1,920
Views
118
CrossRef citations to date
0
Altmetric
Research Articles

Fungal entomopathogens as endophytes: can they promote plant growth?

&
Pages 28-41 | Received 15 Jul 2016, Accepted 21 Sep 2016, Published online: 02 Nov 2016

References

  • Akello, J., Dubois, T., Coyne, D., & Kyamanywa, S. (2008). Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Protection, 27, 1437–1441. doi: 10.1016/j.cropro.2008.07.003
  • Akello, J., Dubois, T., Gold, C. S., Coyne, D., Nakavuma, J., & Paparu, P. (2007). Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). Journal of Invertebrate Pathology, 96, 34–42. doi: 10.1016/j.jip.2007.02.004
  • Akello, J., & Sikora, R. (2012). Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biological Control, 61, 215–221. doi: 10.1016/j.biocontrol.2012.02.007
  • Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van Den Berg, J., & Ekesi, S. (2013). Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecology, 6, 293–301. doi: 10.1016/j.funeco.2013.01.003
  • Arnold, A. E., Maynard, Z., & Gilbert, G. S. (2001). Fungal endophytes in dicotyledonous neotropical trees: Patterns of abundance and diversity. Mycological Research, 105, 1502–1507. doi: 10.1017/S0953756201004956
  • Castillo-Lopez, D., Zhu-Salzman, K., Ek-Ramos, M. J., & Sword, G. A. (2014). The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS ONE, 9, e103891. doi: 10.1371/journal.pone.0103891
  • Daoust, R. A., & Pereira, R. M. (1986). Stability of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae on beetle-attracting tubers and cowpea foliage in Brazil. Environmental Entomology, 15, 1237–1243. doi: 10.1093/ee/15.6.1237
  • Dolci, P., Guglielmo, F., Secchi, F., & Ozino, O. I. (2006). Persistence and efficacy of Beauveria brongniartii strains applied as biocontrol agents against Melolontha melolontha in the Valley of Aosta (northwest Italy). Journal of Applied Microbiology, 100, 1063–1072. doi: 10.1111/j.1365-2672.2006.02808.x
  • Enkerli, J., Kolliker, R., Keller, S., & Widmer, F. (2005). Isolation and characterization of microsatellite markers from the entomopathogenic fungus Metarhizium anisopliae. Molecular Ecology Notes, 5, 384–386. doi: 10.1111/j.1471-8286.2005.00935.x
  • Enkerli, J., Widmer, F., Gessler, C., & Keller, S. (2001). Strain-specific microsatellite markers in the entomopathogenic fungus Beauveria brongniartii. Mycological Research, 105, 1079–1087. doi: 10.1016/S0953-7562(08)61970-X
  • Enkerli, J., Widmer, F., & Keller, S. (2004). Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against European cockchafer larvae in Switzerland. Biological Control, 29, 115–123. doi: 10.1016/S1049-9644(03)00131-2
  • de Faria, M. R., & Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43, 237–256. doi: 10.1016/j.biocontrol.2007.08.001
  • Garcia, J. E., Posadas, J. B., Perticari, A., & Lecuona, R. E. (2011). Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Advances in Biological Research, 5, 22–27.
  • Gardner, W. A., Sutton, R. M., & Noblet, R. (1977). Persistence of Beauveria bassiana, Nomuraea rileyi, and Nosema necatrix on soybean foliage. Environmental Entomology, 6, 616–618. doi: 10.1093/ee/6.5.616
  • Gurulingappa, P., McGee, P. A., & Sword, G. (2011). Endophytic Lecanicillium lecanii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites. Crop Protection, 30, 349–353. doi: 10.1016/j.cropro.2010.11.017
  • Gurulingappa, P., Sword, G. A., Murdoch, G., & McGee, P. A. (2010). Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biological Control, 55, 34–41. doi: 10.1016/j.biocontrol.2010.06.011
  • Humber, R. A. (1997). Fungi: Identification. In L. A. Lacey (Ed.), Manual of techniques in insect pathology (pp. 153–185). London: Academic Press.
  • Inglis, G. D., Goettel, M. S., & Johnson, D. L. (1993). Persistence of the entomopathogenic fungus Beauveria bassiana on phylloplanes of crested wheatgrass and alfalfa. Biological Control, 3, 258–270. doi: 10.1006/bcon.1993.1035
  • Jaber, L. R. (2015). Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. BioControl, 60, 103–112. doi: 10.1007/s10526-014-9618-3
  • Jaber, L. R., & Enkerli, J. (2016). Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biological Control, 103, 187–195. doi: 10.1016/j.biocontrol.2016.09.008
  • Jaber, L. R., & Salem, N. M. (2014). Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Science and Technology, 24, 1096–1109. doi: 10.1080/09583157.2014.923379
  • Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1–41. doi: 10.1016/j.jip.2015.07.009
  • Laengle, T., Pernfuss, B., Seger, C., & Strasser, H. (2005). Field efficacy evaluation of Beauveria brongniartii against Melolontha melolontha in potato cultures. Sydowia, 57, 54–93.
  • Lopez, D. C., & Sword, G. A. (2015). The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biological Control, 89, 53–60. doi: 10.1016/j.biocontrol.2015.03.010
  • 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. Entomologia Experimentalis et Applicata, 154, 78–87. doi: 10.1111/eea.12262
  • Mayerhofer, J., Enkerli, J., Zelger, R., & Strasser, H. (2015). Biological control of the European cockchafer: Persistence of Beauveria brongniartii after long-term applications in the Euroregion Tyrol. BioControl, 60, 617–629. doi: 10.1007/s10526-015-9671-6
  • Meyling, N. V., Lubeck, M., Buckley, E. P., Eilenberg, J., & Rehner, S. A. (2009). Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Molecular Ecology, 18, 1282–1293. doi: 10.1111/j.1365-294X.2009.04095.x
  • Oulevey, C., Widmer, F., Kölliker, R., & Enkerli, J. (2009). An optimized microsatellite marker set for detection of Metarhizium anisopliae genotype diversity on field and regional scales. Mycological Research, 113, 1016–1024. doi: 10.1016/j.mycres.2009.06.005
  • Ownley, B., Gwinn, K. D., & Vega, F. E. (2010). Endophytic fungal entomopathogens with activity against plant pathogens: Ecology and evolution. BioControl, 55, 113–128. doi: 10.1007/s10526-009-9241-x
  • Ownley, B. H., Griffin, M. R., Klingeman, W. E., Gwinn, K. D., Moulton, J. K., & Pereira, R. M. (2008). Beauveria bassiana: Endophytic colonization and plant disease control. Journal of Invertebrate Pathology, 3, 267–270. doi: 10.1016/j.jip.2008.01.010
  • Parsa, S., Ortiz, V., & Vega, F. E. (2013). Establishing fungal entomopathogens as endophytes: Towards endophytic biological control. Journal of Visualized Experiments, 74, e50360.
  • Petrini, O., & Fisher, P. J. (1987). Fungal endophytes in Salicornia perennis. Transactions of the British Mycological Society, 87, 647–651. doi: 10.1016/S0007-1536(86)80109-7
  • Posada, F., Aime, M. C., Peterson, S. W., Rehner, S. A., & Vega, F. E. (2007). Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycological Research, 111, 749–758. doi: 10.1016/j.mycres.2007.03.006
  • Posada, F., & Vega, F. E. (2005). Establishment of the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte in cocoa seedlings (Theobroma cacao). Mycologia, 97, 1195–1200. doi: 10.3852/mycologia.97.6.1195
  • Quesada-Moraga, E., Muũoz-Ledesma, J., & Santiago-Álvarez, C. (2009). Systemic Protection of Papaver somniferum L. Against Iraella luteipes (Hymenoptera: Cynipidae) by an Endophytic Strain of Beauveria bassiana (Ascomycota: Hypocreales). Environmental Entomology, 38, 723–730. doi: 10.1603/022.038.0324
  • Rehner, S. A., & Buckley, E. P. (2003). Isolation and characterization of microsatellite loci from the entomopathogenic fungus Beauveria bassiana (Ascomycota: Hypocreales). Molecular Ecology Notes, 3, 409–411. doi: 10.1046/j.1471-8286.2003.00464.x
  • Resquin-Romero, G., Garrido-Jurado, I., Delso, C., Ríos-Moreno, A., & Quesada-Moraga, E. (2016). Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. Journal of Invertebrate Pathology, 136, 23–31. doi: 10.1016/j.jip.2016.03.003
  • Sasan, R. K., & Bidochka, M. J. (2012). The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany, 99, 101–107. doi: 10.3732/ajb.1100136
  • SAS Institute Inc. (2010). SAS OnlineDoc® Version 9.1.3. Cary, NC, USA.
  • Schulz, B., Guske, S., Dammann, U., & Boyle, C. (1998). Endophyte–host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis, 25, 213–227.
  • Strasser, H., Forer, A., Schinner, F. (1996). Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii. In T. A. Jackson &T. R. Glare (Eds.), Microbial control of soil dwelling pests (pp. 125–130). Lincoln: AgResearch.
  • Tefera, T., & Vidal, S. (2009). Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl, 54, 663–669. doi: 10.1007/s10526-009-9216-y
  • Vega, F. E. (2008). Insect pathology and fungal endophytes. Journal of Invertebrate Pathology, 98, 277–279. doi: 10.1016/j.jip.2008.01.008
  • Vega, F. E., Goettel, M. S., Blackwell, M., Chandler, D., Jackson, M. A., Keller, S., … Roy, H. E. (2009). Fungal entomopathogens: New insights on their ecology. Fungal Ecology, 2, 149–159. doi: 10.1016/j.funeco.2009.05.001
  • Vidal, S., & Jaber, L. R. (2015). Entomopathogenic fungi as endophytes: Plant–endophyte–herbivore interactions and prospects for use in biological control. Current Science, 109, 46–54.
  • Wagner, B. L., & Lewis, L. C. (2000). Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology, 66, 3468–3473. doi: 10.1128/AEM.66.8.3468-3473.2000
  • Wilson, D. (1995). Endophyte – the evolution of a term, and clarification of its use and definition. Oikos, 73, 274–276. doi: 10.2307/3545919

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.