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Genetics and Infection Biology of the Entomopathogenic Fungi

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Fungal Associations

Part of the book series: The Mycota ((MYCOTA,volume 9))

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Abstract

Insects and fungi, both megadiverse groups of organisms, have a long history of associations with each other. Among the fungi, Hypocreales (Ascomycota) and Entomophthoromycotina (Zoopagomycota), contain the most common pathogens of insects. Ascomycete entomopathogenic fungi (EPF) are mostly well-studied and have been found to be either heterothallically or homothallically sexual with a divergent number of genes at the mating-type loci of different species. So far more than 100 strains of >60 EPF species have been genome sequenced which demonstrated substantial variations in genome size and gene content among each other. However, convergent evolution of fungal entomopathogenicity has been coined, especially in terms of the similar expansion of protease and chitinase gene families in EPF for targeting the protein- and chitin-rich insect cuticles. Functional genetic studies have unveiled an array of EPF genes involved in mediating host recognition and interactions with insect hosts, especially mechanisms of invading or evading host immunity to facilitate fungal colonization of insect body cavities. The discovery of small molecules and their essential roles in mediating EPF associations with insect hosts also have been advanced. In addition to advancing the mechanisms of fungus–insect interactions, these works highly benefit the development of cost-effective mycoinsecticides and the protection of ecologically and economically important beneficial insects.

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References

  • Agrawal Y, Khatri I, Subramanian S, Shenoy BD (2015) Genome sequence, comparative analysis, and evolutionary insights into chitinases of entomopathogenic fungus Hirsutella thompsonii. Genome Biol Evol 7:916–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agrawal Y, Narwani T, Subramanian S (2016) Genome sequence and comparative analysis of clavicipitaceous insect-pathogenic fungus Aschersonia badia with Metarhizium spp. BMC Genomics 17:367

    Article  PubMed  PubMed Central  Google Scholar 

  • Altimira F, Arias-Aravena M, Jian L et al (2022) Genomic and experimental analysis of the insecticidal factors secreted by the entomopathogenic fungus Beauveria pseudobassiana RGM 2184. J Fungi (Basel) 8:253

    Article  CAS  PubMed  Google Scholar 

  • Andreadis TG, Weseloh RM (1990) Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proc Natl Acad Sci U S A 87:2461–2465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Araújo JP, Hughes DP (2016) Diversity of entomopathogenic fungi: which groups conquered the insect body? Adv Genet 94:1–39

    Article  PubMed  Google Scholar 

  • Araujo JPM, Hughes DP (2019) Zombie-ant fungi emerged from non-manipulating, beetle-infecting ancestors. Curr Biol 29:3735–3738

    Article  CAS  PubMed  Google Scholar 

  • Arnesen JA, Malagocka J, Gryganskyi A, Grigoriev IV, Voigt K, Stajich JE, De Fine Licht HH (2018) Early diverging insect-pathogenic fungi of the order Entomophthorales possess diverse and unique subtilisin-like serine proteases. G3 (Bethesda) 8:3311–3319

    Article  CAS  PubMed  Google Scholar 

  • Badaruddin M, Holcombe LJ, Wilson RA, Wang ZY, Kershaw MJ, Talbot NJ (2013) Glycogen metabolic genes are involved in trehalose-6-phosphate synthase-mediated regulation of pathogenicity by the rice blast fungus Magnaporthe oryzae. PLoS Pathog 9:e1003604

    Article  PubMed  PubMed Central  Google Scholar 

  • Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577

    Article  CAS  PubMed  Google Scholar 

  • Blackwell M (2011) The Fungi: 1, 2, 3 … 5.1 million species? Am J Bot 98:426–438

    Article  PubMed  Google Scholar 

  • Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–w35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyce GR, Gluck-Thaler E, Slot JC et al (2019) Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens. Fungal Ecol 41:147–164

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruner-Montero G, Wood M, Horn HA, Gemperline E, Li L, Currie CR (2021) Symbiont-mediated protection of Acromyrmex leaf-cutter ants from the entomopathogenic fungus Metarhizium anisopliae. mBio 12:e0188521

    Article  PubMed  Google Scholar 

  • Buchon N, Silverman N, Cherry S (2014) Immunity in Drosophila melanogaster--from microbial recognition to whole-organism physiology. Nat Rev Immunol 14:796–810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bushley KE, Raja R, Jaiswal P et al (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9:e1003496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai Y, Nie Y, Gao Y, Huang B (2022) Natural populations of the entomopathogenic fungus Beauveria bassiana in Chinese forest ecosystems are diverse and reveal equal frequencies of mating types within phylogenetic species. Fungal Ecol 56:101139

    Article  Google Scholar 

  • Castro-Vásquez R, Solano-González S, Molina-Bravo R, Montero-Astúa M (2022) Draft genome sequences of eight isolates of Beauveria bassiana of neotropical origin. Microbiol Resour Announc 11:e00267–e00222

    Article  PubMed  PubMed Central  Google Scholar 

  • Cen K, Li B, Lu YZ, Zhang SW, Wang CS (2017) Divergent LysM effectors contribute to the virulence of Beauveria bassiana by evasion of insect immune defenses. PLoS Pathog 13:e1006604

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang Y, Wang SS, Sekimoto S et al (2015) Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol 7:1590–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Pettis JS, Zhao Y et al (2013) Genome sequencing and comparative genomics of honey bee microsporidia, Nosema apis reveal novel insights into host-parasite interactions. BMC Genomics 14:451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YX, Feng P, Shang YF, Xu YJ, Wang CS (2015) Biosynthesis of non-melanin pigment by a divergent polyketide synthase in Metarhizium robertsii. Fungal Genet Biol 81:142–149

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Xu C, Qian Y et al (2016) MAPK cascade-mediated regulation of pathogenicity, conidiation and tolerance to abiotic stresses in the entomopathogenic fungus Metarhizium robertsii. Environ Microbiol 18:1048–1062

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Wang Y, Shao Y, Huang B (2017) A novel technique for rejuvenation of degenerated caterpillar medicinal mushroom, Cordyceps militaris (Ascomycetes), a valued traditional Chinese medicine. Int J Med Mushrooms 19:87–91

    Article  PubMed  Google Scholar 

  • Chen YX, Li B, Cen K, Lu YZ, Zhang SW, Wang CS (2018a) Diverse effect of phosphatidylcholine biosynthetic genes on phospholipid homeostasis, cell autophagy and fungal developments in Metarhizium robertsii. Environ Microbiol 20:293–304

    Article  CAS  PubMed  Google Scholar 

  • Chen YX, Cen K, Lu Y, Zhang S, Shang YF, Wang CS (2018b) Nitrogen-starvation triggers cellular accumulation of triacylglycerol in Metarhizium robertsii. Fungal Biol 122:410–419

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Wu Y, Liu L et al (2019) Study of the whole genome, methylome and transcriptome of Cordyceps militaris. Sci Rep 9:898

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen B, Sun YL, Luo FF, Wang CS (2020a) Bioactive metabolites and potential mycotoxins produced by Cordyceps fungi: a review of safety. Toxins 12:410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Gao X, Li R et al (2020b) Complete genome of a unicellular parasite (Antonospora locustae) and transcriptional interactions with its host locust. Microb Genom 6:mgen000421

    PubMed  PubMed Central  Google Scholar 

  • Chen B, Sun YL, Li SQ, Yin Y, Wang CS (2021) Inductive production of the iron-chelating 2-pyridones benefits the producing fungus to compete for diverse niches. mBio 12:e0327921

    Article  PubMed  Google Scholar 

  • Cormier A, Chebbi MA, Giraud I et al (2021) Comparative genomics of strictly vertically transmitted, feminizing microsporidia endosymbionts of amphipod crustaceans. Genome Biol Evol 13:evaa245

    Article  PubMed  Google Scholar 

  • Cornman RS, Chen YP, Schatz MC et al (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5:e1000466

    Article  PubMed  PubMed Central  Google Scholar 

  • Cortés JCG, Curto M, Carvalho VSD, Pérez P, Ribas JC (2019) The fungal cell wall as a target for the development of new antifungal therapies. Biotechnol Adv 37:107352

    Article  PubMed  Google Scholar 

  • Cui C, Wang Y, Liu J, Zhao J, Sun P, Wang S (2019) A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection. Nat Commun 10:4298

    Article  PubMed  PubMed Central  Google Scholar 

  • Dang EV, Lei S, Radkov A, Volk RF, Zaro BW, Madhani HD (2022) Secreted fungal virulence effector triggers allergic inflammation via TLR4. Nature 608:161–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Bekker C (2019) Ophiocordyceps-ant interactions as an integrative model to understand the molecular basis of parasitic behavioral manipulation. Curr Opin Insect Sci 33:19–24

    Article  PubMed  Google Scholar 

  • de Bekker C, Ohm RA, Loreto RG et al (2015) Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics 16:620

    Article  PubMed  PubMed Central  Google Scholar 

  • de Bekker C, Ohm RA, Evans HC, Brachmann A, Hughes DP (2017) Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. Sci Rep 7:12508

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Desjardins CA, Sanscrainte ND, Goldberg JM et al (2015) Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes. Nat Commun 6:7121

    Article  CAS  PubMed  Google Scholar 

  • Donzelli BGG, Krasnoff SB, Moon YS, Churchill AC, Gibson DM (2012) Genetic basis of destruxin production in the entomopathogen Metarhizium robertsii. Curr Genet 58:105–116

    Article  CAS  Google Scholar 

  • Duan ZB, Chen YX, Huang W, Shang YF, Chen PL, Wang CS (2013) Linkage of autophagy to fungal development, lipid storage and virulence in Metarhizium robertsii. Autophagy 9:538–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eley KL, Halo LM, Song Z et al (2007) Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana. Chembiochem 8:289–297

    Article  CAS  PubMed  Google Scholar 

  • Elya C, Lok TC, Spencer QE, McCausland H, Martinez CC, Eisen M (2018) Robust manipulation of the behavior of Drosophila melanogaster by a fungal pathogen in the laboratory. elife 7:e34414

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan Y, Liu X, Keyhani NO, Tang G, Pei Y, Zhang W, Tong S (2017) Regulatory cascade and biological activity of Beauveria bassiana oosporein that limits bacterial growth after host death. Proc Natl Acad Sci U S A 114:E1578–E1586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng P, Shang Y, Cen K, Wang C (2015) Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity. Proc Natl Acad Sci U S A 112:11365–11370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrandon D, Imler JL, Hetru C, Hoffmann JA (2007) The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7:862–874

    Article  CAS  PubMed  Google Scholar 

  • Fischer R, Requena N (2022) Small-secreted proteins as virulence factors in nematode-trapping fungi. Trends Microbiol 30:615–617

    Article  CAS  PubMed  Google Scholar 

  • Fredericksen MA, Zhang Y, Hazen ML, Loreto RG, Mangold CA, Chen DZ, Hughes DP (2017) Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants. Proc Natl Acad Sci U S A 114:12590–12595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Q, Jin K, Ying SH et al (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7:e1001264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Q, Shang YF, Huang W, Wang CS (2013) Glycerol-3-phosphate acyltransferase contributes to triacylglycerol biosynthesis, lipid droplet formation, and host invasion in Metarhizium robertsii. Appl Environ Microbiol 79:7646–7653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Q, Lu Y, Yao H, Xu YJ, Huang W, Wang C (2016) Phospholipid homeostasis maintains cell polarity, development and virulence in Metarhizium robertsii. Environ Microbiol 18:3976–3990

    Article  CAS  PubMed  Google Scholar 

  • Gao BJ, Mou YN, Tong SM, Ying SH, Feng MG (2020) Subtilisin-like Pr1 proteases marking evolution of pathogenicity in a wide-spectrum insect-pathogenic fungus. Virulence 11:365–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao DW, Jamieson CS, Wang G, Yan Y, Zhou J, Houk KN, Tang Y (2021) A polyketide cyclase that forms medium-ring lactones. J Am Chem Soc 143:80–84

    Article  CAS  PubMed  Google Scholar 

  • Gleason FH, Marano AV, Johnson P, Martin WW (2010) Blastocladian parasites of invertebrates. Fungal Biol Rev 24:56–67

    Article  Google Scholar 

  • Han P, Gong Q, Fan J, Abbas M, Chen D, Zhang J (2022) Destruxin A inhibits scavenger receptor B mediated melanization in Aphis citricola. Pest Manag Sci 78:1915–1924

    Article  CAS  PubMed  Google Scholar 

  • Hansen AN, De Fine Licht HH (2019) Why are there so few examples of entomopathogenic fungi that manipulate host sexual behaviors? Fungal Ecol 38:21–27

    Article  Google Scholar 

  • Harris-Tryon TA, Grice EA (2022) Microbiota and maintenance of skin barrier function. Science 376:940–945

    Article  CAS  PubMed  Google Scholar 

  • Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr 5:FUNK-0052-2016

    Google Scholar 

  • Hong S, Sun Y, Sun D, Wang CS (2022) Microbiome assembly on Drosophila body surfaces benefits the flies to combat fungal infections. iScience 25:104408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong S, Sun YL, Chen HM, Wang CS (2023) Suppression of the insect cuticular microbiomes by a fungal defensin to facilitate parasite infection. ISME J 17:1–11

    Article  CAS  PubMed  Google Scholar 

  • Horn F, Habel A, Scharf DH et al (2015) Draft genome sequence and gene annotation of the entomopathogenic fungus Verticillium hemipterigenum. Genome Announc 3:e0143914

    Article  Google Scholar 

  • Hu X, Zhang YJ, Xiao GH et al (2013) Genome survey uncovers the secrets of sex and lifestyle in caterpillar fungus. Chin Sci Bull 58:2846–2854

    Article  CAS  Google Scholar 

  • Hu X, Xiao G, Zheng P et al (2014) Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc Natl Acad Sci U S A 111:16796–16801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang W, Hong S, Tang G, Lu Y, Wang C (2019) Unveiling the function and regulation control of the DUF3129 family proteins in fungal infection of hosts. Philos Trans R Soc Lond Ser B Biol Sci 374:20180321

    Article  CAS  Google Scholar 

  • Huang A, Lu M, Ling E, Li P, Wang CS (2020) A M35 family metalloprotease is required for fungal virulence against insects by inactivating host prophenoloxidases and beyond. Virulence 11:222–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Q, Wu ZH, Li WF et al (2021) Genome and evolutionary analysis of Nosema ceranae: A microsporidian parasite of honey bees. Front Microbiol 12:645353

    Article  PubMed  PubMed Central  Google Scholar 

  • Humber RA (2008) Evolution of entomopathogenicity in fungi. J Invertebr Pathol 98:262–266

    Article  PubMed  Google Scholar 

  • Humber RA (2017) Back to the future: cordycipitoid fungi in a postgenomic world. Mycology 8:267–275

    Article  PubMed  PubMed Central  Google Scholar 

  • Hyde KD (2022) The numbers of fungi. Fungal Divers 114:1

    Article  Google Scholar 

  • Imoulan A, Hussain M, Kirk PM, El Meziane A, Yao Y-J (2017) Entomopathogenic fungus Beauveria: Host specificity, ecology and significance of morpho-molecular characterization in accurate taxonomic classification. J Asia-Pacif Entomol 20:1204–1212

    Article  Google Scholar 

  • Iwanicki NSA, Botelho A, Klingen I, Junior ID, Rossmann S, Lysoe E (2022) Genomic signatures and insights into host niche adaptation of the entomopathogenic fungus Metarhizium humberi. G3 12:jkab416

    Article  CAS  PubMed  Google Scholar 

  • Janke RS, Kaftan F, Niehs SP et al (2022) Bacterial ectosymbionts in cuticular organs chemically protect a beetle during molting stages. ISME J 16:2691–2701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JD, Vance RE, Dangl JL (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354:aaf6395

    Article  PubMed  Google Scholar 

  • Kato H, Tsunematsu Y, Yamamoto T, Namiki T, Kishimoto S, Noguchi H, Watanabe K (2016) New natural products isolated from Metarhizium robertsii ARSEF 23 by chemical screening and identification of the gene cluster through engineered biosynthesis in Aspergillus nidulans A1145. J Antibiot 69:561–566

    Article  CAS  Google Scholar 

  • Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3:937–947

    Article  CAS  PubMed  Google Scholar 

  • Kim JC, Park SE, Lee SJ, Kim JS (2022) Whole-genome sequence of Beauveria bassiana JEF-350, a strain with high insecticidal activity against melon thrips (Thrips palmi). Microbiol Resour Announc 11:e0047022

    Article  PubMed  Google Scholar 

  • Kobmoo N, Mongkolsamrit S, Tasanathai K, Thanakitpipattana D, Luangsa-Ard JJ (2012) Molecular phylogenies reveal host-specific divergence of Ophiocordyceps unilateralis sensu lato following its host ants. Mol Ecol 21:3022–3031

    Article  CAS  PubMed  Google Scholar 

  • Kobmoo N, Wichadakul D, Arnamnart N, Rodriguez De La Vega RC, Luangsa-Ard JJ, Giraud T (2018) A genome scan of diversifying selection in Ophiocordyceps zombie-ant fungi suggests a role for enterotoxins in co-evolution and host specificity. Mol Ecol 27:3582–3598

    Article  CAS  PubMed  Google Scholar 

  • Kombrink A, Thomma BP (2013) LysM effectors: secreted proteins supporting fungal life. PLoS Pathog 9:e1003769

    Article  PubMed  PubMed Central  Google Scholar 

  • Kramer GJ, Nodwell JR (2017) Chromosome level assembly and secondary metabolite potential of the parasitic fungus Cordyceps militaris. BMC Genomics 18:912

    Article  PubMed  PubMed Central  Google Scholar 

  • Krasnoff SB, Keresztes I, Gillilan RE, Szebenyi DM, Donzelli BG, Churchill AC, Gibson DM (2007) Serinocyclins A and B, cyclic heptapeptides from Metarhizium anisopliae. J Nat Prod 70:1919–1924

    Article  CAS  PubMed  Google Scholar 

  • Lai Y, Cao X, Chen J, Wang L, Wei G, Wang S (2020) Coordinated regulation of infection-related morphogenesis by the KMT2-Cre1-Hyd4 regulatory pathway to facilitate fungal infection. Sci Adv 6:eaaz1659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SJ, Lee MR, Kim S et al (2018) Genomic analysis of the insect-killing fungus Beauveria bassiana JEF-007 as a biopesticide. Sci Rep 8:12388

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee MR, Li D, Lee SJ et al (2019) Use of Metarhizum aniopliae s.l. to control soil-dwelling longhorned tick, Haemaphysalis longicornis. J Invertebr Pathol 166:107230

    Article  CAS  PubMed  Google Scholar 

  • Li J, Xia Y (2022) Host-pathogen interactions between Metarhizium spp. and locusts. J Fungi 8:602

    Article  CAS  Google Scholar 

  • Li ZZ, Li CR, Huang B, Fan MZ (2001) Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomogenous fungus. Chin Sci Bull 46:751–753

    Article  Google Scholar 

  • Li Y, Hsiang T, Yang RH et al (2016) Comparison of different sequencing and assembly strategies for a repeat-rich fungal genome, Ophiocordyceps sinensis. J Microbiol Methods 128:1–6

    Article  CAS  PubMed  Google Scholar 

  • Li B, Song S, Wei X, Tang G, Wang CS (2022) Activation of microlipophagy during early infection of insect hosts by Metarhizium robertsii. Autophagy 18:608–623

    Article  CAS  PubMed  Google Scholar 

  • Lin R, Zhang X, Xin B et al (2019) Genome sequence of Isaria javanica and comparative genome analysis insights into family S53 peptidase evolution in fungal entomopathogens. Appl Microbiol Biotechnol 103:7111–7128

    Article  CAS  PubMed  Google Scholar 

  • Litwin A, Nowak M, Rozalska S (2020) Entomopathogenic fungi: unconventional applications. Rev Environ Sci Biotechnol 19:23–42

    Article  Google Scholar 

  • Liu H, Brettell LE, Singh B (2020a) Linking the phyllosphere microbiome to plant health. Trends Plant Sci 25:841–844

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Guo L, Li Z et al (2020b) Genomic analyses reveal evolutionary and geologic context for the plateau fungus Ophiocordyceps sinensis. Chin Med 15:107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Qu S, He G, Wei J, Dong C (2022) Mating-type genes play an important role in fruiting body development in Morchella sextelata. J Fungi (Basel) 8:564

    Article  CAS  PubMed  Google Scholar 

  • Long L, Liu Z, Deng C, Li C, Wu L, Hou B, Lin Q (2022) Genomic Sequence and Transcriptome Analysis of the Medicinal Fungus Keithomyces neogunnii. Genome Biol Evol 14:evac033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopes Fischer N, Naseer N, Shin S, Brodsky IE (2020) Effector-triggered immunity and pathogen sensing in metazoans. Nat Microbiol 5:14–26

    Article  CAS  PubMed  Google Scholar 

  • Lovett B, St Leger RJ (2017) The insect pathogens. Microbiol Spectr 5:FUNK-0001-2016

    Google Scholar 

  • Lovett B, Macias A, Stajich JE, Cooley J, Eilenberg J, de Fine Licht HH, Kasson MT (2020) Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding. PLoS Pathog 16:e1008598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe RG, Howlett BJ (2012) Indifferent, affectionate, or deceitful: lifestyles and secretomes of fungi. PLoS Pathog 8:e1002515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Xia Y, Luo F, Dong C, Wang C (2016) Functional convergence and divergence of mating-type genes fulfilling in Cordyceps militaris. Fungal Genet Biol 88:35–43

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Luo F, Cen K et al (2017) Omics data reveal the unusual asexual-fruiting nature and secondary metabolic potentials of the medicinal fungus Cordyceps cicadae. BMC Genomics 18:668

    Article  PubMed  PubMed Central  Google Scholar 

  • Luangsa-Ard J, Tasanathai K, Thanakitpipattana D, Khonsanit A, Stadler M (2018) Novel and interesting Ophiocordyceps spp. (Ophiocordycipitaceae, Hypocreales) with superficial perithecia from Thailand. Stud Mycol 89:125–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo FF, Hong S, Chen B et al (2020) Unveiling of swainsonine biosynthesis via a multi-branched pathway in fungi. ACS Chem Biol 15:2476–2484

    Article  CAS  PubMed  Google Scholar 

  • Luo F, Tang G, Hong S, Gong T, Xin X-F, Wang CS (2023) Promotion of Arabidopsis immune responses by a rhizosphere fungus via supply of pipecolic acid to plants and selective augment of phytoalexins. Sci China Life Sci 66:1119–1133

    Article  CAS  PubMed  Google Scholar 

  • Lv JM, Hu D, Gao H et al (2017) Biosynthesis of helvolic acid and identification of an unusual C-4-demethylation process distinct from sterol biosynthesis. Nat Commun 8:1644

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma LJ, van der Does HC, Borkovich KA et al (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mc Namara L, Dolan SK, Walsh JMD, 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 123:601–610

    Article  CAS  PubMed  Google Scholar 

  • Mei LJ, Chen M, Shang Y et al (2020) Population genomics and evolution of a fungal pathogen after releasing exotic strains to control insect pests for 20 years. ISME J 14:1422–1434

    Article  PubMed  PubMed Central  Google Scholar 

  • Mei L, Wang X, Yin Y, Tang G, Wang CS (2021) Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts. PLoS Pathog 17:e1009656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyling NV, Lubeck M, Buckley EP, Eilenberg J, Rehner SA (2009) Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol Ecol 18:1282–1293

    Article  CAS  PubMed  Google Scholar 

  • Mondo SJ, Dannebaum RO, Kuo RC et al (2017) Widespread adenine N6-methylation of active genes in fungi. Nat Genet 49:964–968

    Article  CAS  PubMed  Google Scholar 

  • Mongkolsamrit S, Khonsanit A, Thanakitpipattana D et al (2020) Revisiting Metarhizium and the description of new species from Thailand. Stud Mycol 95:171–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moon YS, Donzelli BG, Krasnoff SB et al (2008) Agrobacterium-mediated disruption of a nonribosomal peptide synthetase gene in the invertebrate pathogen Metarhizium anisopliae reveals a peptide spore factor. Appl Environ Microbiol 74:4366–4380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moonjely S, Barelli L, Bidochka MJ (2016) Insect pathogenic fungi as endophytes. Adv Genet 94:107–135

    Article  CAS  PubMed  Google Scholar 

  • Mora C, Tittensor DP, Adl S, Simpson AG, Worm B (2011) How many species are there on Earth and in the ocean? PLoS Biol 9:e1001127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moyes DL, Wilson D, Richardson JP et al (2016) Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 532:64–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakjang S, Williams TA, Heinz E et al (2013) Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biol Evol 5:2285–2303

    Article  PubMed  PubMed Central  Google Scholar 

  • Newman DJ, Cragg GM (2020) Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Prod 83:770–803

    Article  CAS  PubMed  Google Scholar 

  • Nielsen KN, Salgado JFM, Natsopoulou ME, Kristensen T, Stajich JE, De Fine Licht HH (2021) Diploidy within a haploid genus of entomopathogenic fungi. Genome Biol Evol 13:evab158

    Article  CAS  PubMed  PubMed Central  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 

  • Palmer JM, Keller NP (2010) Secondary metabolism in fungi: does chromosomal location matter? Curr Opin Microbiol 13:431–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan G, Xu J, Li T et al (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan G, Bao J, Ma Z et al (2018) Invertebrate host responses to microsporidia infections. Dev Comp Immunol 83:104–113

    Article  PubMed  Google Scholar 

  • Pattemore JA, Hane JK, Williams AH, Wilson BA, Stodart BJ, Ash GJ (2014) The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics 15:660

    Article  PubMed  PubMed Central  Google Scholar 

  • Pelin A, Selman M, Aris-Brosou S, Farinelli L, Corradi N (2015) Genome analyses suggest the presence of polyploidy and recent human-driven expansions in eight global populations of the honeybee pathogen Nosema ceranae. Environ Microbiol 17:4443–4458

    Article  CAS  PubMed  Google Scholar 

  • Pessotti RC, Hansen BL, Reaso JN, Ceja-Navarro JA, El-Hifnawi L, Brodie EL, Traxler MF (2021) Multiple lineages of Streptomyces produce antimicrobials within passalid beetle galleries across eastern North America. elife 10:e65091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu S, Wang S (2018) Interaction of entomopathogenic fungi with the host immune system. Dev Comp Immunol 83:96–103

    Article  CAS  PubMed  Google Scholar 

  • Ramos Y, Portal O, Lysoe E, Meyling NV, Klingen I (2017) Diversity and abundance of Beauveria bassiana in soils, stink bugs and plant tissues of common bean from organic and conventional fields. J Invertebr Pathol 150:114–120

    Article  PubMed  Google Scholar 

  • Rehner SA (2020) Genetic structure of Metarhizium species in western USA: finite populations composed of divergent clonal lineages with limited evidence for recent recombination. J Invertebr Pathol 177:107491

    Article  CAS  PubMed  Google Scholar 

  • Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16:1857–1864

    Article  CAS  PubMed  Google Scholar 

  • Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357

    Article  CAS  PubMed  Google Scholar 

  • RoyChowdhury M, Sternhagen J, Xin Y, Lou B, Li X, Li C (2022) Evolution of pathogenicity in obligate fungal pathogens and allied genera. PeerJ 10:e13794

    Article  PubMed  PubMed Central  Google Scholar 

  • Saud Z, Kortsinoglou AM, Kouvelis VN, Butt TM (2021) Telomere length de novo assembly of all 7 chromosomes and mitogenome sequencing of the model entomopathogenic fungus, Metarhizium brunneum, by means of a novel assembly pipeline. BMC Genomics 22:87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savory F, Leonard G, Richards TA (2015) The role of horizontal gene transfer in the evolution of the oomycetes. PLoS Pathog 11:e1004805

    Article  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Feng P, Wang C (2015) Fungi that infect insects: altering host behavior and beyond. PLoS Pathog 11:e1005037

    Article  PubMed  PubMed Central  Google Scholar 

  • Shang YF, Xiao GH, Zheng P, Cen K, Zhan S, Wang CS (2016) Divergent and convergent evolution of fungal pathogenicity. Genome Biol Evol 8:1374–1387

    Article  PubMed  PubMed Central  Google Scholar 

  • Shang JM, Shang YF, Tang GR, Wang CS (2021) Identification of a key G-protein coupled receptor in mediating appressorium formation and fungal virulence against insects. Sci China Life Sci 64:466–477

    Article  CAS  PubMed  Google Scholar 

  • Shang J, Tang G, Lu M, Wang C (2022) Host and environmental sensing by entomopathogenic fungi to infect hosts. Curr Clin Microbiol Rep 9:69–74

    Article  Google Scholar 

  • Shang JM, Tang GR, Yang J, Lu M, Wang CZ, Wang CS (2023) Sensing of a spore surface protein by a Drosophila chemosensory protein induces behavioral defense against fungal parasitic infections. Curr Biol 33:276–286

    Article  CAS  PubMed  Google Scholar 

  • Shen D, Tang Z, Wang C et al (2019) Infection mechanisms and putative effector repertoire of the mosquito pathogenic oomycete Pythium guiyangense uncovered by genomic analysis. PLoS Genet 15:e1008116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen D, Nyawira KT, Xia A (2020) New discoveries and applications of mosquito fungal pathogens. Curr Opin Insect Sci 40:111–116

    Article  PubMed  Google Scholar 

  • Sheng H, McNamara PJ, St Leger RJ (2022) Metarhizium: an opportunistic middleman for multitrophic lifestyles. Curr Opin Microbiol 69:102176

    Article  PubMed  Google Scholar 

  • Shi XZ, Zhong X, Yu XQ (2012) Drosophila melanogaster NPC2 proteins bind bacterial cell wall components and may function in immune signal pathways. Insect Biochem Mol Biol 42:545–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shu R, Zhang J, Meng Q et al (2020) A new high-quality draft genome assembly of the Chinese Cordyceps Ophiocordyceps sinensis. Genome Biol Evol 12:1074–1079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JF Jr (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711

    Article  CAS  PubMed  Google Scholar 

  • St Leger RJ, Wang JB (2020) Metarhizium: jack of all trades, master of many. Open Biol 10:200307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St. Leger RJ (2021) Insects and their pathogens in a changing climate. J Invertebr Pathol 184:107644

    Article  PubMed  Google Scholar 

  • Staats CC, Junges A, Guedes RL et al (2014) Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics 15:822

    Article  PubMed  PubMed Central  Google Scholar 

  • Stuart LM, Paquette N, Boyer L (2013) Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nat Rev Immunol 13:199–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun YL, Hong S, Chen HM, Yin Y, Wang CS (2022a) Production of helvolic acid in Metarhizium contributes to fungal infection of insects by bacteriostatic inhibition of the host cuticular microbiomes. Microbiol Spectr 10:e0262022

    Article  PubMed  Google Scholar 

  • Sun YL, Chen B, Li XL, Yin Y, Wang CS (2022b) Orchestrated biosynthesis of the secondary metabolite cocktails enables the producing fungus to combat diverse bacteria. mBio 13:e0180022

    Article  PubMed  Google Scholar 

  • Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang D, Tang X, Fang W (2022) New downstream signaling branches of the mitogen-activated protein kinase cascades identified in the insect pathogenic and plant symbiotic fungus Metarhizium robertsii. Front Fungal Biol 3:911366

    Article  PubMed  PubMed Central  Google Scholar 

  • Thakur R, Shiratori T, Ishida KI (2019) Taxon-rich multigene phylogenetic analyses resolve the phylogenetic relationship among deep-branching Stramenopiles. Protist 170:125682

    Article  PubMed  Google Scholar 

  • Usman S, Ge X, Xu Y et al (2023) Loss of phosphomannose isomerase impairs growth, perturbs cell wall integrity, and reduces virulence of Fusarium oxysporum f. sp. cubense on banana plants. J Fungi (Basel) 9:478

    Article  CAS  PubMed  Google Scholar 

  • Valero-Jimenez CA, Faino L, Spring In’t Veld D, Smit S, Zwaan BJ, van Kan JA (2016) Comparative genomics of Beauveria bassiana: uncovering signatures of virulence against mosquitoes. BMC Genomics 17:986

    Article  PubMed  PubMed Central  Google Scholar 

  • van Wyk S, Wingfield BD, De Vos L, van der Merwe NA, Steenkamp ET (2021) Genome-wide analyses of repeat-induced point mutations in the Ascomycota. Front Microbiol 11:622368

    Article  PubMed  PubMed Central  Google Scholar 

  • Vega FE, Kaya HK (2012) Insect pathology, 2nd edn. Academic, San Diego, CA

    Google Scholar 

  • Vega FE, Goettel MS, Blackwell M et al (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  • Wang CS (2020) Grand challenges in the research of fungal interactions with animals. Front Fungal Biol 1:602032

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, St Leger RJ (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci U S A 103:6647–6652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, St Leger RJ (2007a) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang CS, St Leger RJ (2007b) The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J Biol Chem 282:21110–21115

    Article  CAS  PubMed  Google Scholar 

  • Wang CS, Wang SB (2017) Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol 62:73–90

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Skrobek A, Butt TM (2003) Concurrence of losing a chromosome and the ability to produce destruxins in a mutant of Metarhizium anisopliae. FEMS Microbiol Lett 226:373–378

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Kang Q, Lu Y, Bai LQ, Wang CS (2012) Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proc Natl Acad Sci U S A 109:1287–1292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JB, St Leger RJ, Wang C (2016) Advances in genomics of entomopathogenic fungi. Adv Genet 94:67–105

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Stata M, Wang W, Stajich JE, White MM, Moncalvo JM (2018) Comparative genomics reveals the core gene toolbox for the fungus-insect symbiosis. mBio 9:e0063618

    Article  Google Scholar 

  • Wang J, Weng Q, Hu Q (2019) Effects of Destruxin A on silkworm's immunophilins. Toxins (Basel) 11:349

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Deng Z, Wu H et al (2019b) A small secreted protein triggers a TLR2/4-dependent inflammatory response during invasive Candida albicans infection. Nat Commun 10:1015

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y-B, Wang Y, Fan Q et al (2020a) Multigene phylogeny of the family Cordycipitaceae (Hypocreales): new taxa and the new systematic position of the Chinese cordycipitoid fungus Paecilomyces hepiali. Fungal Divers 103:1–46

    Article  Google Scholar 

  • Wang Y, Nie Y, Yu D, Xie X, Qin L, Yang Y, Huang B (2020b) Genome-wide study of saprotrophy-related genes in the basal fungus Conidiobolus heterosporus. Appl Microbiol Biotechnol 104:6261–6272

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 114:5994–5999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whisler HC, Zebold SL, Shemanchuk JA (1975) Life history of Coelomomyces psorophorae. Proc Natl Acad Sci U S A 72:693–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wichadakul D, Kobmoo N, Ingsriswang S, Tangphatsornruang S, Chantasingh D, Luangsa-Ard JJ, Eurwilaichitr L (2015) Insights from the genome of Ophiocordyceps polyrhachis-furcata to pathogenicity and host specificity in insect fungi. BMC Genomics 16:881

    Article  PubMed  PubMed Central  Google Scholar 

  • Will I, Das B, Trinh T, Brachmann A, Ohm RA, de Bekker C (2020) Genetic Underpinnings of Host Manipulation by Ophiocordyceps as Revealed by Comparative Transcriptomics. G3 (Bethesda) 10:2275–2296

    Article  CAS  PubMed  Google Scholar 

  • Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7:185–195

    Article  CAS  PubMed  Google Scholar 

  • Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg JD (2010) Comparative virulence of Beauveria bassiana isolates against lepidopteran pests of vegetable crops. J Invertebr Pathol 103:186–199

    Article  CAS  PubMed  Google Scholar 

  • Xia EH, Yang DR, Jiang JJ et al (2017a) The caterpillar fungus, Ophiocordyceps sinensis, genome provides insights into highland adaptation of fungal pathogenicity. Sci Rep 7:1806

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia YL, Luo FF, Shang YF, Chen PL, Lu YZ, Wang CS (2017b) Fungal cordycepin biosynthesis is coupled with the production of the safeguard molecule pentostatin. Cell Chem Biol 24:1479–1489

    Article  CAS  PubMed  Google Scholar 

  • Xiao G, Ying SH, Zheng P et al (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Orozco R, Wijeratne EM, Gunatilaka AA, Stock SP, Molnar I (2008) Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chem Biol 15:898–907

    Article  CAS  PubMed  Google Scholar 

  • Xu Y-J, Luo F, Gao Q, Shang Y, Wang C (2015) Metabolomics reveals insect metabolic responses associated with fungal infection. Anal Bioanal Chem 407:4815–4821

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Feng P, Yin Y, Bushley K, Spatafora JW, Wang C (2018) Cyclosporine biosynthesis in Tolypocladium inflatum benefits fungal adaptation to the environment. MBio 9:e01211–e01218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Chen B, Song SX, Li B, Yang XQ, Wang CS (2020) Production of diverse beauveriolide analogs in closely related fungi: a rare case of fungal chemodiversity. mSphere 5:e0066720

    Article  Google Scholar 

  • Ying SH, Feng MG (2019) Insight into vital role of autophagy in sustaining biological control potential of fungal pathogens against pest insects and nematodes. Virulence 10:429–437

    Article  CAS  PubMed  Google Scholar 

  • Zeng G, Zhang P, Zhang Q et al (2018) Duplication of a Pks gene cluster and subsequent functional diversification facilitate environmental adaptation in Metarhizium species. PLoS Genet 14:e1007472

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Deng W, Yan W, Li T (2018) Whole genome sequence of an edible and potential medicinal fungus, Cordyceps guangdongensis. G3 (Bethesda) 8:1863–1870

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Fasoyin OE, Molnar I, Xu Y (2020a) Secondary metabolites from hypocrealean entomopathogenic fungi: novel bioactive compounds. Nat Prod Rep 37:1181–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Yue Q, Wang C, Xu Y, Molnar I (2020b) Secondary metabolites from hypocrealean entomopathogenic fungi: genomics as a tool to elucidate the encoded parvome. Nat Prod Rep 37:1164–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Meng Y, Huang Y, Zhang D, Fang W (2021) A novel cascade allows Metarhizium robertsii to distinguish cuticle and hemocoel microenvironments during infection of insects. PLoS Biol 19:e3001360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Xu C, Lu HL, Chen X, St Leger RJ, Fang W (2014) Host-to-pathogen gene transfer facilitated infection of insects by a pathogenic fungus. PLoS Pathog 10:e1004009

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng P, Xia Y, Xiao G et al (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12:R116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng P, Xia Y, Zhang S, Wang C (2013) Genetics of Cordyceps and related fungi. Appl Microbiol Biotechnol 97:2797–2804

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

The authors are highly appreciative of Drs. Meredith Blackwell and Yen-Peng Hsueh for their help in preparing this chapter. This work was supported by the National Key R&D Program of China (2022YFD1400700 and 2022YFD1400500).

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Hong, S., Shang, J., Sun, Y., Wang, C. (2024). Genetics and Infection Biology of the Entomopathogenic Fungi. In: Hsueh, YP., Blackwell, M. (eds) Fungal Associations. The Mycota, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-031-41648-4_13

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