Endophytic fungi protect tomato and nightshade plants against Tuta absoluta (Lepidoptera: Gelechiidae) through a hidden friendship and cryptic battle
1.
Ekesi, S., Chabi-Olaye, A., Subramanian, S. & Borgemeister, C. Horticultural pest management and the African economy: successes, challenges and opportunities in a changing global environment. Acta Hortic. 911, 165–183 (2011).
Article Google Scholar
2.
Pratt, C. F., Constantine, K. L. & Murphy, S. T. Economic impacts of invasive alien species on African smallholder livelihoods. Glob. Food Secur. 14, 31–37 (2017).
Article Google Scholar
3.
Desneux, N., Luna, M. G., Guillemaud, T. & Urbaneja, A. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J. Pest Sci. 84, 403–408 (2011).
Article Google Scholar
4.
Idriss, G. E. A. et al. Host range and effects of plant species on preference and fitness of Tuta absoluta (Lepidoptera: Gelechiidae). J. Econ. Entomol. https://doi.org/10.1093/jee/toaa002 (2020).
Article PubMed Google Scholar
5.
Aigbedion-Atalor, P. O. et al. The South America tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), spreads its wings in Eastern Africa: distribution and socioeconomic impacts. J. Econ. Entomol. 112, 2797–2807 (2019).
PubMed Article Google Scholar
6.
Biondi, A., Guedes, R. N. C., Wan, F.-H. & Desneux, N. Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu. Rev. Entomol. 63, 239–258 (2018).
CAS PubMed Article Google Scholar
7.
Desneux, N. et al. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J. Pest Sci. 83, 197–215 (2010).
Article Google Scholar
8.
Guedes, R. N. C. C. et al. Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. J. Pest Sci. 92, 1329–1342 (2019).
Article Google Scholar
9.
Dimbi, S., Maniania, N. K. & Ekesi, S. Horizontal transmission of Metarhizium anisopliae in fruit flies and effect of fungal infection on egg laying and fertility. Insects 4, 206–216 (2013).
PubMed PubMed Central Article Google Scholar
10.
Maniania, N. K., Ekesi, S. & Dolinski, C. Entomopathogens routinely used in pest control strategies: orchards in tropical climate. In Microbial Control of Insect and Mite Pests: From Theory to Practice (Elsevier Inc., 2016). https://doi.org/10.1016/B978-0-12-803527-6.00018-4.
11.
Mweke, A. et al. Evaluation of the entomopathogenic fungi Metarhizium anisopliae, Beauveria bassiana and Isaria sp. for the management of Aphis craccivora (Hemiptera: Aphididdae). J. Econ. Entomol. 111, 1587–1594 (2018).
ADS CAS PubMed Article Google Scholar
12.
Akutse, K. S. et al. Ovicidal effects of entomopathogenic fungal isolates on the invasive Fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). J. Appl. Entomol. 143, 626–634 (2019).
CAS Article Google Scholar
13.
Akutse, K. S., Subramanian, S., Khamis, F. M., Ekesi, S. & Mohamed, S. A. Entomopathogenic fungus isolates for adult Tuta absoluta (Lepidoptera: Gelechiidae) management and their compatibility with Tuta pheromone. J. Appl. Entomol. https://doi.org/10.1111/jen.12812 (2020).
Article Google Scholar
14.
Inglis, G. D., Goettel, M. S., Butt, T. M. & Strasser, H. Use of hyphomycetous fungi for managing insect pests. In Fungi as Biocontrol Agents: Progress, Problems and Potential (eds. Butt, T. M. & Magan, M.) 23–69 (2001). https://doi.org/10.1079/9780851993560.0023.
15.
Behie, S. W. & Bidochka, M. J. 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 (2014).
PubMed PubMed Central Article CAS Google Scholar
16.
Akutse, K. S., Khamis, F. M., Ekesi, S., Wekesa, S. & Subramanian, S. Effect of endophytically-colonized tomato and nightshade host plants on life-history parameters of Tuta absoluta (Lepidoptera: Gelechiidae). (International Congress on Invertebrate Pathology and Microbial Control and 52nd Annual Meeting of the Society for Invertebrate Pathology & 17th Meeting of the IOBC‐WPRS Working Group “Microbial and Nematode Control of Invertebrate Pests”, 2019).
17.
Wilson, D. Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73, 274–276 (1995).
Article Google Scholar
18.
Quesada-Moraga, E., Muñoz-Ledesma, F. J. & Santiago-Álvarez, C. Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ. Entomol. 38, 723–730 (2009).
CAS PubMed Article Google Scholar
19.
Barelli, L., Moonjely, S., Behie, S. W. & Bidochka, M. J. Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Mol. Biol. 90, 657–664 (2016).
CAS PubMed Article Google Scholar
20.
Latz, M. A. C., Jensen, B., Collinge, D. B. & Jørgensen, H. J. L. Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecol. Divers. 11, 555–567 (2018).
Article Google Scholar
21.
Ownley, B. H. et al. Beauveria bassiana: endophytic colonization and plant disease control. J. Invertebr. Pathol. 98, 267–270 (2008).
CAS PubMed Article Google Scholar
22.
Akello, J. & Sikora, R. Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biol. Control 61, 215–221 (2012).
Article Google Scholar
23.
Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van den Berg, J. & Ekesi, S. 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 Ecol. 6, 293–301 (2013).
Article Google Scholar
24.
Russo, M. L. et al. Endophytic effects of Beauveria bassiana on Corn (Zea mays) and its herbivore, Rachiplusia nu (Lepidoptera: Noctuidae). Insects 10, 2–9 (2019).
Article Google Scholar
25.
Lahrmann, U. et al. Host-related metabolic cues affect colonization strategies of a root endophyte. Proc. Natl. Acad. Sci. USA 110, 13965–13970 (2013).
ADS CAS PubMed Article Google Scholar
26.
Fadiji, A. E. & Babalola, O. O. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front. Bioeng. Biotechnol. 8, 1–20 (2020).
Article Google Scholar
27.
Gathage, J. W. et al. Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. Biocontrol 61, 741–753 (2016).
Article Google Scholar
28.
Muvea, A. M. et al. Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE 9, 1–7 (2014).
Article CAS Google Scholar
29.
Powell, W. A., Klingeman, W. E., Ownley, B. H. & Gwinn, K. D. Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). J. Entomol. Sci. 44, 391–396 (2009).
Article Google Scholar
30.
Klieber, J. & Reineke, A. The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. J. Appl. Entomol. 140, 580–589 (2016).
CAS Article Google Scholar
31.
Resquín-romero, G., Garrido-jurado, I., Delso, C., Ríos-moreno, A. & Quesada-moraga, E. Transient endophytic colonizations of plants improve the outcome of foliar applications of mycoinsecticides against chewing insects. J. Invertebr. Pathol. 136, 23–31 (2016).
PubMed Article CAS Google Scholar
32.
Mutune, B. et al. Fungal endophytes as promising tools for the management of bean stem maggot Ophiomyia phaseoli on beans Phaseolus vulgaris. J. Pest Sci. 89, 993–1001 (2016).
Article Google Scholar
33.
Posada, F., Aime, M. C., Peterson, S. W., Rehner, S. A. & Vega, F. E. Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol. Res. 111, 748–757 (2007).
CAS PubMed Article Google Scholar
34.
Bing, L. A. & Lewis, L. C. Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ. Entomol. 20, 1207–1211 (1991).
Article Google Scholar
35.
Behie, S. W., Jones, S. J., Bidochka, M. J. & Hyde, K. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol. 13, 112–119 (2015).
Article Google Scholar
36.
Akello, J. et al. Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J. Invertebr. Pathol. 96, 34–42 (2007).
PubMed Article Google Scholar
37.
Posada, F. J. & Vega, F. E. A new method to evaluate the biocontrol potential of single spore isolates of fungal entomopathogens. J. Insect Sci. 5, 1–10 (2005).
Article Google Scholar
38.
Demers, J. E., Gugino, B. K. & del Jiménez-Gasco, M. Highly diverse endophytic and soil Fusarium oxysporum populations associated with field-grown tomato plants. Appl. Environ. Microbiol. 81, 81–90 (2015).
PubMed Article CAS Google Scholar
39.
Bogner, C. W. et al. Fungal root endophytes of tomato from Kenya and their nematode biocontrol potential. Mycol. Prog. 15, 1–17 (2016).
Article Google Scholar
40.
Hardoim, P. R. et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev. 79, 293–320 (2015).
PubMed PubMed Central Article Google Scholar
41.
Martin, J. T. Role of cuticle in the defense against plant disease. Annu. Rev. Phytopathol. 2, 81–100 (1964).
Article Google Scholar
42.
Jensen, R. E., Enkegaard, A. & Steenberg, T. Increased fecundity of Aphis fabae on Vicia faba plants following seed or leaf inoculation with the entomopathogenic fungus Beauveria bassiana. PLoS ONE 14, 1–12 (2019).
Google Scholar
43.
Landa, B. B. et al. In-planta detection and monitorization of endophytic colonization by a Beauveria bassiana strain using a new-developed nested and quantitative PCR-based assay and confocal laser scanning microscopy. J. Invertebr. Pathol. 114, 128–138 (2013).
CAS PubMed Article Google Scholar
44.
Bing, L. A. & Lewis, L. C. Endophytic Beauveria bassiana (Balsamo) Vuillemin in corn: The influence of the plant growth stage and Ostrinia nubilalis (Hubner). Biocontrol Sci. Technol. 2, 39–47 (1992).
Article Google Scholar
45.
Greenfield, M. et al. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol. Control 95, 40–48 (2016).
PubMed PubMed Central Article Google Scholar
46.
Card, S., Johnson, L., Teasdale, S. & Caradus, J. Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiol. Ecol. 92, 1–19 (2016).
Article CAS Google Scholar
47.
Philippot, L., Raaijmakers, J. M., Lemanceau, P. & Van Der Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Publ. Gr. 11, 789–799 (2013).
CAS Google Scholar
48.
Tumuhaise, V. et al. Pathogenicity and performance of two candidate isolates of Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) in four liquid culture media for the management of the legume pod borer Maruca vitrata (Lepidoptera: Crambidae). Int. J. Trop. Insect Sci. 35, 34–47 (2015).
Article Google Scholar
49.
Branine, M., Bazzicalupo, A. & Branco, S. Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog. 15, 1–7 (2019).
Article CAS Google Scholar
50.
Barelli, L., Moreira, C. C. & Bidochka, M. J. Initial stages of endophytic colonization by Metarhizium involves rhizoplane colonization. Microbiology 164, 1531–1540 (2018).
CAS PubMed Article Google Scholar
51.
Wyrebek, M., Huber, C., Sasan, R. K. & Bidochka, M. J. Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity. Microbiology 157, 2904–2911 (2011).
CAS PubMed Article Google Scholar
52.
Muvea, A. M. et al. Behavioral responses of Thrips tabaci Lindeman to endophyte-inoculated onion plants. J. Pest Sci. 88, 555–562 (2015).
Article Google Scholar
53.
Slansky, F. Jr. Insect nutrition: an adaptationist’s perspective. Florida Entomol. 65, 45–71 (1982).
Article Google Scholar
54.
Carroll, G. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69, 2–9 (1988).
Article Google Scholar
55.
Allegrucci, N., Velazquez, M. S., Russo, M. L., Perez, E. & Scorsetti, A. C. Endophytic colonisation of tomato by the entomopathogenic fungus Beauveria bassiana: the use of different inoculation techniques and their effects on the tomato leafminer Tuta absoluta (Lepidoptera : Gelechiidae). J. Plant Prot. Res. 54, 331–337 (2017).
Google Scholar
56.
Barta, M. In planta bioassay on the effects of endophytic Beauveria strains against larvae of horse-chestnut leaf miner (Cameraria ohridella). Biol. Control 121, 88–98 (2018).
Article Google Scholar
57.
Russo, M. L. et al. Effect of endophytic entomopathogenic fungi on soybean Glycine max (L.) Merr. growth and yield. J. King Saud Univ. Sci. 31, 728–736 (2018).
Article Google Scholar
58.
Contreras-cornejo, H. A., Macías-rodríguez, L. & Larsen, J. The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl. Soil Ecol. 124, 45–53 (2017).
Article Google Scholar
59.
Contreras-Cornejo, H. A., Macías-Rodríguez, L., Del Val, E. & Larsen, J. Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol. Ecol. 92, 1–17 (2016).
Article CAS Google Scholar
60.
Coppola, M. et al. Trichoderma harzianum enhances tomato indirect defense against aphids. Insect Sci. 24, 1025–1033 (2017).
CAS PubMed Article Google Scholar
61.
Meera, M. S., Shivanna, M. B., Kageyama, K. & Hyakumachi, M. Persistence of induced systemic resistance in cucumber in relation to root colonization by plant growth promoting fungal isolates. Crop Prot. 14, 123–130 (1995).
Article Google Scholar
62.
Lewis, L. C., Berry, E. C., Obrycki, J. J. & Bing, L. A. Aptness of insecticides (Bacillus thuringiensis and carbofuran ) with endophytic Beauveria bassiana, in suppressing larval populations of the European corn borer. Agric. Ecosyst. Environ. 57, 27–34 (1996).
Article Google Scholar
63.
Qayyum, M. A., Wakil, W., Arif, M. J., Sahi, S. T. & Dunlap, C. A. Infection of Helicoverpa armigera by endophytic Beauveria bassiana colonizing tomato plants. Biol. Control 90, 200–207 (2015).
Article Google Scholar
64.
Jallow, M. F. A., Dugassa-Gobena, D. & Vidal, S. Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod. Plant. Interact. 2, 53–62 (2008).
Article Google Scholar
65.
Jaber, L. R. & Vidal, S. Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecol. Entomol. 35, 25–36 (2010).
Article Google Scholar
66.
Davis, T. S., Crippen, T. L., Hofstetter, R. W. & Tomberlin, J. K. Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 39, 840–859 (2013).
CAS PubMed Article Google Scholar
67.
Silva, D. B., Bueno, V. H. P., Lins, J. C. & Van Lenteren, J. C. Life history data and population growth of Tuta absoluta at constant and alternating temperatures on two tomato lines. Bull. Insectol. 68, 223–232 (2015).
Google Scholar
68.
Pereyra, P. C. & Sánchez, N. E. Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop. Entomol. 35, 671–676 (2006).
PubMed Article Google Scholar
69.
Dash, C. K. et al. Endophytic entomopathogenic fungi enhance the growth of Phaseolus vulgaris L. (Fabaceae) and negatively affect the development and reproduction of Tetranychus urticae Koch (Acari: Tetranychidae). Microb. Pathog. 125, 385–392 (2018).
PubMed Article Google Scholar
70.
Akello, J., Dubois, T., Coyne, D. & Kyamanywa, S. Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage. Crop Prot. 27, 1437–1441 (2008).
Article Google Scholar
71.
Golo, P. S. et al. Production of destruxins from Metarhizium spp. fungi in artificial medium and in endophytically colonized cowpea plants. PLoS ONE 9, 1–9 (2014).
Article CAS Google Scholar
72.
Goettel, M. S. & Inglis, D. G. Fungi: Hyphomycetes. Manual of Techniques in Insect Pathology (1997). https://doi.org/10.1016/B978-012432555-5/50013-0.
73.
Schulz, B., Guske, S., Dammann, U. & Boyle, C. Endophyte-host interactions. II. Defining symbiosis of the endophyte–host interaction. Symbiosis 25, 213–227 (1998).
Google Scholar
74.
Inglis, G. D., Enkerli, J. & Goettel, M. S. Laboratory Techniques Used for Entomopathogenic Fungi. Hypocreales. Manual of Techniques in Invertebrate Pathology (Elsevier, New York, 2012). https://doi.org/10.1016/B978-0-12-386899-2.00007-5
Google Scholar
75.
Petrini, O. & Fisher, P. J. Fungal endophytes in Salicornia perennis. Trans. Br. Mycol. Soc. 87, 647–651 (1986).
Article Google Scholar
76.
Aigbedion-Atalor, P. O. et al. Host stage preference and performance of Dolichogenidea gelechiidivoris (Hymenoptera: Braconidae), a candidate for classical biological control of Tuta absoluta in Africa. Biol. Control 144, 1–8 (2020).
Article CAS Google Scholar
77.
Oliveira, F. A., da Silva, D. J. H., Leite, G. L. D., Jham, G. N. & Picanço, M. Resistance of 57 greenhouse-grown accessions of Lycopersicon esculentum and three cultivars to Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Sci. Hortic. (Amsterdam) 119, 182–187 (2009).
CAS Article Google Scholar
78.
Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).
MathSciNet MATH Article Google Scholar
79.
De Mendiburu, F. agricolae: statistical procedures for agricultural research. R package version 1.3–2 https://CRAN.R-project.org/package=agricolae (2020).
80.
Therneau, T. A Package for Survival Analysis in R. R package version 3.1-12, https://CRAN.R-project.org/package=survival. (2020).
81.
Crawley, M. J. The R Book (Wiley, New York, 2007). https://doi.org/10.1002/9780470515075.
Google Scholar
82.
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2019).
Google Scholar More