Abstract
Vectors have been wreaking a fatal havoc on mankind by causing diseases in agriculturally important plants and humans. Not only diseases caused by them are a hefty task to deal with, but their increasingly successful survival in human settlements is also a rising concern. The entomopathogenic fungi are considered amongst the first organisms for bio management of agriculturally important pests as they are eco-friendly, economically sustainable, and effective. With this, the collateral need for biocontrol in human disease vectors is also being felt. The first observation of fungi infecting insects was in as early as 900 AD, to the first data published in 1726 about entomopathogenic fungi. Metarhizium is a widespread fungus found all over the globe. More than 200 species of insects are infected by the fungus thereby making it one of the most sought biocontrol agents. This chapter gives an understanding of interaction between an arthropod host and entomopathogenic fungi genera Metarhizium, description of the host and fungal structure, what are some of the conventional and recent efforts done in order to improve the application strategies and what could be some of the possible uses of Metarhizium in enhancing plant health. Some of the plant pests and animal vectors which have been explored as host for Metarhizium are also mentioned.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alkhaibari AM, Maffeis T, Bull JC, Butt TM (2018) Combined use of the entomopathogenic fungus, Metarhizium brunneum, and the mosquito predator, Toxorhynchites brevipalpis, for control of mosquito larvae: is this a risky biocontrol strategy? J Invertebr Pathol 153:38–50. https://doi.org/10.1016/j.jip.2018.02.003
Amiri B, Ibrahim L, Butt TM (1999) Antifeedant properties of Destruxins and their potential use with the Entomogenous fungus Metarhizium anisopliae for improved control of crucifer pests. Biocontrol Sci Tech 9:487–498. https://doi.org/10.1080/09583159929451
Aw KMS, Hue SM (2017) Mode of Infection of Metarhizium spp. fungus and their potential as biological control agents. J Fungi 3(2):30
Barelli L, Moreira CC, Bidochka MJ (2018) Initial stages of endophytic colonization by metarhizium involves Rhizoplane colonization. Microbiol (United Kingdom). https://doi.org/10.1099/mic.0.000729
Behie SW, Bidochka MJ (2014) Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Appl Environ Microbiol 80:1553–1560. https://doi.org/10.1128/AEM.03338-13
Barkai-Golan R (2001) chapter 2 - postharvest disease initiation. In: Barkai-golan (ed) RBT-PD of F and V. Elsevier, Amsterdam, pp 3–24
Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic Fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577. https://doi.org/10.1126/science.1222289
Behie SW, Moreira CC, Sementchoukova I et al (2017) Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nat Commun 8:14245. https://doi.org/10.1038/ncomms14245
Beys da Silva WO, Santi L, Schrank A, Vainstein MH (2010) Metarhizium anisopliae lipolytic activity plays a pivotal role in Rhipicephalus (Boophilus) microplus infection. Fungal Biol 114(1):10–15
Bhattacharya A (2019) Effect of high-temperature stress on the metabolism of plant growth regulators, chapter 6. Academic Press, New York, pp 485–591
Bilgo E, Lovett B, St. Leger RJ et al (2018) Native entomopathogenic Metarhizium spp. from Burkina Faso and their virulence against the malaria vector Anopheles coluzzii and non-target insects. Parasit Vectors 11:209. https://doi.org/10.1186/s13071-018-2796-6
Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530. https://doi.org/10.3852/07-202
Bittencourt VREP, Mascarenhas AG, de Menezes GCR, Monteiro SG (2000) In vitro action of Metarhizium anisopliae (Metschnikoff, 1879) Sorokin, 1883 and Beauveria bassiana (Balsamo) Vuillemin, 1912 on eggs of the tick Anocentor nitens (Neummann, 1897) (Acari: Ixodidae). Rev Bras Med Veterinária 22:248–251
Blanford S, Read AF, Thomas MB (2009) Thermal behaviour of Anopheles stephensi in response to infection with malaria and fungal entomopathogens. Malar J 8:72. https://doi.org/10.1186/1475-2875-8-72
Brancini GTP, Ferreira MES, Rangel DEN, Braga GÚL (2019) Combining Transcriptomics and proteomics reveals potential post-transcriptional control of gene expression after light exposure in Metarhizium acridum. G3 (Bethesda) 9:2951–2961. https://doi.org/10.1534/g3.119.400430
Branine M, Bazzicalupo A, Branco S, Hogan DA (2019) Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog 15(7):e1007831
Brown JC (1956) Iron chlorosis. Annu Rev Plant Physiol 7:171–190. https://doi.org/10.1146/annurev.pp.07.060156.001131
Bukhari T, Takken W, Koenraadt CJM (2011) Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasit Vectors 4:23. https://doi.org/10.1186/1756-3305-4-23
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016a) Chapter nine - Entomopathogenic Fungi: new insights into host–pathogen interactions. In: Lovett B, St. Leger RJ (eds) Genetics and molecular biology of Entomopathogenic fungi. Academic Press, New York, pp 307–364
Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016b) Entomopathogenic Fungi: new insights into host-pathogen interactions. Adv Genet 94:307–364. https://doi.org/10.1016/bs.adgen.2016.01.006
Canassa F, Tall S, Moral RA et al (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
Carolino AT, Paula AR, Silva CP et al (2014) Monitoring persistence of the entomopathogenic fungus Metarhizium anisopliae under simulated field conditions with the aim of controlling adult Aedes aegypti (Diptera: Culicidae). Parasit Vectors 7:198. https://doi.org/10.1186/1756-3305-7-198
Chandler D, Bailey AS, Tatchell GM et al (2011) The development, regulation and use of biopesticides for integrated pest management. Philos Trans R Soc Lond Ser B Biol Sci 366:1987–1998. https://doi.org/10.1098/rstb.2010.0390
Chapman RF (2012) The insects: structure and function, 5th edn. Cambridge University Press, Cambridge
Charnley AK (2003) Fungal pathogens of insects: cuticle degrading enzymes and toxins. Academic Press, New York, pp 241–321
Constanza Mannino M, 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
Contreras J, Mendoza JE, Martinez-Aguirre MR et al (2014) Efficacy of enthomopathogenic fungus Metarhizium anisopliae against Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 107:121–124. https://doi.org/10.1603/ec13404
Donzelli BGG, Krasnoff SB (2016) Molecular genetics of secondary chemistry in Metarhizium fungi. Adv Genet 94:365–436. https://doi.org/10.1016/bs.adgen.2016.01.005
Dornetshuber-Fleiss R, Heffeter P, Mohr T et al (2013) Destruxins: fungal-derived cyclohexadepsipeptides with multifaceted anticancer and antiangiogenic activities. Biochem Pharmacol 86:361–377. https://doi.org/10.1016/j.bcp.2013.05.022
Erler F, Ates AO (2015) Potential of two entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae (Coleoptera: Scarabaeidae), as biological control agents against the June beetle. J Insect Sci 15:44. https://doi.org/10.1093/jisesa/iev029
Farenhorst M, Knols BGJ (2010) A novel method for standardized application of fungal spore coatings for mosquito exposure bioassays. Malar J 9:27. https://doi.org/10.1186/1475-2875-9-27
Farenhorst M, Farina D, Scholte E-J et al (2008) African water storage pots for the delivery of the entomopathogenic fungus Metarhizium anisopliae to the malaria vectors Anopheles gambiae s.s. and Anopheles funestus. Am J Trop Med Hyg 78:910–916
Farenhorst M, Mouatcho JC, Kikankie CK et al (2009) Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc Natl Acad Sci USA 106:17443–17447. https://doi.org/10.1073/pnas.0908530106
Fernandes EKK, Keyser CA, Chong JP et al (2010) Characterization of Metarhizium species and varieties based on molecular analysis, heat tolerance and cold activity. J Appl Microbiol 108:115–128. https://doi.org/10.1111/j.1365-2672.2009.04422.x
Garcia ARM, de Rocha AP, Moreira CC et al (2016) Screening of fungi for biological control of a Triatomine vector of Chagas disease: temperature and trypanosome infection as factors. PLoS Negl Trop Dis 10:e0005128–e0005128. https://doi.org/10.1371/journal.pntd.0005128
Gauthier GM, Keller NP (2013) Crossover fungal pathogens: the biology and pathogenesis of fungi capable of crossing kingdoms to infect plants and humans. Fungal Genet Biol 61:146–157. https://doi.org/10.1016/J.FGB.2013.08.016
Glare TR, Milner RJ, Beaton CD (1996) Variation in Metarhizium, a genus of fungal pathogens attacking Orthoptera: is Phialide morphology a useful taxonomic criterion? J Orthoptera Res 5:19–27. https://doi.org/10.2307/3503572
Goble TA, Gardescu S, Jackson MA, Hajek AE (2016) Evaluating different carriers of Metarhizium brunneum F52 microsclerotia for control of adult Asian longhorned beetles (Coleoptera: Cerambycidae). Biocontrol Sci Tech 26:1212–1229. https://doi.org/10.1080/09583157.2016.1192103
Golo PS, Gardner DR, Grilley MM et al (2014) Production of destruxins from Metarhizium spp. fungi in artificial medium and in endophytically colonized cowpea plants. PLoS One 9:e104946–e104946. https://doi.org/10.1371/journal.pone.0104946
Gomes SA, Paula AR, Ribeiro A et al (2015) Neem oil increases the efficiency of the entomopathogenic fungus Metarhizium anisopliae for the control of Aedes aegypti (Diptera: Culicidae) larvae. Parasit Vectors 8:669. https://doi.org/10.1186/s13071-015-1280-9
González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16. https://doi.org/10.1111/j.1570-7458.2011.01187.x
Götz P, Matha V, Vilcinskas A (1997) Effects of the entomopathogenic fungus Metarhizium anisopliae and its secondary metabolites on morphology and cytoskeleton of plasmatocytes isolated from the greater wax moth, galleria mellonella. J Insect Physiol 43(12):1149–1159. https://doi.org/10.1016/s0022-1910(97)00066-8
Greenfield BPJ, Lord AM, Dudley E, Butt TM (2014) Conidia of the insect pathogenic fungus, Metarhizium anisopliae, fail to adhere to mosquito larval cuticle. R Soc Open Sci 1:140193. https://doi.org/10.1098/rsos.140193
Greenfield M, Gómez-Jiménez MI, Ortiz V et al (2016) Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control theory Appl Pest Manag 95:40–48. https://doi.org/10.1016/j.biocontrol.2016.01.002
Hajek AE, St. Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322. https://doi.org/10.1146/annurev.en.39.010194.001453
Hancock PA (2009) Combining fungal biopesticides and insecticide-treated bednets to enhance malaria control. PLoS Comput Biol 5:e1000525–e1000525. https://doi.org/10.1371/journal.pcbi.1000525
Hu S, Bidochka MJ (2019) Root colonization by endophytic insect-pathogenic fungi. J Appl Microbiol. https://doi.org/10.1111/jam.14503
Hussain A (2018) Reprogramming the virulence: insect defense molecules navigating the epigenetic landscape of Metarhizium robertsii. Virulence 9:447–449. https://doi.org/10.1080/21505594.2017.1421828
Indriyanti DR, Widiyaningrum P, Haryuni H et al (2017) Effectiveness of Metarhizium anisopliae and entomopathogenic nematodes to control Oryctes rhinoceros larvae in the rainy season. Pakistan J Biol Sci 20:320–327. https://doi.org/10.3923/pjbs.2017.320.327
Iwanicki NSA, Pereira AA, Botelho ABRZ et al (2019) Monitoring of the field application of Metarhizium anisopliae in Brazil revealed high molecular diversity of Metarhizium spp in insects, soil and sugarcane roots. Sci Rep 9:4443. https://doi.org/10.1038/s41598-019-38594-8
Jaber LR (2018) Seed inoculation with endophytic fungal entomopathogens promotes plant growth and reduces crown and root rot (CRR) caused by Fusarium culmorum in wheat. Planta 248:1525–1535. https://doi.org/10.1007/s00425-018-2991-x
Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Technol 27:28–41. https://doi.org/10.1080/09583157.2016.1243227
James PJ, Kershaw MJ, Reynolds SE, Charnley AK (1993) Inhibition of desert locust (Schistocerca gregaria) Malpighian tubule fluid secretion by destruxins, cyclic peptide toxins from the insect pathogenic fungus Metarhizium anisopliae. J Insect Physiol 39:797–804. https://doi.org/10.1016/0022-1910(93)90056-W
Kamareddine L (2012) The biological control of the malaria vector. Toxins (Basel) 4:748–767. https://doi.org/10.3390/toxins4090748
Kanga LHB, Adamczyk J, Patt J et al (2010) Development of a user-friendly delivery method for the fungus Metarhizium anisopliae to control the ectoparasitic mite Varroa destructor in honey bee, Apis mellifera, colonies. Exp Appl Acarol 52:327–342. https://doi.org/10.1007/s10493-010-9369-5
Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29. https://doi.org/10.1016/j.tplants.2004.12.003
Kershaw MJ, Talbot NJ (2009) Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci 106(37):15967–15972
Kirkland BH, Westwood GS, Keyhani NO (2004) Pathogenicity of Entomopathogenic Fungi Beauveria bassiana and Metarhizium anisopliae to Ixodidae tick species Dermacentor variabilis, Rhipicephalus sanguineus, and Ixodes scapularis. J Med Entomol 41:705–711. https://doi.org/10.1603/0022-2585-41.4.705
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
Kryukov VY, Kabilov MR, Smirnova N et al (2019) Bacterial decomposition of insects post-metarhizium infection, possible influence on plant growth. Fungal Biol 123(12):927–935. https://doi.org/10.1016/J.FUNBIO.2019.09.012
Kurtti TJ, Keyhani NO (2008) Intracellular infection of tick cell lines by the entomopathogenic fungus Metarhizium anisopliae. Microbiology 154:1700–1709. https://doi.org/10.1099/mic.0.2008/016667-0
Lacey CM, Lacey LA, Roberts DR (1988) Route of invasion and histopathology of Metarhizium anisopliae in Culex quinquefasciatus. J Invertebr Pathol 52:108–118. https://doi.org/10.1016/0022-2011(88)90109-7
Lavine MD, Strand MR (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309. https://doi.org/10.1016/s0965-1748(02)00092-9
Leger RJS, Goettel M, Roberts DW, Staples RC (1991a) Prepenetration events during infection of host cuticle by Metarhizium anisopliae. J Invertebr Pathol 58:168–179. https://doi.org/10.1016/0022-2011(91)90061-T
Leger RJS, Roberts DW, Staples RC (1991b) A model to explain differentiation of appressoria by germlings of Metarhizium anisopliae. J Invertebr Pathol 57:299–310. https://doi.org/10.1016/0022-2011(91)90134-C
Li L, Ortiz C (2014) Pervasive nanoscale deformation twinning as a catalyst for efficient energy dissipation in a bioceramic armour. Nat Mater 13:501–507. https://doi.org/10.1038/nmat3920
Liao X, O’Brien T, Fang W, St Leger R (2014) The plant beneficial effects of Metarhizium species correlate with their association with roots. Appl Microbiol Biotechnol 98. https://doi.org/10.1007/s00253-014-5788-2
Liao X, Lovett B, Fang W, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163:980–991. https://doi.org/10.1099/mic.0.000494
Liu X-H, Gao H-M, Xu F et al (2012) Autophagy vitalizes the pathogenicity of pathogenic fungi. Autophagy 8:1415–1425. https://doi.org/10.4161/auto.21274
Lovett B, St Leger RJ (2018) Genetically engineering better fungal biopesticides. Pest Manag Sci 74:781–789. https://doi.org/10.1002/ps.4734
Lovett B, Bilgo E, Millogo SA et al (2019) Transgenic Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso. Science 364:894–897. https://doi.org/10.1126/science.aaw8737
Lwetoijera DW, Sumaye RD, Madumla EP et al (2010) An extra-domiciliary method of delivering entomopathogenic fungus, Metharizium anisopliae IP 46 for controlling adult populations of the malaria vector, Anopheles arabiensis. Parasit Vectors 3:18. https://doi.org/10.1186/1756-3305-3-18
Mantzoukas S, Chondrogiannis C, Grammatikopoulos G (2015) Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomol Exp Appl 154:78–87. https://doi.org/10.1111/eea.12262
Mkiga AM, Mohamed SA, du Plessis H et al (2020) Metarhizium anisopliae and Beauveria bassiana: pathogenicity, horizontal transmission, and their effects on reproductive potential of Thaumatotibia leucotreta (Lepidoptera: Tortricidae). J Econ Entomol 113(2):660–668. https://doi.org/10.1093/jee/toz342
Mnyone LL, Kirby MJ, Mpingwa MW et al (2011) Infection of Anopheles gambiae mosquitoes with entomopathogenic fungi: effect of host age and blood-feeding status. Parasitol Res 108:317–322. https://doi.org/10.1007/s00436-010-2064-y
Mnyone LL, Lyimo IN, Lwetoijera DW et al (2012) Exploiting the behaviour of wild malaria vectors to achieve high infection with fungal biocontrol agents. Malar J 11:87. https://doi.org/10.1186/1475-2875-11-87
Mondal S, Baksi S, Koris A, Vatai G (2016) Journey of enzymes in entomopathogenic fungi. Pacific Sci Rev A Nat Sci Eng 18:85–99. https://doi.org/10.1016/j.psra.2016.10.001
Money NP (2016) Chapter 3 - Spore production, discharge, and dispersal. In: Watkinson SC, Boddy L, Money NP (eds) The fungi, 3rd edn. Academic Press, Boston, pp 67–97
Moonjely S, Barelli L, Bidochka MJ (2016) Insect pathogenic fungi as endophytes. Adv Genet. https://doi.org/10.1016/bs.adgen.2015.12.004
Moonjely S, Zhang X, Fang W, Bidochka MJ (2019) Metarhizium robertsii ammonium permeases (MepC and Mep2) contribute to rhizoplane colonization and modulates the transfer of insect derived nitrogen to plants. PLoS One 14:e0223718. https://doi.org/10.1371/journal.pone.0223718
Moore D, Bateman RP, Carey M, Prior C (1995) Long-term storage of Metarhizium flavoviride conidia in oil formulations for the control of locusts and grasshoppers. Biocontrol Sci Technol 5:193–200. https://doi.org/10.1080/09583159550039918
Muerrle TM, Neumann P, Dames JF et al (2006) Susceptibility of adult Aethina tumida (Coleoptera: Nitidulidae) to entomopathogenic fungi. J Econ Entomol 99:1–6. https://doi.org/10.1093/jee/99.1.1
Mukherjee K, Vilcinskas A (2018) The entomopathogenic fungus Metarhizium robertsii communicates with the insect host galleria mellonella during infection. Virulence 9(1):402–413. https://doi.org/10.1080/21505594.2017.1405190
Narladkar BW, Shivpuje PR, Harke PC (2015) Fungal biological control agents for integrated management of Culicoides spp. (Diptera: Ceratopogonidae) of livestock. Vet World 8:156–163. https://doi.org/10.14202/vetworld.2015.156-163
Okumu F, Biswaro L, Mbeleyela E et al (2010) Using nylon strips to dispense mosquito attractants for sampling the malaria vector Anopheles gambiae s.s. J Med Entomol 47:274–282. https://doi.org/10.1603/me09114
Ondiaka SN, Masinde EW, Koenraadt CJM et al (2015) Effects of fungal infection on feeding and survival of Anopheles gambiae (Diptera: Culicidae) on plant sugars. Parasit Vectors 8:35. https://doi.org/10.1186/s13071-015-0654-3
Onsongo SK, Gichimu BM, Akutse KS et al (2019) Performance of three isolates of Metarhizium Anisopliae and their virulence against Zeugodacus Cucurbitae under different temperature regimes, with global extrapolation of their efficiency. Insects 10:270. https://doi.org/10.3390/insects10090270
Pandey V, Bhatt ID, Nandi SK (2019) Chapter 20 - Role and regulation of auxin signaling in abiotic stress tolerance. In: MIR K, Reddy PS, Ferrante A, Khan N (eds) Plant signaling molecules. Woodhead Publishing, Sawston, pp 319–331
Pendeville H, Carpino N, Marine J-C, Takahashi Y, Muller M, Martial JA, Cleveland JL (2001) The ornithine decarboxylase gene is essential for cell survival during early murine development. Mol Cell Biol 21(19):6549–6558
Peng G, Xia Y (2015) Integration of an insecticidal scorpion toxin (BjαIT) gene into Metarhizium acridum enhances fungal virulence towards Locusta migratoria manilensis. Pest Manag Sci 71:58–64. https://doi.org/10.1002/ps.3762
Peng G, Jin K, Liu Y, Xia Y (2015) Enhancing the utilization of host trehalose by fungal trehalase improves the virulence of fungal insecticide. Appl Microbiol Biotechnol 99:8611–8618. https://doi.org/10.1007/s00253-015-6767-y
Pryor MGM (1940) On the hardening of the cuticle of insects. Proc R Soc Lond Ser B Biol Sci 128:393–407
Pulido JM, Guerrero IP, Martínez IJM, Valadez BC, Guzman JCT, Solis ES, Corona JFG, Schrank A, Bremont FJ, Hernandez AG (2011) Isolation, characterization and expression analysis of the ornithine decarboxylase gene (ODC1) of the entomopathogenic fungus, Metarhizium anisopliae. Microbiol Res 166(6):494–507
Rasgon JL (2011) Using infections to fight infections: paratransgenic fungi can block malaria transmission in mosquitoes. Future Microbiol 6:851–853. https://doi.org/10.2217/fmb.11.71
Raya-Diaz S, Sanchez-Rodriguez AR, Segura-Fernandez JM et al (2017) Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS One 12:e0185903. https://doi.org/10.1371/journal.pone.0185903
Russell PJ, Hertz PE, McMillan B (2016) Biology: the dynamic science. Cengage Learning, Belmont, CA
Sánchez-Rodríguez AR, Barrón V, Del Campillo MC, Quesada-Moraga E (2016) The entomopathogenic fungus Metarhizium brunneum: a tool for alleviating Fe chlorosis. Plant Soil 406:295–310. https://doi.org/10.1007/s11104-016-2887-0
Sandhu SS, Sharma AK, Beniwal V et al (2012) Myco-biocontrol of insect pests: factors involved, mechanism, and regulation. J Pathog 2012:126819. https://doi.org/10.1155/2012/126819
Santi L, Beys da Silva WO, Berger M et al (2010) Conidial surface proteins of Metarhizium anisopliae: source of activities related with toxic effects, host penetration and pathogenesis. Toxicon 55:874–880. https://doi.org/10.1016/j.toxicon.2009.12.012
Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107. https://doi.org/10.3732/ajb.1100136
Scholte E-J, Knols BGJ, Samson RA, Takken W (2004) Entomopathogenic fungi for mosquito control: a review. J Insect Sci 4:19. https://doi.org/10.1093/jis/4.1.19
Scholte E-J, Takken W, Knols BGJ (2007) Infection of adult Aedes aegypti and Ae. albopictus mosquitoes with the entomopathogenic fungus Metarhizium anisopliae. Acta Trop 102:151–158. https://doi.org/10.1016/j.actatropica.2007.04.011
Screen S, Bailey A, Charnley K, Cooper R, Clarkson J (1997) Carbon regulation of the cuticle-degrading enzyme PR1 from Metarhizium anisopliae may involve a trans-acting DNA-binding protein CRR1, a functional equivalent of the Aspergillus nidulans CREA protein. Curr Genet 31(6):511–518
Senthil Kumar CM, Jacob TK, Devasahayam S et al (2018) Multifarious plant growth promotion by an entomopathogenic fungus Lecanicillium psalliotae. Microbiol Res 207:153–160. https://doi.org/10.1016/J.MICRES.2017.11.017
Shukla E, Thorat LJ, Nath BB, Gaikwad SM (2015) Insect trehalase: Physiological significance and potential applications. Glycobiology 25(4):357–367
Sinha KK, Choudhary AK, Kumari P (2016) Chapter 15 - Entomopathogenic fungi. In: Omkar BT (ed) Ecofriendly pest management for food security. Academic Press, Cambridge, MA, pp 475–505
Sookar P, Bhagwant S, Allymamod MN (2014) Effect of Metarhizium anisopliae on the fertility and fecundity of two species of fruit flies and horizontal transmission of Mycotic infection. J Insect Sci 14:1–12
Sowers AD, Young SP, Grosell M, Browdy CL, Tomasso JR (2006) Hemolymph osmolality and cation concentrations in Litopenaeus vannamei during exposure to artificial sea salt or a mixed-ion solution: relationship to potassium flux. Comp Biochem Physiol A Mol Integr Physiol 145(2):176–180
St Leger R, Joshi L, Bidochka MJ, Roberts DW (1996) Construction of an improved mycoinsecticide overexpressing a toxic protease. Proc Natl Acad Sci USA 93:6349–6354. https://doi.org/10.1073/pnas.93.13.6349
Sun J, Fuxa JR, Henderson G (2002) Sporulation of Metarhizium anisopliae and Beauveria bassiana on Coptotermes formosanus and in vitro. J Invertebr Pathol 81:78–85. https://doi.org/10.1016/s0022-2011(02)00152-0
Sunde M, Kwan AHY, Templeton MD et al (2008) Structural analysis of hydrophobins. Micron 39:773–784. https://doi.org/10.1016/j.micron.2007.08.003
Theopold U, Schmidt O, Söderhäll K, Dushay MS (2004) Coagulation in arthropods: defence, wound closure and healing. Trends Immunol 25:289–294. https://doi.org/10.1016/j.it.2004.03.004
Thines E, Weber RW, Talbot NJ (2000) MAP kinase and protein kinase A: dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12:1703–1718. https://doi.org/10.1105/tpc.12.9.1703
Toei M, Saum R, Forgac M (2010) Regulation and isoform function of the V-ATPases. Biochemistry 49:4715–4723. https://doi.org/10.1021/bi100397s
Wamiti LG, Khamis FM, Abd-Alla AMM et al (2018) Metarhizium anisopliae infection reduces Trypanosoma congolense reproduction in Glossina fuscipes fuscipes and its ability to acquire or transmit the parasite. BMC Microbiol 18:142. https://doi.org/10.1186/s12866-018-1277-6
Wang C, St Leger RJ (2007) The Metarhizium anisopliae Perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. J Biol Chem 282:21110–21115. https://doi.org/10.1074/jbc.M609592200
Wang C, Duan Z, St. Leger RJ (2008) MOS1 Osmosensor of Metarhizium anisopliae Is Required for Adaptation to Insect Host Hemolymph. Eukaryot Cell 7(2):302–309
Wang S, Fang W, Wang C, St Leger RJ (2011) Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathog 7:e1002097–e1002097. https://doi.org/10.1371/journal.ppat.1002097
Wang Y, Wang T, Qiao L, Zhu J, Fan J, Zhang T, Wang Z-X, Li W, Chen A, Huang B (2017a) DNA methyltransferases contribute to the fungal development, stress tolerance and virulence of the entomopathogenic fungus Metarhizium robertsii. Appl Microbiol Biotechnol 101(10):4215–4226. https://doi.org/10.1007/s00253-017-8197-5
Wang W, Shi J, Xie Q et al (2017b) Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol Plant 10:1147–1158. https://doi.org/10.1016/J.MOLP.2017.07.012
Wu C, Zhang X, Fang W (2019) Increasing pyruvate concentration enhances conidial thermotolerance in the entomopathogenic fungus Metarhizium robertsii. Front Microbiol 10:519. https://doi.org/10.3389/fmicb.2019.00519
Wyatt GR (1961) The Biochemistry of Insect Hemolymph. Annu Rev Entomol 6(1):75–102
Xia Y, Clarkson JM, Charnley AK (2002) Trehalose-hydrolysing enzymes of Metarhizium anisopliae and their role in pathogenesis of the tobacco hornworm, Manduca sexta. J Invertebr Pathol 80(3):139–147
Yamamoto K, Ohmae M, Orihara T (2019) Metarhizium brachyspermum sp. nov. (Clavicipitaceae), a new species parasitic on Elateridae from Japan. Mycoscience 61(1):37–42. https://doi.org/10.1016/J.MYC.2019.09.001
Yousef M, Alba-Ramírez C, Garrido Jurado I et al (2018) Metarhizium brunneum (Ascomycota; Hypocreales) treatments targeting olive fly in the soil for sustainable crop production. Front Plant Sci 9:1. https://doi.org/10.3389/fpls.2018.00001
Zhang W, Chen J, Keyhani NO et al (2015) Comparative transcriptomic analysis of immune responses of the migratory locust, Locusta migratoria, to challenge by the fungal insect pathogen, Metarhizium acridum. BMC Genomics 16:867. https://doi.org/10.1186/s12864-015-2089-9
Zhang J, Huang W, Yuan C et al (2017) Prophenoloxidase-mediated ex vivo immunity to delay fungal infection after insect Ecdysis. Front Immunol 8:1445. https://doi.org/10.3389/fimmu.2017.01445
Zhang J, Jiang H, Du Y et al (2019) Members of chitin synthase family in Metarhizium acridum differentially affect fungal growth, stress tolerances, cell wall integrity and virulence. PLoS Pathog 15:e1007964–e1007964. https://doi.org/10.1371/journal.ppat.1007964
Zhou R, Zhou X, Fan A, Wang Z, Huang B (2018) Differential functions of two metalloproteases, Mrmep1 and Mrmep2, in growth, sporulation, cell wall integrity, and virulence in the filamentous fungus Metarhizium robertsii. Front Microbiol 9:1528
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Patil, S., Sarraf, G., Kharkwal, A.C. (2021). Panorama of Metarhizium: Host Interaction and Its Uses in Biocontrol and Plant Growth Promotion. In: Shrivastava, N., Mahajan, S., Varma, A. (eds) Symbiotic Soil Microorganisms. Soil Biology, vol 60. Springer, Cham. https://doi.org/10.1007/978-3-030-51916-2_18
Download citation
DOI: https://doi.org/10.1007/978-3-030-51916-2_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-51915-5
Online ISBN: 978-3-030-51916-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)