Increased fecundity of Aphis fabae on Vicia faba plants following seed or leaf inoculation with the entomopathogenic fungus Beauveria bassiana

Autoři: Rasmus Emil Jensen aff001;  Annie Enkegaard aff001;  Tove Steenberg aff001
Působiště autorů: Department of Agroecology, Section of Plant Pathology and Entomology, Aarhus University, Flakkebjerg, Denmark aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223616


Since the discovery that entomopathogenic fungi can live inside plants as endophytes, researchers have been trying to understand how this affects mainly plants and herbivores. We studied how inoculation of Vicia faba L. (Fabales: Fabaceae) plants with Beauveria bassiana (Balsamo-Crivelli) Vuillemin (Ascomycota: Hypocreales) (strain GHA) either via the seeds or leaves influenced the nymph production of two successive generations of Aphis fabae Scopoli (Hemiptera: Aphididae). While we did not find any difference in nymph production for the first generation of aphids, second-generation aphids on both seed- and spray inoculated plants produced significantly higher numbers of nymphs than aphids on uninoculated plants. This emphasizes the importance of two (or multi-) generational experimentation. Beauveria bassiana was recovered from 26.0, 68.8 and 6.3% of respectively seed-, spray inoculated and control plants, thus, demonstrating its ability to live as an endophyte in V. faba. The confirmation that plants inoculated with entomopathogenic fungi can have a positive effect on pest insects makes careful consideration of these multi-trophic interactions imperative.

Klíčová slova:

Aphids – Fecundity – Fungi – Leaves – Nymphs – Plant fungal pathogens – Plant-herbivore interactions – Seeds


1. Wei Z, Yang T, Friman VP, Xu Y, Shen Q, Jousset A. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun. 2015;6:8413. doi: 10.1038/ncomms9413 26400552

2. Marschner H, Dell B. Nutrient uptake in mycorrhizal symbiosis. Plant and Soil. 1994;159:13.

3. Pineda A, Zheng SJ, van Loon JJ, Pieterse CM, Dicke M. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 2010;15(9):507–14. doi: 10.1016/j.tplants.2010.05.007 20542720

4. Khan AL, Kang S-M, Su Rehman, Hamayun M, Shinwari ZK, Kim J-G, et al. Pure culture of Metarhizium anisopliae LHL07 reprograms soybean to higher growth and mitigates salt stress. World J Microbiol Biotechnol. 2012;28. doi: 10.1007/s11274-011-0950-9 22805930

5. Bing LA, Lewis LC. Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by Endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol. 1991;20(4):5.

6. Wang JB, St Leger RJ, Wang C. Advances in Genomics of Entomopathogenic Fungi. Adv Genet. 2016;94:67–105. doi: 10.1016/bs.adgen.2016.01.002 27131323

7. Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F, Rehner SA. Entomopathogenic fungal endophytes. Biological Control. 2008;46(1):72–82. doi: 10.1016/j.biocontrol.2008.01.008

8. Ownley BH, Gwinn KD, Vega FE. Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl. 2010;55(1):113–28. doi: 10.1007/s10526-009-9241-x

9. Guesmi-Jouini J, Garrido-Jurado I, Lopez-Diaz C, Ben Halima-Kamel M, Quesada-Moraga E. Establishment of fungal entomopathogens Beauveria bassiana and Bionectria ochroleuca (Ascomycota: Hypocreales) as endophytes on artichoke Cynara scolymus. J Invertebr Pathol. 2014;119:1–4. doi: 10.1016/j.jip.2014.03.004 24681358

10. Jaber LR, Ownley BH. Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biological Control. 2017;107:50–9. doi: 10.1016/j.biocontrol.2017.01.013

11. Vega FE. Insect pathology and fungal endophytes. J Invertebr Pathol. 2008;98(3):277–9. doi: 10.1016/j.jip.2008.01.008 18406422

12. Vidal S, Jaber LR. Entomopathogenic fungi as endophytes: plant–endophyte–herbivore interactions and prospects for use in biological control. Current Science. 2015;109.

13. Vega FE. The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia. 2018;110(1):4–30. doi: 10.1080/00275514.2017.1418578 29863999

14. Russo ML, Pelizza SA, Vianna MF, Allegrucci N, Cabello MN, Toledo AV, et al. Effect of endophytic entomopathogenic fungi on soybean Glycine max (L.) Merr. growth and yield. Journal of King Saud University—Science. 2018. doi: 10.1016/j.jksus.2018.04.008

15. Allegrucci N, Velazquez MS, Russo ML, Perez E, Scorsetti AC. 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). Journal of Plant Protection Research. 2018;(57):6. doi: 10.1515/jppr-2017-0045

16. Greenfield M, Gomez-Jimenez MI, Ortiz V, Vega FE, Kramer M, Parsa S. Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control. 2016;95:40–8. doi: 10.1016/j.biocontrol.2016.01.002 27103778

17. Gange AC, Koricheva J, Currie AF, Jaber LR, Vidal S. Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol. 2019.

18. Klieber J, Reineke A. The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. Journal of Applied Entomology. 2016;140(8):580–9. doi: 10.1111/jen.12287

19. Jaber LR, Araj S-E. Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biological Control. 2018. doi: 10.1016/j.biocontrol.2016.09.001

20. Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño ÁM, García-Mina JM, del Campillo MC, Quesada-Moraga E. An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biological Control. 2017. doi: 10.1016/j.biocontrol.2017.01.012

21. McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR. Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl. 2016;62(1):1–17. doi: 10.1007/s10526-016-9769-5

22. Sadd BM, Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol. 2006;16(12):1206–10. doi: 10.1016/j.cub.2006.04.047 16782011

23. Vallet-Gely I, Lemaitre B, Boccard F. Bacterial strategies to overcome insect defences. Nat Rev Microbiol. 2008;6(4):302–13. doi: 10.1038/nrmicro1870 18327270

24. Cutler GC. Insects, insecticides and hormesis: evidence and considerations for study. Dose Response. 2013;11(2):154–77. Epub 2013/08/10. doi: 10.2203/dose-response.12-008.Cutler 23930099.

25. Ayyanath MM, Cutler GC, Scott-Dupree CD, Sibley PK. Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS One. 2013;8(9). doi: 10.1371/journal.pone.0074532 24040272.

26. Wang S, Qi Y, Desneux N, Shi X, Biondi A, Gao X. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. Journal of Pest Science. 2016;90(1):389–96. doi: 10.1007/s10340-016-0770-7

27. Cameron DD, Neal AL, van Wees SC, Ton J. Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci. 2013;18(10):539–45. doi: 10.1016/j.tplants.2013.06.004 23871659

28. Pozo MJ, Azcon-Aguilar C. Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol. 2007;10(4):393–8. doi: 10.1016/j.pbi.2007.05.004 17658291

29. R-Core-Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL

30. Hothorn T, Bretz F, Westfall P. Simultaneous Inference in General Parametric Models. Biometrical Journal. 2008;50(3):17.

31. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software. 2015;67(1):48.

32. Wickham H. Elegant Graphics for Data Analysis. Springer-Verlag New York. 2016.

33. Fox J, Weisberg S. An {R} Companion to Applied Regression. Second Edition Thousand Oaks CA: Sage URL: http://socservsocscimcmasterca/jfox/Books/Companion. 2011.

34. Rondot Y, Reineke A. Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biological Control. 2018;116:82–9. doi: 10.1016/j.biocontrol.2016.10.006

35. Pineda A, Zheng SJ, van Loon JJ, Dicke M. Rhizobacteria modify plant-aphid interactions: a case of induced systemic susceptibility. Plant Biologi (Stuttgard). 2012;14:83–90. doi: 10.1111/j.1438-8677.2011.00549.x 22348327

36. Zitlalpopoca-Hernandez G, Najera-Rincon MB, del-Val E, Alarcon A, Jackson T, Larsen J. Multitrophic interactions between maize mycorrhizas, the root feeding insect Phyllophaga vetula and the entomopathogenic fungus Beauveria bassiana. Applied Soil Ecology. 2017;115:38–43. doi: 10.1016/j.apsoil.2017.03.014

37. Castillo Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA. 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. 2014;9(8). doi: 10.1371/journal.pone.0103891 25093505

38. Clifton EH, Jaronski ST, Coates BS, Hodgson EW, Gassmann AJ. Effects of endophytic entomopathogenic fungi on soybean aphid and identification of Metarhizium isolates from agricultural fields. PLoS One. 2018;13(3):e0194815. doi: 10.1371/journal.pone.0194815 29566067; PubMed Central PMCID: PMC5864058.

39. García JE, Posadas JB, Perticari A, Lecuona RE. Metarhizium anisopliae (Metschnikoff) Sorokin Promotes Growth and Has Endophytic Activity in Tomato Plants. Advances in Biological Research. 2011.

40. Sasan RK, Bidochka MJ. The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot. 2012;99(1):101–7. doi: 10.3732/ajb.1100136 22174335

41. Dara SK, Dara SSR, Dara SS. Impact of Entomopathogenic Fungi on the Growth, Development, and Health of Cabbage Growing under Water Stress. American Journal of Plant Sciences. 2017;8(6):1224–33. doi: 10.4236/ajps.2017.86081

42. Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV. Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecology. 2018;34:43–9. doi: 10.1016/j.funeco.2018.04.002

43. Tall S, Meyling NV. Probiotics for Plants? Growth Promotion by the Entomopathogenic Fungus Beauveria bassiana Depends on Nutrient Availability. Microb Ecol. 2018. doi: 10.1007/s00248-018-1180-6 29594431

44. Afandhi A, Widjayanti T, Emi AAL, Tarno H, Afiyanti M, Handoko RNS. Endophytic fungi Beauveria bassiana Balsamo accelerates growth of common bean (Phaeseolus vulgaris L.). Chemical and Biological Technologies in Agriculture. 2019;6:11.

45. Behie SW, Zelisko PM, Bidochka MJ. Endophytic Insect-Parasitic Fungi Translocate NItrogen Directly from Insects to Plants. SCIENCE. 2012;336:3.

46. Jaber LR, Enkerli J. Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biological Control. 2016;103:187–95. doi: 10.1016/j.biocontrol.2016.09.008

47. Berns AE, Philipp H, Narres HD, Burauel P, Vereecken H, Tappe W. Effect of gamma-sterilization and autoclaving on soil organic matter structure as studied by solid state NMR, UV and fluorescence spectroscopy. European Journal of Soil Science. 2008;59(3):540–50. doi: 10.1111/j.1365-2389.2008.01016.x

48. Awmack CS, Leather SR. Host Plant Quality and Fecundity in Herbivorous Insects. Annu Rev Entomol. 2002;47:30.

49. Ríos Martínez AF, Costamagna AC. Effects of crowding and host plant quality on morph determination in the soybean aphid, Aphis glycines. Entomologia Experimentalis et Applicata. 2018;166(1):53–62. doi: 10.1111/eea.12637

50. Barribeau SM, Sok D, Gerardo NM. Aphid reproductive investment in response to mortality risks. BMC Evol Biol. 2010;10:11. doi: 10.1186/1471-2148-10-11

51. Cutler G, Guedes R. Occurrence and Significance of Insecticide-Induced Hormesis in Insects. In: Duke S, Kudsk P, Solomon K, editors. Pesticide dose: Effects on the environment and target and non-target organisms. 1249. ACS Symposium Series2017. p. 101–19.

52. Kunkel BN, Brooks DM. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology. 2002;5(4):325–31. doi: 10.1016/s1369-5266(02)00275-3 12179966

53. Haney CH, Wiesmann CL, Shapiro LR, Melnyk RA, O'Sullivan LR, Khorasani S, et al. Rhizosphere-associated Pseudomonas induce systemic resistance to herbivores at the cost of susceptibility to bacterial pathogens. Mol Ecol. 2018;27(8):1833–47. Epub 2017/11/01. doi: 10.1111/mec.14400 29087012.

54. McKinnon AC. Interactions between isolates of the fungus Beauveria bassiana and Zea mays: Lincoln University; 2017.

55. Russo ML, Pelizza SA, Cabello MN, Stenglein SA, Scorsetti AC. Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales). Biocontrol Science and Technology. 2015;25(4):475–80. doi: 10.1080/09583157.2014.982511

Článek vyšel v časopise


2019 Číslo 10