Abstract
Chronological histological alterations of Metarhizium anisopliae during interaction with the cattle tick Boophilus microplus were investigated by light and scanning electron microscopy. M. anisopliae invades B. microplus by a process which involves adhesion of conidia to the cuticle, conidia germination, formation of appressoria and penetration through the cuticle. Twenty-four hours post-infection conidia are adhered and germination starts on the surface of the tick. At this time, the conidia differentiate to form appressoria exerting mechanical pressure and trigger hydrolytic enzyme secretion leading to penetration. Massive penetration is observed 72 h post-inoculation, and after 96 h, the hyphae start to emerge from the cuticle surface to form conidia. The intense invasion of adjacent tissues by hyphae was observed by light microscopy, confirming the ability of M. anisopliae to produce significant morphological alterations in the cuticle, and its infective effectiveness in B. microplus.
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S.B. Alves (1998) Controle Microbiano de Insetos Editora da Fundação de Estudos Agrários Luiz de Queiróz Piracicaba
S.O. Andersen (1979) ArticleTitleBiochemistry of the insect cuticle Ann. Rev. Entomol. 24 29–61 Occurrence Handle10.1146/annurev.en.24.010179.000333 Occurrence Handle1:CAS:528:DyaE1MXhtVSnsLY%3D
H. Askary N. Benhamou J. Brodeu (1999) ArticleTitleUltrastructural and citochemical characterization of aphid invasion by the hyphomicete Verticillium lecanii J. Invertebr. Pathol. 74 1–13 Occurrence Handle10388542 Occurrence Handle1:CAS:528:DyaK1MXktV2kt7s%3D
M.J. Bidochka R.J. St Leger (1997) ArticleTitleMechanisms of Deuteromycete fungal infections in grasshoppers and locusts: an overview Mem. Entomol. Soc. Can. 171 213–224
V.R.E.P. Bittencourt A.G. Mascarenhas J.L.H. Faccini (1999) ArticleTitleMecanismo de infecção do fungo Metarhizium anisopliae no carrapato Boophilus microplus em condições experimentais Ciência Rural 29 351–354
M.R. Bogo C.A. Rota H. Pinto M. Ocampos C.T. Correa M.H. Vainstein A. Schrank (1998) ArticleTitleA chitinase encoding gene (chit 1 Gene) from the entomopathogen Metarhizium anisopliae: isolation and characterization of genomic and full-length cDNA Curr. Microbiol. 37 221–225 Occurrence Handle10.1007/s002849900368 Occurrence Handle9732526 Occurrence Handle1:CAS:528:DyaK1cXmt1agsrc%3D
D.G. Boucias J.C. Pendlant (1998) Principles of Insect Pathology Kluwer Academic Publishers Boston, Massachusetts
D.G. Boucias J.C. Pendlant J.P. Latge (1988) ArticleTitleNonespecific factors involved in attachment of entomopathogenic Deuteromycetes to host insect cuticle Appl. Environ. Microbiol. 54 1795–1805 Occurrence Handle1:CAS:528:DyaL1cXltVOlsL8%3D Occurrence Handle16347689
D.G. Boucias J.C. Pendlant J.P. Latge (1991) Attachment of mycopathogens to cuticle: the initial event of mycoses in arthropod hosts G.T. Cole H.C. Hoch (Eds) The Fungal Spore and Disease Initiation in Plants and Animals Plenum Press New York 101–128
T.M. Butt L. Ibrahim S.J. Clark A. Beckett (1995) ArticleTitleThe germination behavior of Metarhizium anisopliae on the surface of aphid and flea beetle cuticles Mycol. Res. 99 945–950 Occurrence Handle10.1016/S0953-7562(09)80754-5
J.J. Castro R.M. Newson (1993) ArticleTitleHost resistance in cattle tick control Parasitol. Today 9 13–17 Occurrence Handle15463656
J. Clarkson K. Charnley (1996) ArticleTitleNew insights into the mechanisms of fungal pathogenesis in insects Trends Microbiol. 4 197–203 Occurrence Handle10.1016/0966-842X(96)10022-6 Occurrence Handle8727600 Occurrence Handle1:STN:280:DyaK28zisVSmsg%3D%3D
Clarkson J., Screen S., Bailey A., Cobb B. and Charnley K. 1998. Fungal pathogenesis in insects. In: Bridge P.D., Couteaudier Y. and Clarkson J.M. (eds), Molecular Variability of Fungal Pathogens. CAB International, pp. 83–94.
A.C.B. Correia A.C. Fiorin A.C. Monteiro C.J. Veríssimo (1998) ArticleTitleEffects of Metarhizium anisopliae on the tick Boophilus microplus (Acari: Ixodidae) in stabled cattle J. Invertebr. Pathol. 71 189–191
A.P.G. Frazzon I.S.V. Junior A. Masuda A. Schrank M.H. Vainstein (2000) ArticleTitleIn vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus Vet. Parasitol. 94 117–125 Occurrence Handle11078949 Occurrence Handle1:STN:280:DC%2BD3M7itFajsg%3D%3D
G. Gindin M. Samish G. Zangi A. Mishoutchenko I. Glazer (2002) ArticleTitleThe susceptibility of different species and stages of ticks to entomopathogenic fungi Exp. Appl. Acarol. 28 283–288 Occurrence Handle10.1023/A:1025379307255 Occurrence Handle14570142
M.S. Goettel R.J. St Leger N.W. Rizzo R.C. Staples W. Roberts (1989) ArticleTitleUltrastructural localization of a cuticle-degrading protease produced by the entomopathogenic fungus Metarhizium anisopliae during penetration of host (Manduca Sexta) cuticle J. Gen. Microbiol. 135 2233–2239 Occurrence Handle1:CAS:528:DyaL1MXlvFWisrw%3D
S.G.S. Gunnarsson (1988) ArticleTitleInfection of Schistocerca gregaria by the fungus Metarhizium anisopliae: cellular reactions in the integument studied by scanning electron and light microscopy J. Invertebr. Pathol. 52 9–17
Inglis G.D., Goettel M.S., Butt T.M. and Strasser H. 2001. Use of Hyfomicetous fungi for managing insect pests. In: Butt T. (eds), Fungi as Biological Agents: Progress, Problems and Potential. CABI Publishing, pp. 23–69.
G.P. Kaaya S. Hassan (2000) ArticleTitleEntomogenous fungi as promising biopesticides for tick control Exp. Appl. Acarol. 24 913–926 Occurrence Handle10.1023/A:1010722914299
G.P. Kaaya E.N. Mwangi E. Ouna (1996) ArticleTitleProspects for biological control of livestock ticks, Rhipicephalus appendiculatus and Amblyomma variegatumusing the emtomogenous fungi Bauveria bassiana and Metarhizium anisopliae J. Invertebr. Pathol. 67 15–20 Occurrence Handle8812559 Occurrence Handle1:STN:280:DyaK28vhtFynug%3D%3D
A. Kassa D. Stephan S. Vidal G. Zimmermann (2004) ArticleTitleLaboratory and field evaluation of different formulations of Metarhizium anisopliae var. acridum submerged spores and aerial conidia for the control locusts and grasshoppers BioControl 49 63–81 Occurrence Handle10.1023/B:BICO.0000009384.46858.aa Occurrence Handle1:CAS:528:DC%2BD3sXpvVKrtbs%3D
B.H. Kay D.H. Kemp (1994) ArticleTitleVaccines against arthropods Am. J. Trop. Med. Hyg. 50 87–96 Occurrence Handle8024089 Occurrence Handle1:STN:280:DyaK2c3psFyksQ%3D%3D
B.H. Kirkland E. Cho N.O. Keyhani (2004) ArticleTitleDifferential susceptibility of Amblyomma maculatum and Amblyomma americanum (Acari: Ixodidea) to the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae Biol. Control 31 414–421 Occurrence Handle10.1016/j.biocontrol.2004.07.007
C. Krieger de Moraes A. Schrank M.H. Vainstein (2003) ArticleTitleRegulation of extracellular chitinases and proteases in the entomopathogen and acaricide Metarhizium anisopliae Curr. Microbiol. 46 205–210 Occurrence Handle10.1007/s00284-002-3863-x Occurrence Handle12567244 Occurrence Handle1:CAS:528:DC%2BD3sXhs1agurc%3D
C.M. Lacey L.A. Lacey D.R. Roberts (1988) ArticleTitleRoute of invasion and histopathology of Metarhizium anisopliae in Culex quinquefasciatus J. Invertebr. Pathol. 52 108–118 Occurrence Handle3418133 Occurrence Handle1:STN:280:DyaL1czjtFyqsg%3D%3D
C. Luz M.S. Tigano I.G. Silva C.M.T. Cordeiro S.M. Aljanabi (1998) ArticleTitleSelection of Beauveria bassiana and Metarhizium anisopliae isolates to control Triatoma infestans Mem. Inst. Oswaldo Cruz 93 839–846 Occurrence Handle10.1590/S0074-02761998000600026 Occurrence Handle9921313 Occurrence Handle1:STN:280:DyaK1M7hvFyrsw%3D%3D
V.J.E. McCauley R.Y. Zacharuck R.D. Tinline (1968) ArticleTitleHistopathology of green muscardine in larvae of four species of Elateridae (Coleoptera) J. Invertebr. Pathol. 12 444–459
A.C. Monteiro A.C. Fiorin A.C.B. Correia (1998a) ArticleTitlePathogenicity of isolates of Metarhizium anisopliae (Metsh.) sorokin towords the cattle tick Booplhilus microplus (Can.) (Acari: Ixodidae) under laboratory conditions Rev. Microbiol. 29 109–112
S.G. Monteiro V.R.E.P. Bittencourt E. Daemon J.L.H. Faccini (1998b) ArticleTitleEfeito dos fungos entomopatogênicos Metarhizium anisopliae e Beauveria bassiana em ovos de Rhipicephalus sanguineus (Acari: Ixodidae) Ciência Rural 28 461–466
A.S. Pinto C.C. Barreto A. Schrank C.J. Ulhoa M.H. Vainstein (1997) ArticleTitlePurification and characterization of an extracellular chitinase from the entomopathogenic Metarhizium anisopliae Can. J. Microbiol. 43 322–327 Occurrence Handle1:CAS:528:DyaK2sXis1Oqsbs%3D Occurrence Handle10.1139/m97-045
Y.B. Rosato C.L. Messias J.L. Azevedo (1981) ArticleTitleProduction of extracelular enzymes by isolates of Metarhizium anisopliae J. Invertebr. Pathol. 38 1–3 Occurrence Handle1:CAS:528:DyaL3MXkvFels74%3D
E. Scholte B.N. Njiru R.C. Smallegange W. Takken B.G.J. Knols (2003) ArticleTitleInfection of malaria (Anopheles gambiae s.s.) and filariasis (Culex quinquefasciatus) vectors with the entomopatogenic fungus Metarhizium anisopliae Malar. J. 2 29–36 Occurrence Handle10.1186/1475-2875-2-29 Occurrence Handle14565851
D.R. Sosa-Gomez D.G. Boucias J.L. Nation (1997) ArticleTitleAttachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipides and aldehydes J. Invertebr. Pathol. 69 31–39 Occurrence Handle9028925 Occurrence Handle1:CAS:528:DyaK2sXhvFOmu7w%3D
R.J. St Leger R.M. Cooper A.K. Charnley (1987) ArticleTitleProduction of cuticle-degrading enzymes by the Entomopathogen Metarhizium anisopliae during infection of cuticles from Calliphora vomitoria and Manduca Sexta J. Gen. Microbiol. 133 1371–1382 Occurrence Handle1:CAS:528:DyaL2sXkt1SnurY%3D
R.J. St Leger M. Goettel D.W. Roberts R.C. Staples (1991) ArticleTitlePenetration events during infection of host cuticle by Metarhizium anisopliae J. Invertebr. Pathol. 58 168–179
R.J. St Leger L. Joshi M.J. Bidochka N.W. Rizzo D.W. Roberts (1996a) ArticleTitleCharacterization and ultrastructural localization of chitinases from Metarhizium anisopliae, M. flavoviride, and Beauveria bassiana during fungal invasion of host (Manduca Sexta) cuticle Appl. Environ. Microbiol. 62 907–912 Occurrence Handle1:CAS:528:DyaK28XhsVWqsL8%3D
R.J. St Leger L. Joshi M.J. Bidochka N.W. Rizzo D.W. Roberts (1996b) ArticleTitleBiochemical characterization and ultrastructural localization of two extracellular trypsins produced by Metarhizium anisopliae in infected insect cuticles Appl. Environ. Microbiol. 62 1257–1264 Occurrence Handle1:CAS:528:DyaK28XitFektr0%3D
P.V. Tiago M.H.P. Fungaro M.C. Furlaneto (2002) ArticleTitleCuticle-degrading proteases from the entomopathogen Metarhizium flavoviridetheir distribuition in secreted and intracellular fractions Lett. Appl. Microbiol. 34 91–94 Occurrence Handle10.1046/j.1472-765x.2002.01064.x Occurrence Handle11849501 Occurrence Handle1:CAS:528:DC%2BD38XhsVGkt70%3D
S. Vestergaard T.M. Butt J. Bresciani T.A. Gillespie J. Eilenberg (1999) ArticleTitleLight and electron microscopy studies of the infection of the western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae) by the entomopathogenic fungus Metarhizium anisopliae J. Invertebr. Pathol. 73 25–33 Occurrence Handle9878286
V.B. Wigglesworth (1972) The Principles of Insect Physiology Chapman and Hall London
R.Y. Zacharuk (1970) ArticleTitleFine structure of the fungus Metarhizium anisopliae infecting three species of larval Elateridae (Colepotera). III. Penetration of host integument J. Invertebr. Pathol. 15 372–396
E. Zhioua M. Browning P.W. Johnson H.S. Ginsberg R.A. LeBrum (1997) ArticleTitlePathogenicity of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycetes) to Ixodes scapularis (Acari: Ixodidae) J. Parasitol. 83 815–818 Occurrence Handle9379283 Occurrence Handle1:STN:280:DyaK1c%2Fis1Sqtw%3D%3D
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Arruda, W., Lübeck, I., Schrank, A. et al. Morphological Alterations of Metarhizium anisopliae During Penetration of Boophilus microplus Ticks. Exp Appl Acarol 37, 231–244 (2005). https://doi.org/10.1007/s10493-005-3818-6
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DOI: https://doi.org/10.1007/s10493-005-3818-6