mays L.) defense against the Asian corn borer, Ostrinia furnacalis (Lepidoptera, Crambidae) and larval immune response. Int. J Mol Sci. 21(21), 8215. https://doi.org/10.3390/ijms21218215.
Bava R, Castagna F, Piras C, Musolino V, Lupia C, Palma E, Musella V (2022) Entomopathogenic fungi for pests and predators’ control in beekee**. Vet Sci 9(2):95. https://doi.org/10.3390/vetsci9020095
Bayman P, Mariño YA, García-Rodríguez NM, Oduardo-Sierra OF, Rehner SA (2021) Local isolates of Beauveria bassiana for control of the coffee berry borer Hypothenemus hampei in Puerto rico: virulence, efficacy and persistence. Biol Control 155:104533. https://doi.org/10.1016/j.biocontrol.2021.104533
Bhadani RV, Gajera HP, Hirpara DG, Kachhadiya HJ, Dave RA (2021) Metabolomics of extracellular compounds and parasitic enzymes of Beauveria bassiana associated with biological control of whiteflies (Bemisia tabaci). Pestic Biochem Phys 176:104877. https://doi.org/10.1016/j.pestbp.2021.104877
Bihal R, Al-Khayri JM, Banu AN, Kudesia N, Ahmed FK, Sarkar R, Abd-Elsalam KA (2023) Entomopathogenic fungi: an eco-friendly synthesis of sustainable nanoparticles and their nanopesticide properties. Microorganisms 11(6):1617. https://doi.org/10.3390/microorganisms11061617
Bitencourt RDOB, dos Santos Mallet JR, Mesquita E, Gôlo PS, Fiorotti J, Bittencourt VREP, da Costa Angelo I (2021) Larvicidal activity, route of interaction and ultrastructural changes in Aedes aegypti exposed to entomopathogenic fungi. Acta Trop 213:105732. https://doi.org/10.1016/j.actatropica.2020.105732
Bitencourt RDOB, de Souza Faria F, Marchesini P, dos Santos-Mallet JR, Camargo MG, Bittencourt VREP, da Costa Angelo I (2022) Entomopathogenic fungi and Schinus molle essential oil: the combination of two eco-friendly agents against Aedes aegypti larvae. J Invertebr Pathol 194:107827. https://doi.org/10.1016/j.jip.2022.107827
Boguś MI, Czygier M, Gołębiowski M, Kędra E, Kucińska J, Mazgajska J, Włóka E (2010) Effects of insect cuticular fatty acids on in vitro growth and pathogenicity of the entomopathogenic fungus Conidiobolus coronatus. Exp Parasitol 125(4):400–408
Boni SB, Mwashimaha RA, Mlowe N, Sotelo-Cardona P, Nordey T (2021) Efficacy of indigenous entomopathogenic fungi against the black aphid, Aphis fabae Scopoli under controlled conditions in Tanzania. Int J Trop Insect Sci 41:1643–1651. https://doi.org/10.1007/s42690-020-00365-8
Bordalo MD, Gravato C, Beleza S, Campos D, Lopes I, Pestana JLT (2020) Lethal and sublethal toxicity assessment of Bacillus thuringiensis var. israelensis and Beauveria bassiana based bioinsecticides to the aquatic insect Chironomus riparius. Sci. Total Environ. 698:134155. https://doi.org/10.1016/j.scitotenv.2019.134155
Branine M, Bazzicalupo A, Branco S (2019) Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog 15(7):e1007831. https://doi.org/10.1371/journal.ppat.1007831
Cafarchia C, Pellegrino R, Romano V, Friuli M, Demitri C, Pombi M, Otranto D (2022) Delivery and effectiveness of entomopathogenic fungi for mosquito and tick control: current knowledge and research challenges. Acta Trop. https://doi.org/10.1016/j.actatropica.2022.106627
Canassa F, Tall S, Moral RA, de Lara IA, Delalibera I Jr, Meyling NV (2019) Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites. Biol Control 132:199–208. https://doi.org/10.1016/j.biocontrol.2019.02.003
Carollo CA, Calil ALA, Schiave LA, Guaratini T, Roberts DW, Lopes NP, Braga GU (2010) Fungal tyrosine betaine, a novel secondary metabolite from conidia of entomopathogenic Metarhizium spp. fungi. Fungal Biol 114(5–6):473–480
Chairin T, Petcharat V (2017) Induction of defense responses in longkong fruit (Aglaia dookkoo Griff.) against fruit rot fungi by Metarhizium guizhouense. Biol Control 111:40–44. https://doi.org/10.1016/j.biocontrol.2017.05.012
Chen W, Modi D, Picot A (2023) Soil and phytomicrobiome for plant disease suppression and management under climate change: a review. Plants 12(14):2736. https://doi.org/10.3390/plants12142736
Coutinho-Rodrigues CJB, da Rosa RL, de Freitas MC, Fiorotti J, Berger M, Santi L, Bittencourt VREP (2021) Exposure to a sublethal menadione concentration modifies the mycelial secretome and conidial enzyme activities of Metarhizium anisopliae sensu lato and increases its virulence against Rhipicephalus microplus. Microbiol Res 248:126753. https://doi.org/10.1016/j.micres.2021.126753
Crespo R, Pedrini N, Juárez MP, Dal Bello GM (2008) Volatile organic compounds released by the entomopathogenic fungus Beauveria bassiana. Microbiol Res 163(2):148–151. https://doi.org/10.1016/j.micres.2006.03.013
Da Costa Stuart AK, Furuie JL, Zawadneak MAC, Pimentel IC (2020) Increased mortality of the European pepper moth Duponchelia fovealis (Lepidoptera: Crambidae) using entomopathogenic fungal consortia. J Invertebr Pathol 177:107503. https://doi.org/10.1016/j.jip.2020.107503
Da Rocha IU, Bitencourt RDOB, de Moraes Freitas A, Moreira HVS, de Amorim Magalhães KL, Augusto B, da Costa Angelo I (2024) Exploiting the combination of entomopathogenic fungi and Illicium verum essential oil against Aedes aegypti larvae. Biol Control 193:105526
de Freitas GS, de Araújo Lira V, Jumbo LOV, dos Santos FJ, Rêgo AS, Teodoro AV (2021) The potential of Beauveria bassiana to control Raoiella indica (Acari: Tenuipalpidae) and its compatibility with predatory mites. Crop Prot 149:105776. https://doi.org/10.1016/j.cropro.2021.105776
Diao H, **ng P, Tian J, Han Z, Wang D, **ang H, Ma R (2022) Toxicity of crude toxin protein produced by Cordyceps fumosorosea IF-1106 against Myzus persicae (Sulze). J Invertebr Pathol 194:107825. https://doi.org/10.1016/j.jip.2022.107825
Ding BY, Niu J, Shang F, Yang L, Zhang W, Smagghe G, Wang JJ (2020) Parental silencing of a horizontally transferred carotenoid desaturase gene causes a reduction of red pigment and fitness in the pea aphid. Pest Manag Sci 76(7):2423–2433
Durán-Aranguren D, Chiriví-Salomón JS, Anaya L, Durán-Sequeda D, Cruz LJ, Serrano JD, Sierra R (2020) Effect of bioactive compounds extracted from Cordyceps nidus ANDES-F1080 on laccase activity of Pleurotus ostreatus ANDES-F515. Biotechnol Rep 26:e00466. https://doi.org/10.1016/j.btre.2020.e00466
Eski A, Biryol S, Acici O, Demir İ (2022) Biocontrol of the western conifer seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) using indigenous entomopathogenic fungi. Egyptian J Biol Pest Control 32(1):140
Espinoza F, Vidal S, Rautenbach F, Lewu F, Nchu F (2019) Effects of Beauveria bassiana (Hypocreales) on plant growth and secondary metabolites of extracts of hydroponically cultivated chive (Allium schoenoprasum L. [Amaryllidaceae]). Heliyon. https://doi.org/10.1016/j.heliyon.2019.e03038
Fabelico FL (2015) The phytochemical and antimicrobial properties of entomopathogenic fungi in Nueva Vizcaya, Philippines Asia. Pac J Multidisciplinary Res 3:126–133
Fan Z, Wang L, Qin Y, Li P (2023) Activity of chitin/chitosan/chitosan oligosaccharide against plant pathogenic nematodes and potential modes of application in agriculture: a review. Carbohydr Polym. https://doi.org/10.1016/j.carbpol.2023.120592
Farooq M, Freed S (2018) Insecticidal activity of toxic crude proteins secreted by entomopathogenic fungi against Musca domestica L. (Diptera: Muscidae). Kuwait J Sci 45(2):64–74
Fingu-Mabola JC, Bawin T, Francis F (2021) Direct and indirect effect via endophytism of entomopathogenic fungi on the fitness of Myzus persicae and its ability to spread PLRV on tobacco. Insects 12(2):89. https://doi.org/10.3390/insects12020089
Friuli M, Pellegrino R, Lamanna L, Nitti P, Madaghiele M, Demitri C (2023) Materials engineering to help pest control: a narrative overview of biopolymer-based entomopathogenic fungi formulations. Journal of Fungi 9(9):918
Fuguet R, Vey A (2004) Comparative analysis of the production of insecticidal and melanizing macromolecules by strains of Beauveria spp.: in vivo studies. J. Invertebr. Pathol 85(3):152–167. https://doi.org/10.1016/j.jip.2004.03.001
Gava CAT, da Silva JC, Simoes WL, Paranhos BAJ (2021) Impact of soil texture on conidia movement and residual effect of entomopathogenic fungi applied through irrigation to control fruit-fly pupae in mango orchards. Biol Control 163:104559. https://doi.org/10.1016/j.biocontrol.2021.104559
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. J Invertebr Pathol 98(3):256–261
Golzan SR, Talaei-Hassanloui R, Homayoonzadeh M, Safavi SA (2023) Role of cuticle-degrading enzymes of Beauveria bassiana and Metarhizium anisopliae in virulence on Plodia interpunctella (Lepidoptera, Pyralidae) larvae. J Asia-Pacific Entomol 26(2):102038
Gonzalez-Guzman A, Raya-Diaz S, Sacristán D, Yousef M, Sánchez-Rodríguez AR, Barrón V, Torrent J (2021) Effects of entomopathogenic fungi on durum wheat nutrition and growth in the field. Eur J Agron 128:126282. https://doi.org/10.1016/j.eja.2021.126282
González-Pérez E, Ortega-Amaro MA, Bautista E, Delgado-Sánchez P, Jiménez-Bremont JF (2022) The entomopathogenic fungus Metarhizium anisopliae enhances Arabidopsis, tomato, and maize plant growth. Plant Physiol Biochem 176:34–43. https://doi.org/10.1016/j.plaphy.2022.02.008
Görg LM, Eilenberg J, Jensen AB, Jensen AH, Gross J (2021) Pathogenicity against hemipteran vector insects of a novel insect pathogenic fungus from Entomophthorales (Pandora sp. nov. inedit.) with potential for biological control. J Invertebr Pathol 183:107621. https://doi.org/10.1016/j.jip.2021.107621
Gu CX, Zhang BL, Bai WW, Liu J, Zhou W, Ling ZQ, Wan YJ (2020) Characterization of the endothiapepsin-like protein in the entomopathogenic fungus Beauveria bassiana and its virulence effect on the silkworm, Bombyx mori. J Invertebr Pathol 169:107277. https://doi.org/10.1016/j.jip.2019.107277
Gupta R, Leibman-Markus M, Anand G, Rav-David D, Yermiyahu U, Elad Y, Bar M (2022) Nutrient elements promote disease resistance in tomato by differentially activating immune pathways. Phytopathology® 112(11):2360–2371
Hanan A, Basit A, Nazir T, Majeed MZ, Qiu D (2020) Anti-insect activity of a partially purified protein derived from the entomopathogenic fungus Lecanicillium lecanii (Zimmermann) and its putative role in a tomato defense mechanism against green peach aphid. J Invertebr Pathol 170:107282. https://doi.org/10.1016/j.jip.2019.107282
Heo I, Kim S, Han GH, Im S, Kim JW, Hwang D, Shin TY (2023) Characteristics of insecticidal substances from the entomopathogenic fungus Metarhizium **haense 15R against cotton aphid in Korea. J Asia Pac Entomol 26(1):102013. https://doi.org/10.1016/j.parint.2022.102688
Hong S, Shang J, Sun Y, Tang G, Wang C (2023) Fungal infection of insects: molecular insights and prospects. Trends Microbiol. https://doi.org/10.1016/j.tim.2023.09.005
Hou Q, Xu L, Liu G, Pang X, Wang X, Zhang Y, Liang R (2019) Plant-mediated gene silencing of an essential olfactory-related Gqα gene enhances resistance to grain aphid in common wheat in greenhouse and field. Pest Manag Sci 75(6):1718–1725
Hummadi EH, Dearden A, Generalovic T, Clunie B, Harrott A, Cetin Y, Butt T (2021) Volatile organic compounds of Metarhizium brunneum influence the efficacy of entomopathogenic nematodes in insect control. Biol Control 155:104527. https://doi.org/10.1016/j.biocontrol.2020.104527
Ishidoh KI, Kinoshita H, Igarashi Y, Ihara F, Nihira T (2014) Cyclic lipodepsipeptides verlamelin A and B, isolated from entomopathogenic fungus Lecanicillium sp. J Antibiot 67(6):459–463
Islam W, Adnan M, Shabbir A, Naveed H, Abubakar YS, Qasim M, Ali H (2021) Insect-fungal-interactions: a detailed review on entomopathogenic fungi pathogenicity to combat insect pests. Microb Pathog 159:105122. https://doi.org/10.1016/j.micpath.2021.105122
Jaber LR, Araj SE (2018) Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biol Control 116:53–61. https://doi.org/10.1016/j.biocontrol.2017.04.005
Jaronski ST (2023) Mass production of entomopathogenic fungi—state of the art. Mass Prod Beneficial Organ. https://doi.org/10.1016/B978-0-12-822106-8.00017-8
Karabörklü S, Aydınlı V, Dura O (2022) The potential of Beauveria bassiana and Metarhizium anisopliae in controlling the root-knot nematode Meloidogyne incognita in tomato and cucumber. J Asia-Pacific Entomol 25(1):101846
Karthi S, Vasantha-Srinivasan P, Senthil-Nathan S, Han YS, Shivakumar MS, Murali-Baskaran RK, Malafaia G (2024) Entomopathogenic fungi promising biocontrol agents for managing lepidopteran pests: Review of current knowledge. Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2024.103146
Keshmirshekan A, de Souza Mesquita LM, Ventura SP (2024) Biocontrol manufacturing and agricultural applications of Bacillus velezensis. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2024.02.003
Khan A, Khan A, Ali A, Fatima S, Siddiqui MA (2023) Root-Knot Nematodes (Meloidogyne spp.): biology plant-nematode interactions and their environmentally benign management strategies. Gesunde Pflanzen. https://doi.org/10.1007/s10343-023-00886
Khoja S, Eltayef KM, Baxter I, Myrta A, Bull JC, Butt T (2021) Volatiles of the entomopathogenic fungus, Metarhizium brunneum, attract and kill plant parasitic nematodes. Biol Control 152:104472. https://doi.org/10.1016/j.biocontrol.2020.104472
Khun KK, Ash GJ, Stevens MM, Huwer RK, Wilson BA (2020) Response of the macadamia seed weevil Kuschelorhynchus macadamiae (Coleoptera: Curculionidae) to Metarhizium anisopliae and Beauveria bassiana in laboratory bioassays. J Invertebr Pathol 174:107437. https://doi.org/10.1016/j.jip.2020.107437
Kim JJ, Goettel MS, Gillespie DR (2007) Potential of Lecanicillium species for dual microbial control of aphids and the cucumber powdery mildew fungus. Sphaerotheca Fuliginea Biological Control 40(3):327–332
Kim JS, Roh JY, Choi JY, Wang Y, Shim HJ, Je YH (2010) Correlation of the aphicidal activity of Beauveria bassiana SFB-205 supernatant with enzymes. Fungal Biol 114(1):120–128
Kim JC, Lee SJ, Kim S, Lee MR, Baek S, Park SE, Kim JS (2020) Management of pine wilt disease vectoring Monochamus alternatus adults using spray and soil application of Metarhizium anisopliae JEF isolates. J Asia Pac Entomol 23(1):224–233. https://doi.org/10.1016/j.aspen.2019.12.012
Kirubakaran SA, Abdel-Megeed A, Senthil-Nathan S (2018) Virulence of selected indigenous Metarhizium **shaense (Ascomycota: Hypocreales) isolates against the rice leaffolder, Cnaphalocrocis medinalis (Guenèe) (Lepidoptera: Pyralidae). Physiol Mol Plant Pathol 101:105–115. https://doi.org/10.1016/j.pmpp.2017.06.004
Klieber J, Reineke A (2016) The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. J Appl Entomol 140(8):580–589. https://doi.org/10.1111/jen.12287
Koodalingam A, Dayanidhi MK (2021) Studies on biochemical and synergistic effects of immunosuppressive concentration of imidacloprid with Beauveria bassiana and Metarhizium anisopliae for enhancement of virulence against vector mosquito Culex quinquefasciatus. Pestic Biochem Physiol 176:104882
Koppenhöfer AM, Kostromytska OS, Ebssa L (2022) Species combinations, split applications, and syringing to optimize the efficacy of entomopathogenic nematodes against Agrotis ipsilon (Lepidoptera: Noctuidae) larvae in turfgrass. Crop Prot 155:105927
Kornsakulkarn J, Pruksatrakul T, Surawatanawong P, Thangsrikeattigun C, Komwijit S, Boonyuen N, Thongpanchang C (2021) Antimicrobial, antimalarial, and cytotoxic substances from the insect pathogenic fungus Beauveria asiatica BCC 16812. Phytochem Lett 43:8–15. https://doi.org/10.1016/j.phytol.2021.03.003
Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV (2018) Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecol 34:43–49. https://doi.org/10.1016/j.funeco.2018.04.002
Kreutz J, Vaupel O, Kolb M, Zimmermann G (2022) Effect of mineral dusts alone and in combination with the entomopathogenic fungus Beauveria bassiana (Bals.) Vuill. Against the bark beetle Ips typographus L. (Col, Scolytidae) in the laboratory and under field conditions. For Ecol Manag 515:120225. https://doi.org/10.1016/j.foreco.2022.120225
Kumar S, Korra T, Thakur R, Arutselvan R, Kashyap AS, Nehela Y, Keswani C (2023) Role of plant secondary metabolites in defence and transcriptional regulation in response to biotic stress. Plant Stress. https://doi.org/10.1016/j.stress.2023.100154
Kumawat KC, Sharma B, Nagpal S, Kumar A, Tiwari S, Nair RM (2023) Plant growth-promoting rhizobacteria: Salt stress alleviators to improve crop productivity for sustainable agriculture development. Front Plant Sci 13:1101862. https://doi.org/10.3389/fpls.2022.1101862
Landlinez-Torres A, Panelli S, Picco AM, Comandatore F, Tosi S, Capelli E (2019) A meta-barcoding analysis of soil mycobiota of the upper Andean Colombian agro-environment. Sci Rep 9(1):10085
Lee SY, Nakajima I, Ihara F, Kinoshita H, Nihira T (2005) Cultivation of entomopathogenic fungi for the search of antibacterial compounds. Mycopathologia 160:321–325. https://doi.org/10.1007/s11046-005-0179-y
Lee SY, Kinoshita H, Ihara F, Igarashi Y, Nihira T (2008) Identification of a novel derivative of helvolic acid from Metarhizium anisopliae grown in medium with insect component. J Biosci Bioeng 105(5):476–480. https://doi.org/10.1263/jbb.105.476
Lee JY, Woo RM, Woo SD (2023) Formulation of the entomopathogenic fungus Beauveria bassiana JN5R1W1 for the control of mosquito adults and evaluation of its novel applicability. J Asia-Pac Entomol 26(2):102056. https://doi.org/10.1016/j.aspen.2023.102056
Li D, Park SE, Lee MR, Kim JC, Lee SJ, Kim JS (2021) Soil application of Beauveria bassiana JEF-350 granules to control melon thrips, thrips palmi Karny (Thysanoptera: Thripidae). J Asia-Pac Entomol 24(3):636–644. https://doi.org/10.1016/j.aspen.2021.05.010
Li S, Liu F, Kang Z, Li X, Lu Y, Li Q, Yin X (2022) Cellular immune responses of the yellow peach moth, Conogethes punctiferalis (Lepidoptera: Crambidae), to the entomopathogenic fungus, Beauveria bassiana (Hypocreales: Cordycipitaceae). J Invertebr Pathol 194:107826. https://doi.org/10.1016/j.jip.2022.107826
Liao X, Luo Q, Wu C, Zhou D, Li J, Meng Z (2023) A 1-aminocyclopropane-1-carboxylate deaminase MrACCD from Metarhizium robertsii is associated with plant growth promotion for Metarhizium spp. J Invertebr Pathol. https://doi.org/10.1016/j.jip.2023.107928
Liu JF, Zhang ZQ, Beggs JR, Paderes E, Zou X, Wei XY (2020) Lethal and sublethal effects of entomopathogenic fungi on tomato/potato psyllid, Bactericera cockerelli (Šulc)(Hemiptera: Triozidae) in Capsicum. Crop Prot 129:105023. https://doi.org/10.1016/j.cropro.2019.105023
Liu ZC, Zhou L, Wang JL, Liu XS (2021) Expression of a phenoloxidase cascade inhibitor enhances the virulence of the fungus Beauveria bassiana against the insect Helicoverpa armigera. Dev Comp Immunol 117:103986. https://doi.org/10.1016/j.dci.2020.103986
Liu Y, Yang Y, Wang B (2022) Entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae play roles of maize (Zea mays) growth promoter. Sci Rep 12(1):15706
Lorenz SC, Humbert P, Wassermann M, Mackenstedt U, Patel AV (2020) A broad approach to screening of Metarhizium spp. blastospores for the control of Ixodes ricinus nymphs. Biol Control 146:104270. https://doi.org/10.1016/j.biocontrol.2020.104270
Lozano-Tovar MD, Ortiz-Urquiza A, Garrido-Jurado I, Trapero-Casas A, Quesada-Moraga E (2013) Assessment of entomopathogenic fungi and their extracts against a soil-dwelling pest and soil-borne pathogens of olive. Biol Control 67(3):409–420. https://doi.org/10.1016/j.biocontrol.2013.09.006
Ma X, Wang W, Li E, Gao F, Guo L, Pei Y (2016) A new sesquiterpene from the entomogenous fungus Phomopsis amygdali. Nat Prod Res 30(3):276–280. https://doi.org/10.1080/14786419.2015.1055742
Mannino MC, Huarte-Bonnet C, Davyt-Colo B, Pedrini N (2019) Is the insect cuticle the only entry gate for fungal infection? Insights into alternative modes of action of entomopathogenic fungi. J Fungi 5(2):33. https://doi.org/10.3390/jof5020033
Mantzoukas S, Grammatikopoulos G (2020) The effect of three entomopathogenic endophytes of the sweet sorghum on the growth and feeding performance of its pest, Sesamia nonagrioides larvae, and their efficacy under field conditions. Crop Prot. https://doi.org/10.1016/j.cropro.2019.104952
Mascarin GM, Lopes RB, Delalibera Í Jr, Fernandes ÉKK, Luz C, Faria M (2019) Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. J Invertebr Pathol 165:46–53. https://doi.org/10.1016/j.jip.2018.01.001
Mc Namara L, Dolan SK, Walsh JM, Stephens JC, Glare TR, Kavanagh K, Griffin CT (2019) Oosporein, an abundant metabolite in Beauveria caledonica, with a feedback induction mechanism and a role in insect virulence. Fungal Biol 123(8):601–610
McGuire AV, Northfield TD (2021) Identification and evaluation of endemic Metarhizium strains for biological control of banana rust thrips. Biol Control 162:104712. https://doi.org/10.1016/j.biocontrol.2021.104712
Mei L, Chen M, Shang Y, Tang G, Tao Y, Zeng L, Wang C (2021) Population genomics and evolution of a fungal pathogen after releasing exotic strains to control insect pests for 20 years. ISME J 14(6):1422–1434. https://doi.org/10.1038/s41396-020-0620-8
Membang G, Ambang Z, Mahot HC, Kuate AF, Fiaboe KKM, Hanna R (2021) Thermal response and horizontal transmission of Cameroonian isolates of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae–candidates for microbial controls of the banana root borer Cosmopolites sordidus. Fungal Ecol 50:101042. https://doi.org/10.1016/j.funeco.2021.101042
Michereff-Filho M, Navia D, Quevedo IA, de Almeida Magalhães M, da Silva Melo JW, Lopes RB (2022) The effect of spider mite-pathogenic strains of Beauveria bassiana and humidity on the survival and feeding behavior of Neoseiulus predatory mite species. Biol Control 176:105083. https://doi.org/10.1016/j.biocontrol.2022.105083
Muniz ER, Bedini S, Sarrocco S, Vannacci G, Mascarin GM, Fernandes ÉK, Conti B (2020) Carnauba wax enhances the insecticidal activity of entomopathogenic fungi against the blowfly Lucilia sericata (Diptera: Calliphoridae). J Invertebr Pathol 174:107391. https://doi.org/10.1016/j.jip.2020.107391
Nirma C, Eparvier V, Stien D (2015) Reactivation of antibiosis in the entomogenous fungus Chrysoporthe sp. SNB-CN74. J Antibiot 68(9):586–590
Ortiz-Urquiza A, Garrido-Jurado I, Santiago-Álvarez C, Quesada-Moraga E (2009) Purification and characterisation of proteins secreted by the entomopathogenic fungus Metarhizium anisopliae with insecticidal activity against adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Pest Manag Sci 65(10):1130–1139
Ownley BH, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol 55:113–128. https://doi.org/10.1007/s10526-009-9241
Park SE, Kim JC, Im Y, Kim JS (2023) Pathogenesis and defense mechanism while Beauveria bassiana JEF-410 infects poultry red mite Dermanyssus gallinae. Plos One 18(2):e0280410. https://doi.org/10.1371/journal.pone.0280410
Paschapur A, Subbanna ARNS, Singh AK, Jeevan B, Stanley J, Rajashekhar H, Mishra KK (2021) Unraveling the importance of metabolites from entomopathogenic fungi in insect pest management. Microbes Sustain Insect Pest Manag 2:89–120. https://doi.org/10.1007/978-3-030-67231-7_5
Pattnaik SS, Busi S (2019) Rhizospheric fungi: diversity and potential biotechnological applications. Recent advancement in white biotechnology through fungi: diversity and enzymes perspectives. Springer International Publishing, Cham, pp 63–84. https://doi.org/10.1007/978-3-030-10480-1_2
Pedrini N (2018) Molecular interactions between entomopathogenic fungi (Hypocreales) and their insect host: Perspectives from stressful cuticle and hemolymph battlefields and the potential of dual RNA sequencing for future studies. Fungal Biol 122(6):538–545. https://doi.org/10.1016/j.funbio.2017.10.003
Qasim M, Islam SU, Islam W, Noman A, Khan KA, Hafeez M, Wang L (2020) Characterization of mycotoxins from entomopathogenic fungi (Cordyceps fumosorosea) and their toxic effects to the development of Asian citrus psyllid reared on healthy and diseased citrus plants. Toxicon 188:39–47. https://doi.org/10.1016/j.toxicon.2020.10.012
Qasim M, **ao H, He K, Omar MA, Hussain D, Noman A, Li F (2021) Host-pathogen interaction between Asian citrus psyllid and entomopathogenic fungus (Cordyceps fumosorosea) is regulated by modulations in gene expression, enzymatic activity and HLB-bacterial population of the host. Comp Biochem Physiol Part C 248:109112. https://doi.org/10.1016/j.cbpc.2021.109112
Quesada-Moraga EEAA, Maranhao EAA, Valverde-García P, Santiago-Álvarez C (2006) Selection of Beauveria bassiana isolates for control of the whiteflies Bemisia tabaci and Trialeurodes vaporariorum on the basis of their virulence, thermal requirements, and toxicogenic activity. Biol Control 36(3):274–287
Quesada-Moraga E, Yousef-Naef M, Garrido-Jurado I (2020) Advances in the use of entomopathogenic fungi as biopesticides in suppressing crop pests. In: Shal V (ed) Biopesticides for sustainable agriculture. Burleigh Dodds Science Publishing, Cambridge, pp 63–98
Rajula J, Rahman A, Krutmuang P (2020) Entomopathogenic fungi in Southeast Asia and Africa and their possible adoption in biological control. Biol Control 151:104399. https://doi.org/10.1016/j.biocontrol.2020.104399
Ramakuwela T, Hatting J, Bock C, Vega FE, Wells L, Mbata GN, Shapiro-Ilan D (2020) Establishment of Beauveria bassiana as a fungal endophyte in pecan (Carya illinoinensis) seedlings and its virulence against pecan insect pests. Biol Control 140:104102. https://doi.org/10.1016/j.biocontrol.2019.104102
Rauch H, Steinwender BM, Mayerhofer J, Sigsgaard L, Eilenberg J, Enkerli J, Strasser H (2017) Field efficacy of Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae), Metarhizium brunneum (Hypocreales: Clavicipitaceae), and chemical insecticide combinations for Diabrotica virgifera virgifera larval management. Biol Control 107:1–10
Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E (2016) Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticide against chewing insects. J Invertebr Pathol 136:23–31. https://doi.org/10.1016/j.jip.2016.03.003
Rocha LF, Rodrigues J, Martinez JM, Pereira TC, Neto JR, Montalva C, Luz C (2022) Occurrence of entomopathogenic hypocrealean fungi in mosquitoes and their larval habitats in Central Brazil, and activity against Aedes aegypti. J Invertebr Pathol 194:107803. https://doi.org/10.1016/j.jip.2022.107803
Rosa A, Piras A, Carta G, Solari P, Crnjar R, Masala C (2018) Evaluation of the attractant effect and lipid profile modulation of natural fixed oils on the medfly Ceratitis capitata (Wiedemann). Arch Insect Biochem Physiol 99(4):e21508
Russo ML, Pelizza SA, Vianna MF, Allegrucci N, Cabello MN, Toledo AV, Scorsetti AC (2019) Effect of endophytic entomopathogenic fungi on soybean Glycine max (L.) Merr growth and yield. J King Saud Univ Sci 31(4):728–736. https://doi.org/10.1016/j.jksus.2018.04.008
Sadorn K, Saepua S, Punyain W, Saortep W, Choowong W, Rachtawee P, Pittayakhajonwut P (2020) Chromanones and aryl glucoside analogs from the entomopathogenic fungus Aschersonia confluens BCC53152. Fitoterapia 144:104606. https://doi.org/10.1016/j.fitote.2020.104606
Saeed MB, Laing MD, Miller RM, Bancole B (2017) Ovicidal, larvicidal and insecticidal activity of strains of Beauveria bassiana (Balsamo) Vuillemin against the cigarette beetle, Lasioderma serricorne Fabricius (Coleoptera: Anobiidae), on rice grain. J Stored Prod Res 74:78–86. https://doi.org/10.1016/j.jspr.2017.10.001
Saidi A, Mebdoua S, Mecelem D, Al-Hoshani N, Sadrati N, Boufahja F, Bendif H (2023) Dual Biocontrol Potential of the entomopathogenic fungus Akanthomyces muscarius against Thaumetopoea pityocampa and plant pathogenic fungi. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2023.103719
Salem HH, Mohammed SH, Eltaly RI, Moustafa MA, Fónagy A, Farag SM (2023) Co-application of entomopathogenic fungi with chemical insecticides against Culex pipiens. J Invertebr Pathol 198:107916. https://doi.org/10.1016/j.jip.2023.107916
Sani I, Ismail SI, Abdullah S, Jalinas J, Jamian S, Saad N (2020) A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects 11(9):619. https://doi.org/10.3390/insects11090619
Santos ACDS, Lopes RDS, de Oliveira LG, Diniz AG, Shakeel M, Lima EÁDLA, Lima VLDM (2022) Entomopathogenic fungi: current status and prospects. New Future Dev Biopesticide Res. https://doi.org/10.1007/978
Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99(1):101–107. https://doi.org/10.1016/j.jip.2016.03.003
Selvaraj A, Thangavel K (2021) Arbuscular mycorrhizal fungi: Potential plant protective agent against herbivorous insect and its importance in sustainable agriculture. Symbiotic Soil Microorgan. https://doi.org/10.1007/978-3-030-51916-2_19
Shah FA, Wang CS, Butt TM (2005) Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett 251(2):259–266
Shahrajabian MH, Kuang Y, Cui H, Fu L, Sun W (2023) Metabolic changes of active components of important medicinal plants on the basis of traditional Chinese medicine under different environmental stresses. Curr Org Chem 27(9):782–806
Sharma A, Sharma S, Yadav PK (2023) Entomopathogenic fungi and their relevance in sustainable agriculture: a review. Cogent Food Agric 9(1):2180857. https://doi.org/10.1080/23311932.2023.2180857
Shukla P, Bankar DR, Kumar A, Mishra PK, Raghuvanshi HR, Gayithri M (2023) Advancements in the use of entomopathogenic microbes for pest and disease management-a review. Int J Environ Clim Change 13(10):945–953. https://doi.org/10.9734/IJECC/2023/v13i102740
Siddiqui JA, Zhang Y, Luo Y, Bamisile BS, Rehman NU, Islam W, Xu Y (2022) Comprehensive detoxification mechanism assessment of red imported fire ant (Solenopsis invicta) against indoxacarb. Molecules 27(3):870. https://doi.org/10.3390/molecules27030870
Spechenkova N, Kalinina NO, Zavriev SK, Love AJ, Taliansky M (2023) ADP-ribosylation and antiviral resistance in plants. Viruses 15(1):241. https://doi.org/10.3390/v15010241
Spescha A, Weibel J, Wyser L, Brunner M, Hermida MH, Moix A, Maurhofer M (2023) Combining entomopathogenic Pseudomonas bacteria, nematodes and fungi for biological control of a below-ground insect pest. Agric Ecosyst Environ 348:108414. https://doi.org/10.1016/j.agee.2023.108414
Sun S, Wang Z, Zhang Z, Hoffmann AA, Guo H (2021) The roles of entomopathogenic fungal infection of viruliferous whiteflies in controlling tomato yellow leaf curl virus. Biol Control 156:104552. https://doi.org/10.1016/j.biocontrol.2021.104552
Sword GA (2015) The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control. https://doi.org/10.1016/j.biocontrol.2015.03.010
Thaochan N, Benarlee R, Prabhakar CS, Hu Q (2020) Impact of temperature and relative humidity on effectiveness of Metarhizium guizhouense PSUM02 against longkong bark eating caterpillar Cossus chloratus Swinhoe under laboratory and field conditions. J Asia-Pac Entomol 23(2):285–290. https://doi.org/10.1016/j.aspen.2020.01.006
Tomson M, Sahayaraj K, Sayed S, Elarnaouty SA, Petchidurai G (2021) Entomotoxic proteins of Beauveria bassiana Bals. (Vuil.) and their virulence against two cotton insect pests. J King Saud Univ Sci 33(8):101595. https://doi.org/10.1016/j.jksus.2021.101595
Tsoupras A, Kouvelis VN, Pappas KM, Demopoulos CA, Typas MA (2022) Anti-inflammatory and anti-thrombotic properties of lipid bioactives from the entomopathogenic fungus Beauveria bassiana. Prostaglandins Other Lipid Mediat 158:106606. https://doi.org/10.1016/j.prostaglandins.2021.106606
Tu C, Zhang Y, Zhu P, Sun L, Xu P, Wang T, Xu L (2023) Enhanced toxicity of entomopathogenic fungi Beauveria bassiana with bacteria expressing immune suppressive dsRNA in a leaf beetle. Pestic Biochem Physiol 193:105431. https://doi.org/10.1016/j.pestbp.2023.105431
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2(4):149–159
Wakil W, Ghazanfar MU, Usman M, Hunter D, Shi W (2022) Fungal-based biopesticide formulations to control nymphs and adults of the desert locust, Schistocerca gregaria Forskål (Orthoptera: Acrididae): a laboratory and field cage study. Agronomy 12(5):1160
Wang C, Huang Y, Zhao J, Ma Y, Xu X, Wan Q, Pan B (2019a) First record of Aspergillus oryzae as an entomopathogenic fungus against the poultry red mite Dermanyssus gallinae. Vet Parasitol 271:57–63. https://doi.org/10.1016/j.vetpar.2019.06.011
Wang J, Lovett B, Leger RJS (2019b) The secretome and chemistry of Metarhizium; a genus of entomopathogenic fungi. Fungal Ecol 38:7–11. https://doi.org/10.1016/j.funeco.2018.04.001
Wang L, Wang J, Zhang X, Yin Y, Li R, Lin Y, Wang Z (2021) Pathogenicity of Metarhizium rileyi against Spodoptera litura larvae: appressorium differentiation, proliferation in hemolymph, immune interaction, and reemergence of mycelium. Fungal Genet Biol 150:103508. https://doi.org/10.1016/j.fgb.2020.103508
Wang JL, Sun J, Song YJ, Zheng HH, Wang GJ, Luo WX, Liu XS (2023a) An entomopathogenic fungus exploits its host humoral antibacterial immunity to minimize bacterial competition in the hemolymph. Microbiome 11(1):1–18. https://doi.org/10.1186/s40168-023-01538-6
Wang P, Yang G, Shi N, Zhao C, Hu F, Coutts RH, Huang B (2023) A novel partitivirus orchestrates condition, stress response, pathogenicity, and secondary metabolism of the entomopathogenic fungus Metarhizium majus. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1011397
Woolley VC, Teakle GR, Prince G, de Moor CH, Chandler D (2020) Cordycepin, a metabolite of Cordyceps militaris, reduces immune-related gene expression in insects. J Invertebr Pathol 177:107480. https://doi.org/10.1016/j.jip.2020.107480
Wu JH, Ali S, Ren SX (2010) Evaluation of chitinase from Metarhizium anisopliae as biopesticide against Plutella xylostella. Pak J Zool 42(5):521–528
Wu S, Wu J, Wang Y, Qu Y, He Y, Wang J, Cheng C (2022) Discovery of entomopathogenic fungi across geographical regions in southern China on pine sawyer beetle Monochamus alternatus and implication for multi-pathogen vectoring potential of this beetle. Front Plant Sci 13:1061520. https://doi.org/10.1016/j.funeco.2018.04.001
Xu Y, Orozco R, Wijeratne EK, Espinosa-Artiles P, Gunatilaka AL, Stock SP, Molnár I (2009) Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana. Fungal Genet Biol 46(5):353–364
Yang R, Zhang M, Schal C, Jiang M, Cai T, Zhang F (2021) Boric acid enhances Metarhizium anisopliae virulence in Blattella germanica (L.) by disrupting the gut and altering its microbial community. Biol Control 152:104430. https://doi.org/10.1016/j.biocontrol.2020.104430
Yang Z, Wu Q, Fan J, Huang J, Wu Z, Lin, J.s, Shu, B. (2021b) Effects of the entomopathogenic fungus Clonostachys rosea on mortality rates and gene expression profiles in Diaphorina citri adults. J Invertebr Pathol 179:107539. https://doi.org/10.1016/j.jip.2021.107539
Yang TH, Wu LH, Liao CT, Li D, Shin TY, Kim JS, Nai YS (2023) Entomopathogenic fungi-mediated biological control of the red palm weevil Rhynchophorus ferrugineus. J Asia-Pac Entomol. https://doi.org/10.1016/j.aspen.2023.102037
Ye G, Zhang L, Zhou X (2021) Long noncoding RNAs are potentially involved in the degeneration of virulence in an aphid-obligate pathogen, Conidiobolus obscurus (Entomophthoromycotina). Virulence 12(1):1705–1716
Yosri M, Abdel-Aziz MM, Sayed RM (2018) Larvicidal potential of irradiated myco-insecticide from Metarhizium anisopliae and larvicidal synergistic effect with its mycosynthesized titanium nanoparticles (TiNPs). J Radiation Res Appl Sci 11(4):328–334. https://doi.org/10.1016/j.jrras.2018.06.001
Yuan Y, Huang W, Chen K, Ling E (2020) Beauveria bassiana ribotoxin inhibits insect immunity responses to facilitate infection via host translational blockage. Dev Comp Immunol 106:103605. https://doi.org/10.1016/j.dci.2019.103605
Zhang B, Zou C, Hu Q (2016) Effects of Isaria fumosorosea on TYLCV (tomato yellow leaf curl virus) accumulation and transmitting capacity of Bemisia tabaci. PLoS One. https://doi.org/10.1371/journal.pone.0164356
Zhang J, Yu H, Li S, Zhong X, Wang H, Liu X (2020a) Comparative metabolic profiling of Ophiocordyceps sinensis and its cultured mycelia using GC–MS. Food Res Int 134:109241. https://doi.org/10.1016/j.foodres.2020.109241
Zhang L, Fasoyin OE, Molnár I, Xu Y (2020b) Secondary metabolites from hypocrealean entomopathogenic fungi: Novel bioactive compounds. Nat Prod Rep 37(9):1181–1206
Zhang C, Teng B, Liu H, Wu C, Wang L, ** S (2023a) Impact of Beauveria bassiana on antioxidant enzyme activities and metabolomic profiles of Spodoptera frugiperda. J Invertebr Pathol 198:107929. https://doi.org/10.1016/j.jip.2023.107929
Zhang J, Ye C, Wang ZG, Ding BY, Smagghe G, Zhang Y, Wang JJ (2023b) DsRNAs spray enhanced the virulence of entomopathogenic fungi Beauveria bassiana in aphid control. J Pest Sci 96(1):241–251
Zhang Z, Sui L, Tian Y, Lu Y, **a X, Liu W, Shi W (2024) Metarhizium rileyi with broad-spectrum insecticidal ability confers resistance against phytopathogens and insect pests as a phytoendophyte. Pest Manag Sci. https://doi.org/10.1002/ps.8027
Zhou L, Zheng J, Liu Z, Ma W, Lei C (2016) Effects of UVA radiation on the performance of adults and the first filial generation of the fruit fly Drosophila melanogaster Meigen, 1830 (Diptera: Drosophilidae). Proc Entomol Soc Wash 118(3):456–465
Zhou TT, Qian ZHAO, Li CZ, Lu YE, Li YF, Keyhani NO, Huang Z (2023) Synergistic effects of the entomopathogenic fungus Isaria javanica and low doses of dinotefuran on the efficient control of the rice pest Sogatella furcifera. J Integr Agric. https://doi.org/10.1016/j.jia.2023.06.007
Zhu KY, Palli SR (2020) Mechanisms, applications, and challenges of insect RNA interference. Annu Rev Entomol 65:293–311
Zuharah WF, Rohaiyu MR, Azmi WA, Nagao H (2021) Pathogenicity of entomopathogenic fungus, Metarhizium anisopliae MET-GRA4 isolate on dengue vectors, Aedes albopictus and Aedes aegypti mosquito larvae (Diptera: Culicidae). J Asia-Pac Entomol 24(2):24–29. https://doi.org/10.1016/j.aspen.2021.04.008
Funding
No funding.
Author information
Authors and Affiliations
Contributions
Muhammad Shahbaz and Jaya Seelan Sathiya Seelan: Conceptualization; formal analysis, writing original draft. Kishneth Palaniveloo, Tan Yee Shin, Praneetha Palasuberniam, Noshin Ilyas, and Christophe Wiart: Initial review & editing. Jaya Seelan Sathiya Seelan: Supervision, critically reviewed, English editing and final validation.
Corresponding authors
Ethics declarations
Competing interest
The authors declare no competing interests.
Ethical approval
The current study does not involve the use of animals.
Consent to participate
Not applicable.
Consent to publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shahbaz, M., Palaniveloo, K., Tan, Y. et al. Entomopathogenic fungi in crops protection with an emphasis on bioactive metabolites and biological activities. World J Microbiol Biotechnol 40, 217 (2024). https://doi.org/10.1007/s11274-024-04022-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-024-04022-x