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Fungal entomopathogens in the rhizosphere

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Abstract

The ecology of fungal entomopathogens in the rhizosphere is an understudied area of insect pathology. The rhizosphere is the region of soil in which the release of root exudates influences the soil microbiota, and may provide a favorable environment for fungal entomopathogens. The objective of this review is to bring together the relatively scant data available to date on the subject of fungal entomopathogens colonizing the rhizosphere and to highlight the importance of these findings. Gaining a better understanding of the ecology of fungal entomopathogens in the rhizosphere will help in the development of successful microbial control strategies against root-feeding insect pests.

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References

  • Agrios G (2005) Plant pathology, 5th edn. Elsevier Academic Press, San Diego

    Google Scholar 

  • Aratchige NS, Lesna I, Sabelis MW (2004) Below-ground plant parts emit herbivore-induced volatiles: olfactory responses of a predatory mite to tulip bulbs infested by rust mites. Exp Appl Acarol 33:21–30

    Article  CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Barea J-M, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  CAS  PubMed  Google Scholar 

  • Bidochka MJ, Kasperski JE, Wild GAM (1998) Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Can J Bot 76:1198–1204

    Article  Google Scholar 

  • Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, Amritha de Croos JN (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? Appl Environ Microbiol 67:1335–1342

    Article  CAS  PubMed  Google Scholar 

  • Bidochka MJ, Menzies FV, Kamp AM (2002) Genetic groups of the insect-pathogenic fungus Beauveria bassiana are associated with habitat and thermal growth preferences. Arch Microbiol 178:531–537

    Article  CAS  PubMed  Google Scholar 

  • Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211

    Google Scholar 

  • Bing LA, Lewis LC (1992) Endophytic Beauveria bassiana (Balsamo) Vuillemin in corn: the influence of the plant growth stage and Ostrinia nubilalis (Hübner). Biocontrol Sci Technol 2:39–47

    Article  Google Scholar 

  • Bing LA, Lewis LC (1993) Occurrence of the entomopathogen Beauveria bassiana (Balsamo) Vuillemin in different tillage regimes and in Zea mays L. and virulence towards Ostrinia nubilalis (Hübner). Agric Ecosystems Environ 45:147–156

    Article  Google Scholar 

  • Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101:512–530

    Article  CAS  PubMed  Google Scholar 

  • Boff MIC, Zoon FC, Smits PH (2001) Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer. Entomol Exp Appl 98:329–337

    Article  Google Scholar 

  • Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Advanc Agron 66:1–102

    Article  Google Scholar 

  • Bruck DJ (2004) Natural occurrence of entomopathogens in Pacific Northwest nursery soils and their virulence to the black vine weevil. Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae). Environ Entomol 33:1335–1343

    Article  Google Scholar 

  • Bruck DJ (2005) Ecology of Metarhizium anisopliae in soilless potting media and the rhizosphere: implications for pest management. Biol Control 32:155–163

    Article  Google Scholar 

  • Chandler D, Hay D, Reid AP (1997) Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Appl Soil Ecol 5:133–141

    Article  Google Scholar 

  • Cory J, Ericsson JD (2009) Fungal entomopathogens in a tritrophic context. BioControl. doi:10.1007/s10526-009-9247-4 (this SI)

  • Cory JS, Hoover K (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecol Evol 21:278–286

    Article  Google Scholar 

  • Dicke M, Sabelis MW, Takabayashi J, Bruin J, Posthummus MA (1990) Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. J Chem Ecol 16:3091–3118

    Article  CAS  Google Scholar 

  • Dicke M, van Baarlen P, Wessels R, Dijkman H (1993) Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J Chem Ecol 19:581–599

    Article  CAS  Google Scholar 

  • Elliot SL, Sabelis MW, Janssen A, van der Geest LPS, Beerling EAM, Fransen J (2000) Can plants use entompathogens as bodyguards? Ecol Lett 3:228–235

    Article  Google Scholar 

  • Engler KM, Gold RE (2004) Effects of multiple generations of Metarhizium anisopliae on subterranean termite feeding and mortality (Isoptera: Rhinotermitidae). Sociobiology 44:211–240

    Google Scholar 

  • Giri B, Giang PH, Kumari R, Prasad R, Varma A (2005) Microbial diversity in soils. In: Buscot F, Varma S (eds) Microorganisms in soils: roles in genesis and functions. Springer-Verlag, Heidelberg, pp 19–55

    Chapter  Google Scholar 

  • Harrison RD, Gardner WA (1991) Occurrence of entomogenous fungus Beauveria bassiana in pecan orchard soils in Georgia. J Entomol Sci 26:360–366

    Google Scholar 

  • Hiltner L (1904) Uber neure Erfahrungen und probleme auf dem gebeit der bodenenbackteriologie und unter besonderer berucksichtigung der grundungung und brache. Arb Deut Landwirsch Ges 98:59–78

    Google Scholar 

  • Hoeksema JD, Schwartz MW (2003) Expanding comparative-advantage biological market models: contingency of mutualism on partners’ resource requirements and acquisition trade-offs. Proc R Soc London Ser B 270:913–919

    Article  Google Scholar 

  • Hountondji FCC, Sabelis MW, Hanna R, Janssen A (2005) Herbivore-induced plant volatiles trigger sporulation in entomopathogenic fungi: the case of Neozygites tanajoae infecting the cassava green mite. J Chem Ecol 31:1003–1021

    Article  CAS  PubMed  Google Scholar 

  • Hu G, Leger RJ (2002) Field trials using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl Environ Microbiol 68:6383–6387

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Inglis GD, Duke GM, Goettel MS, Kabaluk JT (2008) Genetic diversity of Metarhizium anisopliae var. anisopliae in southwestern British Columbia. J Invertbr Pathol 98:101–113

    Article  CAS  Google Scholar 

  • Jaronski ST (2007) Soil ecology of the entomopathogenic ascomycetes: a critical examination of what we (think) we know. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological pest management. Research Signpost, Kerala India, pp 91–144

    Google Scholar 

  • Jaronski ST, Larson B, Fuller-Schaefer C (2006) Effect of three bacterial disease control agents on the entomopathogenic fungi, Metarhizium ansisopliae and Beauveria bassiana. The American Phytopathological Society, North Central Division Meeting, June 13–15, 2006. Fargo, North Dakota

  • Jones DG (1998) The epidemiology of plant diseases. Kluwer AcademicPublishers, Dordrecht, The Netherlands

    Google Scholar 

  • Kabaluk JT, Ericsson JD (2007a) Environmental and behavioral constraints on the infection of wireworms by Metarhizium anisopliae. Environ Entomol 36:1415–1420

    Article  PubMed  Google Scholar 

  • Kabaluk JT, Ericsson JD (2007b) Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agron J 99:1377–1381

    Article  Google Scholar 

  • Kennedy AC (1998) The rhizosphere and spermosphere. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology. Prentice Hall, New Jersey, pp 389–407

    Google Scholar 

  • Kepler RM, Bruck DJ (2006) Examination of the interaction between the black vine weevil (Coleoptera: Curculionidae) and an entompathogenic fungus reveals a new tritrophic interaction. Environ Entomol 35:1021–1029

    Article  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced volatile emissions in nature. Science 291:2141–2144

    Article  CAS  PubMed  Google Scholar 

  • Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol 39:215–236

    Article  Google Scholar 

  • Klingen I, Hajek A, Meadow R, Renwick JAA (2002) Effect of brassicaceous plants on the survival and infectivity of insect pathogenic fungi. BioControl 47:411–425

    Article  CAS  Google Scholar 

  • Lacey LA, Kaya HK (2007) Field manual of techniques in invertebrate pathology. Springer, Dordrecht, The Netherlands

    Book  Google Scholar 

  • Leger RJ (2008) Studies on adaptations of Metarhizium anisopliae to life in soil. J Invertebr Pathol 98:271–276

    Article  Google Scholar 

  • Lewis LC, Bruck DJ, Gunnarson RD, Bidne KG (2001) Assessment of plant pathogenicity of endophytic Beauveria bassiana in Bt transgenic and non-transgenic corn. Crop Sci 41:1395–1400

    Article  Google Scholar 

  • Lewis LC, Bruck DJ, Gunnarson RD (2002) On-farm evaluation of Beauveria bassiana for control of Ostrinia nubilalis in Iowa, USA. BioControl 47:167–176

    Article  Google Scholar 

  • Lord JC (2005) From Metchnikoff to Monsanto and beyond: the path of microbial control. J Invertebr Pathol 89:19–29

    Article  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • McNew GL (1960) The nature, origin, and evolution of parasitism. In: Horsfall JG, Dimond AE (eds) Plant pathology: an advanced treatise, vol 2. Academic Press, New York, pp 19–69

    Google Scholar 

  • Nelson EB, Burpee LL, Lawton MB (1994) Biological control of turfgrass diseases. In: Leslie A (ed) Handbook of integrated pest management for turf and ornamentals. CRC Press, Boca Raton, FL, pp 409–421

    Google Scholar 

  • Neveu N, Grandgirard J, Nenon JP, Cortesero AM (2002) Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J Chem Ecol 28:1717–1732

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39

    Article  CAS  PubMed  Google Scholar 

  • Prior C (1992) Discovery and characterization of fungal pathogens for locust and grasshopper control. In: Lomer CJ, Prior C (eds) Biological control of locusts and grasshoppers. CAB International, Wallingford, pp 159–180

    Google Scholar 

  • Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  CAS  PubMed  Google Scholar 

  • Rath AC (2000) The use of entomopathogenic fungi for control of termites. Biocontrol Sci Technol 10:563–581

    Article  Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98

    Article  CAS  PubMed  Google Scholar 

  • Roberts DW, Humber RA (1981) Entomogenous fungi. In: Cole GT, Kendrick WB (eds) Biology of conidal fungi, vol 2. Academic Press, New York, pp 201–236

    Google Scholar 

  • Sabelis MW, van de Baan HE (1983) Location of distant spidermite colonies by phyoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol Exp Appl 33:303–314

    Google Scholar 

  • Sabelis MW, Janssen A, Pallini A, Venzon M, Bruin J, Drukker B, Scutareanu P (1999) Behavioral responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications. In: Agrawal AA, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores: biochemistry, ecology, and agriculture. American Phytopathological Society, St. Paul, Minnesota, pp 269–296

    Google Scholar 

  • Schmidt EL (1979) Initiation of plant root-microbe interactions. Ann Rev Microbiol 33:355–376

    Article  CAS  Google Scholar 

  • Shapiro-Ilan DI, Gardner WA, Fuxa JR, Wood BW, Nguyen KB, Adams BJ, Humber RA, Hall MJ (2003) Survey of entomopathogenic nematodes and fungi endemic to pecan orchards of the Southeastern United States and their virulence to the pecan weevil (Coleoptera: Curculionidae). Environ Entomol 32:187–195

    Article  Google Scholar 

  • Thompson SR, Brandenburg RL (2005) Tunneling responses of mole crickets (Orthoptera: Gryllotalpidae) to the entomopathogenic fungus, Beauveria bassiana. Environ Entomol 34:140–147

    Article  Google Scholar 

  • Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402

    Article  CAS  PubMed  Google Scholar 

  • Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  CAS  PubMed  Google Scholar 

  • Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174

    Article  CAS  PubMed  Google Scholar 

  • van Tol RWHM, van der Sommen ATC, Boff MIC, van Bezooijen J, Sabelis MW, Smits PH (2001) Plants protect their roots by alerting the enemies of grubs. Ecol Lett 4:292–294

    Article  Google Scholar 

  • Vega FE (2008) Insect pathology and fungal endophytes. J Invertebr Pathol 98:277–279

    Article  PubMed  Google Scholar 

  • Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  • Villani MG, Krueger SR, Schroeder PC, Consolie R, Consolie NH, Preston-Wilsey LM, Roberts DW (1994) Soil application effects of Metarhizium anisopliae on Japanese beetle (Coleoptera: Scarabaediae) behavior and survival in turfgrass microcosms. Environ Entomol 23:502–513

    Google Scholar 

  • Villani MG, Allee LL, Preston-Wilsey L, Consolie N, Xia Y, Brandenburg RL (2002) Use of radiography and tunnel castings for observing mole cricket (Orthoptera: Gryllotalpidae) behavior in soil. Am Entomol 48:42–50

    Google Scholar 

  • Wang C, Leger RJ (2007) The MAD1 adhesion of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesion enables attachment to plants. Eukary Cell 6:808–816

    Article  CAS  Google Scholar 

  • Wang C, Hu G, Leger RJ (2005) Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol 42:7.4–718

    Article  CAS  Google Scholar 

  • Whipps JM (1997) Developments in the biological control of soil-borne plant pathogens. Advan Botanic Res 26:1–134

    Article  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exper Bot 52:487–511

    CAS  Google Scholar 

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Acknowledgments

I would like to thank Leslie Lewis and David Shapiro-Ilan for helpful suggestions which improved the manuscript. I would also like to thank Helen Roy, Fernando Vega, Mark Goettel, Judith Pell, Eric Wajnberg and David Chandler for the invitation to prepare this review. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

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Correspondence to Denny J. Bruck.

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Bruck, D.J. Fungal entomopathogens in the rhizosphere. BioControl 55, 103–112 (2010). https://doi.org/10.1007/s10526-009-9236-7

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