Probiotics for Plants? Growth Promotion by the Entomopathogenic Fungus Beauveria bassiana Depends on Nutrient Availability

  • Susanna Tall
  • Nicolai V. Meyling
Plant Microbe Interactions


Cultivation of crops requires nutrient supplements which are costly and impact the environment. Furthermore, global demands for increased crop production call for sustainable solutions to increase yield and utilize resources such as nutrients more effectively. Some entomopathogenic fungi are able to promote plant growth, but studies over such effects have been conducted under optimal conditions where nutrients are abundantly available. We studied the effects of Beauveria bassiana (strain GHA) seed treatment on the growth of maize (Zea mays) at high and low nutrient conditions during 6 weeks in greenhouse. As expected, B. bassiana seed treatment increased plant growth, but only at high nutrient conditions. In contrast, the seed treatment did not benefit plant growth at low nutrient conditions where the fungus potentially constituted a sink and tended to reduce plant growth. The occurrence of endophytic B. bassiana in experimental plant tissues was evaluated by PCR after 6 weeks, but B. bassiana was not documented in any of the above-ground plant tissues indicating that the fungus-plant interaction was independent of endophytic establishment. Our results suggest that B. bassiana seed treatment could be used as a growth promoter of maize when nutrients are abundantly available, while the fungus does not provide any growth benefits when nutrients are scarce.


Plant-microbe interactions Entomopathogenic fungi Symbiosis Endophyte Context dependency 



We thank Maya Pedersen for assistance in the greenhouse and Professor Helle Sørensen for statistical advice.

Funding Information

ST was supported by a Marie Curie Intra European Fellowship (grant no. 331125), the Foundations’ Postdoc Pool, and Osk. Huttunen Foundation.


  1. 1.
    Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrance D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818CrossRefPubMedGoogle Scholar
  2. 2.
    Montanez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28CrossRefGoogle Scholar
  3. 3.
    Pineda A, Zheng S-J, van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514CrossRefPubMedGoogle Scholar
  4. 4.
    Lugtenberg BJJ, Caradus JR, Johnson LJ (2016) Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol 92:fiw194. CrossRefPubMedGoogle Scholar
  5. 5.
    Vega FE, Meyling NV, Luangsa-Ard JJ, Blackwell M (2012) Fungal entomopathogens. In: Vega FE, Kaya HK (eds) Insect pathology 2nd edn. Academic Press, Amsterdam, pp 171–220CrossRefGoogle Scholar
  6. 6.
    Behie SW, Jones SJ, Bidochka MJ (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119CrossRefGoogle Scholar
  7. 7.
    Barelli L, Moonjely S, Behie SW, Bidochka MJ (2016) Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Mol Biol 90:657–664CrossRefPubMedGoogle Scholar
  8. 8.
    Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107CrossRefPubMedGoogle Scholar
  9. 9.
    Lopez DC, Sword GA (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). Biol Control 89:53–60CrossRefGoogle Scholar
  10. 10.
    Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45CrossRefGoogle Scholar
  11. 11.
    Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577CrossRefPubMedGoogle Scholar
  12. 12.
    Behie SW, Bidochka MJ (2014) Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Appl Environ Microbiol 80:1553–1560CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kabaluk JT, Ericsson JD (2007) Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agric J 99:1377–1381Google Scholar
  14. 14.
    Liao XG, O’Brien TR, Fang W, St, Leger RJ (2014) The plant beneficial effects of Metarhizium correlate with their association with roots. Appl Microbiol Biotechnol 98:7089–7096CrossRefPubMedGoogle Scholar
  15. 15.
    Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  16. 16.
    McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR (2017) Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl 62:1–17CrossRefGoogle Scholar
  17. 17.
    Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hubner) (Lepidoptera, Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211CrossRefGoogle Scholar
  18. 18.
    Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Technol 27:28–41CrossRefGoogle Scholar
  19. 19.
    Parsa S, Ortiz V, Vega FE (2013) Establishing fungal entomopathogens as endophytes: towards endophytic biological control. J Vis Exp (74):50360Google Scholar
  20. 20.
    Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  21. 21.
    Landa BB, Lopez-Diaz C, Jimenez-Fernandez D, Montes-Borrego M, Munoz-Ledesma FJ, Ortiz-Urquiza A, Quesada-Moraga E (2013) 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 114:128–138CrossRefPubMedGoogle Scholar
  22. 22.
    Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997CrossRefPubMedGoogle Scholar
  23. 23.
    SAS (1991) SAS system for statistical graphics1st edn. SAS Institute Inc., CaryGoogle Scholar
  24. 24.
    Tukey JW (1977) Exploratory data analysis. Addison-Wesley, ReadingGoogle Scholar
  25. 25.
    Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39CrossRefGoogle Scholar
  26. 26.
    Megali L, Schlau B, Rasmann S (2015) Soil inoculation increases corn yield and insect attack. Agron Sustain Dev 35:1511–1519CrossRefGoogle Scholar
  27. 27.
    Keyser CA, Thorup-Kristensen K, Meyling NV (2014) Metarhizium seed treatment mediates fungal dispersal via roots and induces infections in insects. Fungal Ecol 11:122–131CrossRefGoogle Scholar
  28. 28.
    Behie SW, Moreira CC, Sementchoukova I, Barelli L, Zelisko PM, Bidochka MJ (2017) Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nat Commun 8:14245CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113CrossRefGoogle Scholar
  30. 30.
    Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127CrossRefPubMedGoogle Scholar
  31. 31.
    Spiering MJ, Greer DH, Schmid J (2006) Effects of the fungal endophyte, Neotyphodium lolii, on net photosynthesis and growth rates of perennial ryegrass (Lolium perenne) are independent of in planta endophyte concentration. Ann Bot 98:379–387CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Cheplick GP, Clay K, Marks S (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97CrossRefGoogle Scholar
  33. 33.
    Bacon CW (1993) Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agric Ecosyst Environ 44:123–141CrossRefGoogle Scholar
  34. 34.
    Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161:310–325CrossRefPubMedGoogle Scholar
  35. 35.
    Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41CrossRefGoogle Scholar
  36. 36.
    Russo ML, Pelizza SA, Cabello MN, Stenglein SA, Scorsetti AC (2015) Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales). Biocontrol Sci Technol 25:475–480CrossRefGoogle Scholar
  37. 37.
    Biswas C, Dey P, Satpathy S, Satya P, Mahapatra BS (2013) Endophytic colonization of white jute (Corchorus capsularis) plants by different Beauveria bassiana strains for managing stem weevil (Apion corchori). Phytoparasitica 41:17–21CrossRefGoogle Scholar
  38. 38.
    Powell WA, Klingeman WE, Ownley BH, Gwinn K (2009) Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). J Entomol Sci 44:391–396CrossRefGoogle Scholar
  39. 39.
    Dara SK, Dara SR, Dara SS (2013) Endophytic colonization and pest management potential of Beauveria bassiana in strawberries. J Berry Res 3:203–211Google Scholar
  40. 40.
    Santyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR (2016) Plant growth promoting bacterial endophytes. Microbiol Res 183:92–99CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Plant and Environmental SciencesUniversity of CopenhagenFrederiksberg CDenmark

Personalised recommendations