Virulence Factors of the Entomopathogenic Genus Metarhizium

Author(s): Gloria A. González-Hernández, Israel E. Padilla-Guerrero*, Azul Martínez-Vázquez, Juan C. Torres-Guzmán.

Journal Name: Current Protein & Peptide Science

Volume 21 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

The fungal genus Metarhizium has been used as an entomopathogen worldwide for approximately 140 years, and its mechanism of infection and its virulence factors have been studied. The present review is a compilation of virulence factors described in the literature to date and their participation in specific stages of the infection process.

Keywords: Host insect, metchnikoff, insecticides, appressorium, pathogenicity factors, mechanism of infection, biological control.

[1]
Roberts, D.W.; St Leger, R.J. Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv. Appl. Microbiol., 2004, 54(1), 1-70.
[http://dx.doi.org/10.1016/S0065-2164(04)54001-7] [PMID: 15251275]
[2]
Lord, J.C. From Metchnikoff to Monsanto and beyond: the path of microbial control. J. Invertebr. Pathol., 2005, 89(1), 19-29.
[http://dx.doi.org/10.1016/j.jip.2005.04.006] [PMID: 16039302]
[3]
Brunner-Mendoza, C.; Reyes-Montes, M. delR.; Moonjely, S.; Bidochka, M.J.; Toriello, C. A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Sci. Technol., 2019, 29(1), 83-102.
[http://dx.doi.org/10.1080/09583157.2018.1531111]
[4]
Zimmermann, G. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci. Technol., 2007, 17(9), 879-920.
[http://dx.doi.org/10.1080/09583150701593963]
[5]
Bischoff, J.F.; Rehner, S.A.; Humber, R.A. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia, 2009, 101(4), 512-530.
[http://dx.doi.org/10.3852/07-202] [PMID: 19623931]
[6]
Wang, C.; Wang, S. Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu. Rev. Entomol., 2017, 62, 73-90.
[http://dx.doi.org/10.1146/annurev-ento-031616-035509] [PMID: 27860524]
[7]
Shah, F.A.; Wang, C.S.; Butt, T.M. Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol. Lett., 2005, 251(2), 259-266.
[http://dx.doi.org/10.1016/j.femsle.2005.08.010] [PMID: 16168581]
[8]
Wang, C.; St Leger, R.J. Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot. Cell, 2005, 4(5), 937-947.
[http://dx.doi.org/10.1128/EC.4.5.937-947.2005] [PMID: 15879528]
[9]
Clarkson, J.M.; Charnley, A.K. New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol., 1996, 4(5), 197-203.
[http://dx.doi.org/10.1016/0966-842X(96)10022-6] [PMID: 8727600]
[10]
Santi, L.; Beys da Silva, W.O.; Berger, M.; Guimarães, J.A.; Schrank, A.; Vainstein, M.H. Conidial surface proteins of Metarhizium anisopliae: Source of activities related with toxic effects, host penetration and pathogenesis. Toxicon, 2010, 55(4), 874-880.
[http://dx.doi.org/10.1016/j.toxicon.2009.12.012] [PMID: 20034509]
[11]
Wang, Z.; Zhou, Q.; Li, Y.; Qiao, L.; Pang, Q.; Huang, B. iTRAQ-based quantitative proteomic analysis of conidia and mycelium in the filamentous fungus Metarhizium robertsii. Fungal Biol., 2018, 122(7), 651-658.
[http://dx.doi.org/10.1016/j.funbio.2018.03.010] [PMID: 29880200]
[12]
Zhao, T.; Tian, H.; Xia, Y.; Jin, K. MaPmt4, a protein O-mannosyltransferase, contributes to cell wall integrity, stress tolerance and virulence in Metarhizium acridum. Curr. Genet., 2019, 65(4), 1025-1040.
[http://dx.doi.org/10.1007/s00294-019-00957-z] [PMID: 30911768]
[13]
St Leger, R.J.; Staples, R.C.; Roberts, D.W. Cloning and regulatory analysis of starvation-stress gene, ssgA, encoding a hydrophobin-like protein from the entomopathogenic fungus, Metarhizium anisopliae. Gene, 1992, 120(1), 119-124.
[http://dx.doi.org/10.1016/0378-1119(92)90019-L] [PMID: 1398117]
[14]
Wang, C.; St Leger, R.J. 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, 2007, 6(5), 808-816.
[http://dx.doi.org/10.1128/EC.00409-06] [PMID: 17337634]
[15]
St.Leger, R.J.; Butt, T.M.; Goettel, M.S.; Staples, R.C.; Roberts, D.W. Production in vitro of appressoria by the entomopathogenic fungus Metarhizium anisopliae. Exp. Mycol., 1989, 13(3), 274-288.
[http://dx.doi.org/10.1016/0147-5975(89)90049-2]
[16]
Vincent, J.F.V.; Wegst, U.G.K. Design and mechanical properties of insect cuticle. Arthropod Struct. Dev., 2004, 33(3), 187-199.
[http://dx.doi.org/10.1016/j.asd.2004.05.006] [PMID: 18089034]
[17]
St.Leger, R.J.; Goettel, M.; Roberts, D.W.; Staples, R.C. Prepenetration events during infection of host cuticle by Metarhizium anisopliae. J. Invertebr. Pathol., 1991, 58(2), 168-179.
[http://dx.doi.org/10.1016/0022-2011(91)90061-T]
[18]
Freimoser, F.M.; Hu, G.; St Leger, R.J. Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology, 2005, 151(Pt 2), 361-371.
[http://dx.doi.org/10.1099/mic.0.27560-0] [PMID: 15699187]
[19]
Fang, W.; Pava-ripoll, M.; Wang, S.; St Leger, R. Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Genet. Biol., 2009, 46(3), 277-285.
[http://dx.doi.org/10.1016/j.fgb.2008.12.001] [PMID: 19124083]
[20]
Gao, Q.; Jin, K.; Ying, S.H.; Zhang, Y.; Xiao, G.; Shang, Y.; Duan, Z.; Hu, X.; Xie, X.Q.; Zhou, G.; Peng, G.; Luo, Z.; Huang, W.; Wang, B.; Fang, W.; Wang, S.; Zhong, Y.; Ma, L.J.; St Leger, R.J.; Zhao, G.P.; Pei, Y.; Feng, M.G.; Xia, Y.; Wang, C. Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet., 2011, 7(1) e1001264
[http://dx.doi.org/10.1371/journal.pgen.1001264] [PMID: 21253567]
[21]
Wang, C.; St Leger, R.J. The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J. Biol. Chem., 2007, 282(29), 21110-21115.
[http://dx.doi.org/10.1074/jbc.M609592200] [PMID: 17526497]
[22]
Madrigal Pulido, J.; Padilla Guerrero, I. Magaña Martínez, Ide.J.; Cacho Valadez, B.; Torres Guzman, J.C.; Salazar Solis, E.; Felix Gutierrez Corona, J.; Schrank, A.; Jiménez Bremont, F.; González Hernandez, A. Isolation, characterization and expression analysis of the ornithine decarboxylase gene (ODC1) of the entomopathogenic fungus, Metarhizium anisopliae. Microbiol. Res., 2011, 166(6), 494-507.
[http://dx.doi.org/10.1016/j.micres.2010.10.002] [PMID: 21236653]
[23]
Padilla-Guerrero, I.E.; Barelli, L.; González-Hernández, G.A.; Torres-Guzmán, J.C.; Bidochka, M.J. Flexible metabolism in Metarhizium anisopliae and Beauveria bassiana: role of the glyoxylate cycle during insect pathogenesis. Microbiology, 2011, 157(Pt 1), 199-208.
[http://dx.doi.org/10.1099/mic.0.042697-0] [PMID: 20929953]
[24]
Fang, W.; Fernandes, É.K.K.; Roberts, D.W.; Bidochka, M.J.; St Leger, R.J. A laccase exclusively expressed by Metarhizium anisopliae during isotropic growth is involved in pigmentation, tolerance to abiotic stresses and virulence. Fungal Genet. Biol., 2010, 47(7), 602-607.
[http://dx.doi.org/10.1016/j.fgb.2010.03.011] [PMID: 20382249]
[25]
Guo, N.; Qian, Y.; Zhang, Q.; Chen, X.; Zeng, G.; Zhang, X.; Mi, W.; Xu, C.; St Leger, R.J.; Fang, W. Alternative transcription start site selection in Mr-OPY2 controls lifestyle transitions in the fungus Metarhizium robertsii. Nat. Commun., 2017, 8(1), 1565.
[http://dx.doi.org/10.1038/s41467-017-01756-1] [PMID: 29146899]
[26]
Wang, Z.; Jiang, Y.; Li, Y.; Feng, J.; Huang, B. MrArk1, an actin-regulating kinase gene, is required for endocytosis and involved in sustaining conidiation capacity and virulence in Metarhizium robertsii. Appl. Microbiol. Biotechnol., 2019, 103(12), 4859-4868.
[http://dx.doi.org/10.1007/s00253-019-09836-6] [PMID: 31025075]
[27]
Meng, Y.; Zhang, X.; Guo, N.; Fang, W. MrSt12 implicated in the regulation of transcription factor AFTF1 by Fus3-MAPK during cuticle penetration by the entomopathogenic fungus Metarhizium robertsii. Fungal Genet. Biol., 2019, 131 103244
[http://dx.doi.org/10.1016/j.fgb.2019.103244] [PMID: 31228645]
[28]
Wei, Q.; Du, Y.; Jin, K.; Xia, Y. The Ste12-like transcription factor MaSte12 is involved in pathogenicity by regulating the appressorium formation in the entomopathogenic fungus, Metarhizium acridum. Appl. Microbiol. Biotechnol., 2017, 101(23-24), 8571-8584.
[http://dx.doi.org/10.1007/s00253-017-8569-x] [PMID: 29079863]
[29]
Morales Hernández, C.E.; Padilla Guerrero, I.E.; González Hernández, G.A.; Salazar Solís, E.; Torres Guzmán, J.C. Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium anisopliae. Appl. Microbiol. Biotechnol., 2010, 87(3), 1033-1044.
[http://dx.doi.org/10.1007/s00253-010-2517-3] [PMID: 20361327]
[30]
Lin, L.; Fang, W.; Liao, X.; Wang, F.; Wei, D.; St Leger, R.J. The MrCYP52 cytochrome P450 monoxygenase gene of Metarhizium robertsii is important for utilizing insect epicuticular hydrocarbons. PLoS One, 2011, 6(12) e28984
[http://dx.doi.org/10.1371/journal.pone.0028984] [PMID: 22194968]
[31]
Wang, C.; St Leger, R.J. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc. Natl. Acad. Sci. USA, 2006, 103(17), 6647-6652.
[http://dx.doi.org/10.1073/pnas.0601951103] [PMID: 16614065]
[32]
Wang, C.; Duan, Z.; St Leger, R.J. MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryot. Cell, 2008, 7(2), 302-309.
[http://dx.doi.org/10.1128/EC.00310-07] [PMID: 18055914]
[33]
Jin, K.; Peng, G.; Liu, Y.; Xia, Y. The acid trehalase, ATM1, contributes to the in vivo growth and virulence of the entomopathogenic fungus, Metarhizium acridum. Fungal Genet. Biol., 2015, 77, 61-67.
[http://dx.doi.org/10.1016/j.fgb.2015.03.013] [PMID: 25865794]
[34]
Zhang, M.; Wei, Q.; Xia, Y.; Jin, K. MaPacC, a pH-responsive transcription factor, negatively regulates thermotolerance and contributes to conidiation and virulence in Metarhizium acridum. Curr. Genet., 2019. [Epub Ahead of Print
[http://dx.doi.org/10.1007/s00294-019-01032-3] [PMID: 31471639]
[35]
Song, D.; Shi, Y.; Ji, H.; Xia, Y.; Peng, G. The MaCreA gene regulates normal conidiation and microcycle conidiation in Metarhizium acridum. Front. Microbiol., 2019, 10, 1946.
[http://dx.doi.org/10.3389/fmicb.2019.01946] [PMID: 31497008]
[36]
Fang, W.; Pei, Y.; Bidochka, M.J. A regulator of a G protein signalling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation, virulence and hydrophobin synthesis. Microbiology, 2007, 153(Pt 4), 1017-1025.
[http://dx.doi.org/10.1099/mic.0.2006/002105-0] [PMID: 17379711]
[37]
Oliveira, A.S.; Braga, G.U.L.; Rangel, D.E.N. Metarhizium robertsii illuminated during mycelial growth produces conidia with increased germination speed and virulence. Fungal Biol., 2018, 122(6), 555-562.
[http://dx.doi.org/10.1016/j.funbio.2017.12.009] [PMID: 29801800]
[38]
Angelone, S.; Piña-Torres, I.H.; Padilla-Guerrero, I.E.; Bidochka, M.J. “Sleepers” and “Creepers”: a theoretical study of colony polymorphisms in the fungus Metarhizium related to insect pathogenicity and plant rhizosphere colonization. Insects, 2018, 9(3), 104.
[http://dx.doi.org/10.3390/insects9030104] [PMID: 30126092]
[39]
Hu, X.; Xiao, G.; Zheng, P.; Shang, Y.; Su, Y.; Zhang, X.; Liu, X.; Zhan, S.; St Leger, R.J.; Wang, C. Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc. Natl. Acad. Sci. USA, 2014, 111(47), 16796-16801.
[http://dx.doi.org/10.1073/pnas.1412662111] [PMID: 25368161]
[40]
Pattemore, J.A.; Hane, J.K.; Williams, A.H.; Wilson, B.A.L.; Stodart, B.J.; Ash, G.J. The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics, 2014, 15(1), 660.
[http://dx.doi.org/10.1186/1471-2164-15-660] [PMID: 25102932]
[41]
Staats, C.C.; Junges, A.; Guedes, R.L.; Thompson, C.E.; de Morais, G.L.; Boldo, J.T.; de Almeida, L.G.; Andreis, F.C.; Gerber, A.L.; Sbaraini, N.; da Paixão, R.L.; Broetto, L.; Landell, M.; Santi, L.; Beys-da-Silva, W.O.; Silveira, C.P.; Serrano, T.R.; de Oliveira, E.S.; Kmetzsch, L.; Vainstein, M.H.; de Vasconcelos, A.T.; Schrank, A. Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics, 2014, 15(1), 822.
[http://dx.doi.org/10.1186/1471-2164-15-822] [PMID: 25263348]
[42]
Al-Aidroos, K.; Roberts, D.W. Mutants of Metarhizium anisopliae with increase virulence toward mosquito larvae. Can. J. Genet. Cytol., 1978, 20(2), 211-219.
[http://dx.doi.org/10.1139/g78-024]
[43]
St Leger, R.; Joshi, L.; Bidochka, M.J.; Roberts, D.W. Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc. Natl. Acad. Sci. USA, 1996, 93(13), 6349-6354.
[http://dx.doi.org/10.1073/pnas.93.13.6349] [PMID: 8692818]
[44]
Wang, C.; St Leger, R.J. A scorpion neurotoxin increases the potency of a fungal insecticide. Nat. Biotechnol., 2007, 25(12), 1455-1456.
[http://dx.doi.org/10.1038/nbt1357] [PMID: 17994009]
[45]
Fang, W.; Vega-Rodríguez, J.; Ghosh, A.K.; Jacobs-Lorena, M.; Kang, A.; St Leger, R.J. Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science, 2011, 331(6020), 1074-1077.
[http://dx.doi.org/10.1126/science.1199115] [PMID: 21350178]
[46]
Fang, W.; Lu, H.L.; King, G.F.; St Leger, R.J. Construction of a hypervirulent and specific mycoinsecticide for locust control. Sci. Rep., 2014, 4, 7345.
[http://dx.doi.org/10.1038/srep07345] [PMID: 25475694]
[47]
Bilgo, E.; Lovett, B.; Fang, W.; Bende, N.; King, G.F.; Diabate, A.; St Leger, R.J. Improved efficacy of an arthropod toxin expressing fungus against insecticide-resistant malaria-vector mosquitoes. Sci. Rep., 2017, 7(1), 3433.
[http://dx.doi.org/10.1038/s41598-017-03399-0] [PMID: 28611355]
[48]
Lovett, B.; Bilgo, E.; Millogo, S.A.; Ouattarra, A.K.; Sare, I.; Gnambani, E.J.; Dabire, R.K.; Diabate, A.; St Leger, R.J. Transgenic Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso. Science, 2019, 364(6443), 894-897.
[http://dx.doi.org/10.1126/science.aaw8737] [PMID: 31147521]
[49]
Small, C.L.N.; Bidochka, M.J. Up-regulation of Prl, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycol. Res., 2005, 109(Pt 3), 307-313.
[http://dx.doi.org/10.1017/S0953756204001856] [PMID: 15912947]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 3
Year: 2020
Page: [324 - 330]
Pages: 7
DOI: 10.2174/1389203721666200116092407
Price: $65

Article Metrics

PDF: 11
HTML: 2