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4 - Crossing Frontiers: Endophytic Entomopathogenic Fungi for Biological Control of Plant Diseases

from Part II - Role of Endophytes in Growth and Biotic and Abiotic Stress Resistance

Published online by Cambridge University Press:  01 April 2019

By
Lorena Barra-Bucarei ,
Andrés France  and
Paz Millas
Edited by
Trevor R. Hodkinson ,
Fiona M. Doohan ,
Matthew J. Saunders  and
Brian R. Murphy
Trevor R. Hodkinson
Affiliation:
Trinity College Dublin
Fiona M. Doohan
Affiliation:
University College Dublin
Matthew J. Saunders
Affiliation:
Trinity College Dublin
Brian R. Murphy
Affiliation:
Trinity College Dublin
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Summary

World population growth has generated a demand for increased healthy food production and the development of sustainable agricultural technologies to replace environmentally damaging farming practices, including the overuse of pesticides. Biological control using entomopathogenic fungi, as natural pathogens of arthropod pests, is an alternative method to meet this objective. These fungi have been traditionally studied to control insects, but recent studies have begun to examine their activity as plant endophytes to protect plants against phytopathogens and improve other aspects of crop production. This chapter reviews the importance of these entomopathogenic fungi as endophytes in the context of biological control. Our studies focus on determining the ability of native strains of entomopathogenic fungi for endophytic colonisation and their potential application for the control of diseases in tomato. The chapter also discusses aspects to consider for their development as commercial biopesticides and suggests ways to make this control method available to producers of agricultural crops.

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Endophytes for a Growing World , pp. 67 - 92
Publisher: Cambridge University Press
Print publication year: 2019

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References

Aly, A. H., Debbab, A., Kjer, J. and Proksch, P. (2010). Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Diversity, 41, 1–16.CrossRefGoogle Scholar
Akello, J. and 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.CrossRefGoogle Scholar
Akello, J., Dubois, T., Coyne, D. and Hillnhutter, C. (2007). Beauveria bassiana as an endophyte in tissue-cultured banana plants: a novel way to combat the banana weevil Cosmopolites sordidus. In III International Symposium on Banana: ISHS-ProMusa Symposium on Recent Advances in Banana Crop Protection for Sustainable Production and Improved Livelihoods, ed. D. Jones and I. Van den Bergh. Acta Horticulturae, 828, 129–138.Google Scholar
Akello, J., Dubois, T., Coyne, D. and Kyamanywa, S. (2008). Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Protection, 27, 1437–1441.CrossRefGoogle Scholar
Akello, J., Dubois, T., Coyne, D. and Kyamanywa, S. (2009). The effects of Beauveria bassiana dose and exposure duration on colonization and growth of tissue cultured banana (Musa sp.) plants. Biological Control, 49, 6–10.CrossRefGoogle Scholar
Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van den Berg, J. and 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.CrossRefGoogle Scholar
Arnold, A., Maynard, Z., Gilbert, G., Coley, P. and Kursar, T. (2000). Are tropical endophytic fungi hyper diverse? Ecology Letters, 3, 267–274.CrossRefGoogle Scholar
Arnold, A., Mejía, L., Kyllo, D. et al. (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Sciences of the United States of America, 100, 15649–15654.CrossRefGoogle Scholar
Barelli, L., Moonjely, S., Behie, S. W. and Bidochka, M. J. (2016). Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Molecular Biology, 90, 657–664.CrossRefGoogle ScholarPubMed
Behie, S. W. and Bidochka, M. J. (2014). Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Applied and Environmental Microbiology, 80, 1553–1560.CrossRefGoogle ScholarPubMed
Behie, S. W., Zelisko, P. M. and Bidochka, M. J. (2012). Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science, 336, 1576–1577.CrossRefGoogle ScholarPubMed
Behie, S. W., Jones, S. J. and Bidochka, M. J. (2015). Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology, 13, 112–119.CrossRefGoogle Scholar
Benhamou, N. and Brodeur, J. (2001). Pre-inoculation of Ri T-DNA transformed cucumber roots with the mycoparasite, Verticillium lecanii, induces host defense reactions against Pythium ultimum infection. Physiological and Molecular Plant Pathology, 58, 133–146.CrossRefGoogle Scholar
Bernardini, M., Carilli, A., Pacioni, G. and Santurbano, B. (1975). Isolation of beauvericin from Paecilomyces fumoso-roseus. Phytochemistry, 14, 1865.CrossRefGoogle Scholar
Bidochka, M. and Khachatourians, C. (1991). The implication of metabolic acids produced by Beauveria bassiana in pathogenesis of the migratory grasshopper, Melanoplus sanguinipes. Journal of Invertebrate Pathology, 58, 106–117.CrossRefGoogle Scholar
Bing, L. and Lewis, L. (1992). Endophytic Beauveria bassiana in corn, the influence of the plant growth stage and Ostrimia nubilalis. Biocontrol Science and Technology, 2, 39–47.CrossRefGoogle Scholar
Boucias, D. G. and Pendland, J. C. (1998). Entomopathogenic fungi: fungi imperfecti. In Principles of Insect Pathology, ed. D. Boucias and Jacquelyn C. Pendland. Boston, MA: Springer, pp. 321–364.CrossRefGoogle Scholar
Brownbridge, M., Reay, S. D., Nelson, T. L. and Glare, T. R. (2012). Persistence of Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte following inoculation of radiata pine seed and seedlings. Biological Control, 61, 194–200.CrossRefGoogle Scholar
Bruck, D. J. and Lewis, L. C. (2002). Rainfall and crop residue effects on soil dispersion and Beauveria bassiana spread to corn. Applied Soil Ecology, 20, 183–190.CrossRefGoogle Scholar
Bultman, T. L. and Bell, G. D. (2003). Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos, 103, 182–190.CrossRefGoogle Scholar
Card, S., Johnson, L., Teasdale, S. and Caradus, J. (2016). Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiology Ecology, 92, fiw114.CrossRefGoogle ScholarPubMed
Carroll, G. (1988). Fungal endophytes in stems and leaves: from latent pathogens to mutualistic symbiont. Ecology, 69, 2–9.CrossRefGoogle Scholar
Clayton, W., Eaton, C. J., Dupont, P.-Y. et al. (2017). Analysis of simple sequence repeat (SSR) structure and sequence within Epichloë endophyte genomes reveals impacts on gene structure and insights into ancestral hybridization events. PLoS One 12, e0183748.CrossRefGoogle ScholarPubMed
Craven, K. D., Hsiau, P. T. W., Leuchtmann, A., Hollin, W. and Schardl, C. L. (2001). Multigene phylogeny of Epichloë species, fungal symbionts of grasses. Annals of the Missouri Botanical Garden, 88, 14–34.CrossRefGoogle Scholar
De Bary, A. (1884). Vergleichende Morphologie und Biologie der Pilze, Mycetozoen und Bacterien. Leipzig: Wilhelm Engelmann.Google Scholar
De Faria, M. R. and Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43, 237–256.CrossRefGoogle Scholar
Elena, G. J., Beatriz, P. J., Alejandro, P. and Lecuona, R. E. (2011). Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Advances in Biological Research, 5, 22–27.Google Scholar
Fargues, J., Goettel, M. S., Smits, N. et al. (1996). Variability in susceptibility to simulated sunlight of conidia among isolates of entomopathogenic Hyphomycetes. Mycopathologia, 135, 171–181.CrossRefGoogle ScholarPubMed
Feng, M. G., Chen, C. and Chen, B. (2004). Wide dispersal of aphid pathogenic Entomophthorales among aphids relies upon migratory alates. Environmental Microbiology, 6, 510–516.CrossRefGoogle ScholarPubMed
Feng, P., Shang, Y., Cen, K. and Wang, C. (2015). Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity. Proceedings of the National Academy of Sciences of the United States of America, 112, 11365–11370.CrossRefGoogle ScholarPubMed
Fenice, M. and Gooday, G. W. (2006). Mycoparasitic actions against fungi and oomycetes by a strain (CCFEE 5003) of the fungus Lecanicillium muscarium isolated in Continental Antarctica. Annals of Microbiology, 56, 1.CrossRefGoogle Scholar
Ferron, P. (1978). Biological control of insect pests by entomogenous fungi. Annual Review of Entomology, 23, 409–442.CrossRefGoogle Scholar
Fisher, P. J. and Petrini, O. (1987). Location of fungal endophytes in tissues of Suaeda fruticosa: a preliminary study. Transactions of the British Mycological Society, 89, 246–249.CrossRefGoogle Scholar
France, I., Gerding, G., Gerding, M. and Sandoval, A. (2000). Patogenicidad de una colección de cepas nativas de Metarhizium spp. y Beauveria spp. en Aegorhinus superciliosus, Asynonychus cervinus y Otiorhynchus sulcatus. Agricultura Técnica, 60, 205–215.CrossRefGoogle Scholar
Gao, F. K., Dai, C. C. and Liu, X. Z. (2010). Mechanisms of fungal endophytes in plant protection against pathogens. African Journal of Microbiology Research, 4, 1346–1351.Google Scholar
Garrido-Jurado, I., Landa, B. B. and Quesada-Moraga, E. (2016). Detection and quantification of the entomopathogenic fungal endophyte Beauveria bassiana in plants by nested and quantitative PCR. Microbial-Based Biopesticides: Methods and Protocols, pp. 161–166.CrossRefGoogle ScholarPubMed
Glare, T., Caradus, J., Gelernter, W. et al. (2012). Have biopesticides come of age? Trends in Biotechnology, 30, 250–258.CrossRefGoogle ScholarPubMed
Greenfield, M., Gómez-Jiménez, M. I., Ortiz, V. et al. (2016). Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biological Control, 95, 40–48.CrossRefGoogle ScholarPubMed
Griffin, M. R. (2007). Beauveria bassiana, a cotton endophyte with biocontrol activity against seedling disease. PhD Dissertation. The University of Tennessee, Knoxville, TN.Google Scholar
Grille, G., Pascal, C., Franco, J. and Basso, C. (2001). Distribución espacial de Trialeurodes vaporariorum (Homoptera: Aleyrodidae) en plantas de tomate. Boletín de Sanidad Vegetal. Plagas, 27, 475–488.Google Scholar
Gómez-Vidal, S., Lopez-Lorca, L., Jansson, H. and Salinas, J. (2006). Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron, 37, 624–632.CrossRefGoogle ScholarPubMed
Gurulingappa, P., McGee, P. A. and 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.CrossRefGoogle Scholar
Hajek, A. and St. Leger, F. (1994). Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39, 293–322.CrossRefGoogle Scholar
Hajek, A. E. (1997). Ecology of terrestrial fungal entomopathogens. In Advances in Microbial Ecology, Vol. 15, ed. J. G. Jones. Boston, MA: Springer, pp. 193–249.CrossRefGoogle Scholar
Hamil, R., Higgens, C., Boaz, H. and Gorman, M. (1969). The structure of beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahedron Letters, 49, 4255–4258.CrossRefGoogle Scholar
Hardoim, P. R., Van Overbeek, L. S., Berg, G. et al. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews, 79, 293–320.CrossRefGoogle ScholarPubMed
Herre, E. A., Mejía, L. C., Kyllo, D. A. et al. (2007). Ecological implications of antipathogen effects of tropical fungal endophytes and mycorrhizae. Ecology, 88, 550–558.CrossRefGoogle ScholarPubMed
Hirano, E., Koike, M., Aiuchi, D. and Tani, M. (2008). Pre-inoculation of cucumber roots with Verticillium lecanii (Lecanicillium muscarium) induces resistance to powdery mildew. Research Bulletin of Obihiro University, 29, 82–94.Google Scholar
Holt, R. D. and Hochberg, M. E. (1997). When is biological control evolutionarily stable (or is it)? Ecology, 78, 1673–1683.CrossRefGoogle Scholar
Hoffmann, M. and Frodsham, A. (1993). Los Enemigos Naturales de las Plagas de Insectos Vegetales. Ithaca, New York: Extensión Cooperativa de la Universidad de Cornell.Google Scholar
Hu, Q., Li, F. and Zhang, Y. (2016). Risks of mycotoxins from mycoinsecticides to humans. BioMed Research International, 2016, ID 3194321, 1–13.Google ScholarPubMed
Hyde, K. D. and Soytong, K. (2008). The fungal endophyte dilemma. Fungal Diversity, 33, e173.Google Scholar
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.CrossRefGoogle Scholar
Jaber, L. R. and 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.CrossRefGoogle Scholar
Jaber, L. R. and Ownley, B. H. (2017). Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control, 116, 35–45.Google Scholar
Jaber, L. R. and 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.CrossRefGoogle Scholar
Jaber, L. R. and Vidal, S. (2010). Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecological Entomology, 35, 25–36.CrossRefGoogle Scholar
Karthiba, L., Saveetha, K., Suresh, S. et al. (2010). PGPR and entomopathogenic fungus bioformulation for the synchronous management of leaffolder pest and sheath blight disease of rice. Pest Management Science, 66, 555–564.CrossRefGoogle ScholarPubMed
Kauppinen, M., Saikkonen, K., Helander, M., Pirttilä, A. M. and Wäli, P. R. (2016). Epichloë grass endophytes in sustainable agriculture. Nature Plants, 2, 15224.CrossRefGoogle ScholarPubMed
Kavroulakis, N., Ntougias, S., Zervakis, G. I. et al. (2007). Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain. Journal of Experimental Botany, 58, 3853–3864.CrossRefGoogle ScholarPubMed
Kepler, R. M. and Rehner, S. A. (2013). Genome-assisted development of nuclear intergenic sequence markers for entomopathogenic fungi of the Metarhizium anisopliae species complex. Molecular Ecology Resources, 13, 210–217.CrossRefGoogle ScholarPubMed
Kim, J. J., Goettel, M. S. and Gillespie, D. R. (2007). Potential of Lecanicillium species for dual microbial control of aphids and the cucumber powdery mildew fungus, Sphaerotheca fuliginea. Biological Control, 40, 327–332.CrossRefGoogle Scholar
Kim, K. H., Kabir, E. and Jahan, S. A. (2017). Exposure to pesticides and the associated human health effects. Science of The Total Environment, 575, 525–535.CrossRefGoogle ScholarPubMed
Kolattukudy, P. (1984). Biochemistry and function of cutin and suberin. Canadian Journal of Botany, 62, 2918–2933.CrossRefGoogle Scholar
Kumar, V. (2015). A review on efficacy of biopesticides to control the agricultural insect’s pest. International Journal of Agricultural Science Research, 4, 168–179.Google Scholar
Krell, V., Jakobs-Schoenwandt, D., Vidal, S. and Patel, A. V. (2017). Encapsulation of Metarhizium brunneum enhances endophytism in tomato plants. Biological Control, 116, 62–73.CrossRefGoogle Scholar
Kwak, M. J., Song, J. Y., Kim, S. Y. et al. (2012). Complete genome sequence of the endophytic bacterium Burkholderia sp. strain KJ006. Journal of Bacteriology, 194, 4432–4433.CrossRefGoogle ScholarPubMed
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I. et al. (2015). Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology, 132, 1–41.CrossRefGoogle ScholarPubMed
Lahiri, A., Douglas, G. C., Murphy, B. R. and Hodkinson, T. R. (2019). In vitro methods for plant–microbe interaction and biocontrol studies in european ash (Fraxinus excelsior L.). In Endophytes for a Growing World, ed. Hodkinson, T. R., Doohan, F. M., Saunders, M. J. and Murphy, B. R.. Cambridge: Cambridge University Press, Chapter 15.Google Scholar
Leroux, P., Gredt, M., Leroch, M. and Walker, A. S. (2010). Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Applied and Environmental Microbiology, 76, 6615–6630.CrossRefGoogle ScholarPubMed
Levitan, L., Merwin, I. and Kovach, J. (1995). Assessing the relative environmental impacts of agricultural pesticides: the quest for a holistic method. Agriculture, Ecosystems & Environment, 55, 153–168.CrossRefGoogle Scholar
Liao, X., O’Brien, T. R., Fang, W. and Leger, R. J. S. (2014). The plant beneficial effects of Metarhizium species correlate with their association with roots. Applied Microbiology and Biotechnology, 98, 7089–7096.CrossRefGoogle ScholarPubMed
Lingg, A. and Donaldson, M. (1981). Biotic and abiotic factors affecting stability of B. bassiana conidia in soil. Journal of Invertebrate Pathology, 38, 191–200.CrossRefGoogle Scholar
Logrieco, A., Moretti, A., Castella, G. et al. (1998). Beauvericin production by Fusarium species. Applied Environmental Microbiology, 64, 3084–3088.CrossRefGoogle ScholarPubMed
Lohse, R., Jakobs-Schönwandt, D., Vidal, S. and Patel, A. V. (2015). Evaluation of new fermentation and formulation strategies for a high endophytic establishment of Beauveria bassiana in oilseed rape plants. Biological Control, 88, 26–36.CrossRefGoogle Scholar
Lopez, D. C. and 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.CrossRefGoogle Scholar
Majumder, D., Kangjam, B., Devi, K. J. et al. (2016). Endophytes: an emerging tool for plant disease management. In The Handbook of Microbial Bioresources, ed. Gupta, V. K., Sharma, G. D., Tuohy, M. G. and R. Gaur. Oxfordshire: CABI, pp. 179–192.CrossRefGoogle Scholar
Mantzoukas, S., Chondrogiannis, C. and 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.CrossRefGoogle Scholar
Martin, K. J. and Rygiewicz, P. T. (2005). Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiology, 5, 28.CrossRefGoogle ScholarPubMed
Mazón, A. (2001). Producción, uso y control de calidad de hongos entomopatógenos en Nicaragua. Manejo Integrado de plagas, CATIE, Costa Rica, 63, 95–103.Google Scholar
Meyling, N. V. and Eilenberg, J. (2007). Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biological Control, 43, 145–155.CrossRefGoogle Scholar
Moore, D., Bateman, R. P., Carey, M. and Prior, C. (1995). Long-term storage of Metarhizium flavoviride conidia in oil formulations for the control of locusts and grasshoppers. Biocontrol Science and Technology, 5, 193–200.CrossRefGoogle Scholar
Murphy, B. R., Martin Nieto, L., Doohan, F. M. and Hodkinson, T. R. (2015). Fungal endophytes enhance agronomically important traits in severely drought-stressed barley. Journal of Agronomy and Crop Science, 201, 419–427.CrossRefGoogle Scholar
Murphy, B. R., Doohan, F. M., Hodkinson, T. R. (2018). From concept to commerce: developing a successful fungal endophyte inoculant for agricultural crops. Journal of Fungi, 4, 24.CrossRefGoogle ScholarPubMed
Murphy, B. R., Doohan, F. M and Hodkinson, T. R. (2019). Prospecting crop wild relatives for beneficial endophytes. In Endophytes for a Growing World, ed. Hodkinson, T. R., Doohan, F. M., Saunders, M. J. and Murphy, B. R.. Cambridge: Cambridge University Press, Chapter 18.Google Scholar
Oerke, E. C. and Dehne, H. W. (2004). Safeguarding production: losses in major crops and the role of crop protection. Crop Protection, 23, 275–285.CrossRefGoogle Scholar
Ownley, B. H., Pereira, R. M., Klingeman, W. E., Quigley, N. B. and Leckie, B. M. (2004). Beauveria bassiana, a dual purpose biocontrol organism, with activity against insect pests and plant pathogens. In Emerging Concepts in Plant Health Management, ed. Lartey, R. T. and Caesar, A. J.. Kerala, India: Research Signposts, pp. 255–269.Google Scholar
Ownley, B. H., Griffin, M. R., Klingeman, W. E. et al. (2008). Beauveria bassiana: endophytic colonization and plant disease control. Journal of Invertebrate Pathology, 98, 267–270.CrossRefGoogle ScholarPubMed
Ownley, B., Gwinn, K. and Vega, F. (2010). Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol, 55, 113–128.CrossRefGoogle Scholar
Parine, N. R., Devinder, K., Khan, P. A. A. and Varaprasad, B. (2010). Antifungal efficacy of secondary metabolites from entomopathogenic fungi Beauveria bassiana. Journal of Pharmacy Research, 3, 855–856.Google Scholar
Parsa, S., Ortiz, V. and Vega, F. E. (2013). Establishing fungal entomopathogens as endophytes: towards endophytic biological control. JoVE, 74, e50360.Google Scholar
Pereira, R., Stimac, J. and Alves, S. (1993). Soil antagonism affecting the dose- response of workers of the red imported fire ant Solenopsis invicta, to Beauveria bassiana conidia. Journal of Invertebrate Pathology, 61, 156–161.CrossRefGoogle Scholar
Petrini, O. (1991). Fungal endophytes of tree leaves. In Microbial Ecology of Leaves, ed. Andrews, J. H. and Hirano, S. S.. New York, NY: Springer, pp. 179–197.CrossRefGoogle Scholar
Pieterse, C. M., Van Wees, S. C., Van Pelt, J. A. et al. (1998). A novel signaling pathway controlling induced systemic resistance in Arabidopsis. The Plant Cell, 10, 1571–1580.CrossRefGoogle ScholarPubMed
Posada, F., Aime, M. C., Peterson, S. W., Rehner, S. A. and Vega, F. E. (2007). Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycological Research, 111, 748–757.CrossRefGoogle ScholarPubMed
Posada, F. J., Chaves, F. C., Gianfagna, T. J., Pava-Ripoll, M. and Hebbar, P. (2010). Establishment of the fungal entomopathogen Beauveria bassiana as an endophyte in cocoa pods (Theobroma cacao L.). Revista UDCA Actualidad & Divulgación Científica, 13, 71–78.Google Scholar
Powell, W. A., Klingeman, W. E., Ownley, B. H. and Gwinn, K. D. (2009). Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). Journal of Entomological Science, 44, 391–396.CrossRefGoogle Scholar
Quesada-Moraga, E. and Vey, A. (2004). Bassiacridin, a protein toxic for locusts secreted by the entomopathogenic fungus Beauveria bassiana. Mycological Research, 108, 441–452.CrossRefGoogle ScholarPubMed
Quesada-Moraga, E., Ruiz-García, A. and Santiago-Alvarez, C. (2006). Laboratory evaluation of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against puparia and adults of Ceratitis capitata (Diptera: Tephritidae). Journal of Economic Entomology, 99, 1955–1966.CrossRefGoogle Scholar
Quesada-Moraga, E., Muñoz-Ledesma, F. J. and Santiago-Alvarez, 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.CrossRefGoogle ScholarPubMed
Quesada-Moraga, E., López-Díaz, C. and Landa, B. B. (2014). The hidden habit of the entomopathogenic fungus Beauveria bassiana: first demonstration of vertical plant transmission. PloS One, 9, e89278.CrossRefGoogle ScholarPubMed
Ravindran, K., Chitra, S., Wilson, A. and Sivaramakrishnan, S. (2014). Evaluation of antifungal activity of Metarhizium anisopliae against plant phytopathogenic fungi. In Microbial Diversity and Biotechnology in Food Security, ed. Kharwar, R. N., Upadhyay, R. S., Dubey, N. K. and Raghuwanshi, R.. India: Springer, pp. 251–255.CrossRefGoogle Scholar
Rehner, S. A., Minnis, A. M., Sung, G.-H., Luangsa-ard, J. J., Devotto, L. and Humber, R. A. (2011). Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia, 103, 1055–1073.CrossRefGoogle ScholarPubMed
Roberts, D. W. and Hajek, A. E. (1992). Entomopathogenic fungi as bioinsecticides. In Frontiers in Industrial Mycology, ed. G. Leatham. New York: Chapman and Hall, pp. 144–159.CrossRefGoogle Scholar
Roberts, D. W. and Leger, R. J. S. (2004). Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Advances in Applied Microbiology, 54, 1–70.CrossRefGoogle ScholarPubMed
Rodríguez, R., WhiteJr, J., Arnold, A. and Redman, R. (2009). Fungal endophytes: diversity and functional roles. New Phytologist, 182, 314–330.CrossRefGoogle ScholarPubMed
Rondot, Y. and Reineke, A. (2016). Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biological Control, 116, 82–89.CrossRefGoogle Scholar
Ryu, C. M., Hu, C. H., Reddy, M. S. and Kloepper, J. W. (2003). Different signaling pathways of induced resistance by rhizobacteria in Arabidopsis thaliana against two pathovars of Pseudomonas syringae. New Phytologist, 160, 413–420.CrossRefGoogle ScholarPubMed
Sánchez Márquez, S., Bills, G. F., Herrero, N. and Zabalgogeazcoa, I. (2011). Non-systemic fungal endophytes of grasses. Fungal Ecology, 5, 289–297.CrossRefGoogle Scholar
Sasan, R. K. and 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.CrossRefGoogle ScholarPubMed
Sasan, R. K. and Bidochka, M. J. (2013). Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Canadian Journal of Plant Pathology, 35, 288–293.CrossRefGoogle Scholar
Shah, F. A., Ansari, M. A., Watkins, J. et al. (2009). Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocontrol Science and Technology, 19, 743–753.CrossRefGoogle Scholar
Sharma, P. (2011). Complexity of ‘Trichoderma-fusarium’ interaction and manifestation of biological control. Australian Journal of Crop Science, 5, 1027–1038.Google Scholar
Shoresh, M., Harman, G. E. and Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology, 48, 21–43.CrossRefGoogle ScholarPubMed
Soper, R. S. and Ward, M. G. (1981). Production, formulation and application of fungi for insect control. In Biological Control in Crop Production, BARC Symposium No. 5, ed. Papavizas, G. C.. Montclair, NJ: Allanheld, Osmun, pp. 161–180.Google Scholar
Stone, J., Polishook, J. and White, J. (2004). Endophytic fungi. In Biodiversity of Fungi, Inventory and Monitoring Methods, ed. Mueller, G. M., Bills, G. F. and Foster, M. S.. Amsterdam: Elsevier, pp. 241–270.CrossRefGoogle Scholar
Strobel, G. and Daisy, B. (2003). Bioprospecting for microbial endophytes and their natural products. Microbiology and Molecular Biology Reviews, 67, 491–502.CrossRefGoogle ScholarPubMed
Susuki, A., Kanaoka, M., Isogai, A. et al. (1977). Bassianolide, a new insecticidal cyclodepsipeptide from Beauveria bassiana and Verticillium lecanni. Tetrahedrom, 25, 2167–2170.CrossRefGoogle Scholar
Tefera, T. and Vidal, S. (2009). Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. Biocontrol, 4, 663–669.CrossRefGoogle Scholar
Taylor, A. G. and Harman, G. E. (1990). Concepts and technologies of selected seed treatments. Annual Review of Phytopathology, 28, 321–339.CrossRefGoogle Scholar
Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. and Polasky, S. (2002). Agricultural sustainability and intensive production practices. Nature, 418, 671–677.CrossRefGoogle ScholarPubMed
Vega, F., Posada, F., Aime, M. et al. (2008). Entomopathogenic fungal endophytes. Biological Control, 46, 72–82.CrossRefGoogle Scholar
Vega, F. E., Goettel, M. S., Blackwell, M. et al. (2009). Fungal entomopathogens: new insights on their ecology. Fungal Ecology, 2, 149–159.CrossRefGoogle Scholar
Vega, F. E., Meyling, N. V., Luangsaard, J. J. and Blackwell, M. (2012). Fungal entomopathogens. Insect Pathology, 2, 171–220.CrossRefGoogle Scholar
Venugopalan, A. and Srivastava, S. (2015). Endophytes as in vitro production platforms of high value plant secondary metabolites. Biotechnology Advances, 33, 873–887.CrossRefGoogle ScholarPubMed
Vicari, M., Hatcher, P. and Ayres, P. (2002). Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology, 83, 2452–2464.CrossRefGoogle Scholar
Vidal, S. and Jaber, L. R. (2015). Entomopathogenic fungi as endophytes: plant–endophyte–herbivore interactions and prospects for use in biological control. Current Science, 109, 46–54.Google Scholar
Vining, L., Kelleher, W. and Schwarting, A. (1962). Oosporein production by a strain of Beauveria bassiana originally identified as Amanita muscaria. Canadian Journal of Microbiology, 8, 931–933.CrossRefGoogle Scholar
Wagner, B. L. and Lewis, L. C., (2000). Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology 66, 3468–3473.CrossRefGoogle ScholarPubMed
Wang, C. and Wang, S. (2017). Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annual Review of Entomology, 62, 73–90.CrossRefGoogle ScholarPubMed
Wang, Q. and Xu, L. (2012). Beauvericin, a bioactive compound produced by fungi: a short review. Molecules, 17, 2367–2377.CrossRefGoogle ScholarPubMed
Wang, X., Radwan, M. M., Taráwneh, A. H. et al. (2013). Antifungal activity against plant pathogens of metabolites from the endophytic fungus Cladosporium cladosporioides. Journal of Agricultural and Food Chemistry, 61, 4551–4555.CrossRefGoogle ScholarPubMed
White, T. J., Bruns, T. D., Lee, S. and Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications, ed. Innis, M. A., Gelfand, D. H., Sninsky, J. J. and White, T. J.. New York: Academic Press, pp. 315–322.Google Scholar
Wilson, D. (1995). Endophyte: the evolution of a term, and clarification of its use and definition. Oikos, 73, 274–276.CrossRefGoogle Scholar
Xu, Y., Orozco, R., Wijeratne, E. K. et al. (2009). Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana. Fungal Genetics and Biology, 46, 353–364.CrossRefGoogle ScholarPubMed
Xu, L., Wang, J., Zhao, J. et al. (2010). Beauvericin from the endophytic fungus, Fusarium redolens, isolated from Dioscorea zingiberensis and its antibacterial activity. Natural Product Communications, 5, 811–814.CrossRefGoogle ScholarPubMed

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