Skip to main content
Log in

Seed inoculation with endophytic fungal entomopathogens promotes plant growth and reduces crown and root rot (CRR) caused by Fusarium culmorum in wheat

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Fungal entomopathogens, Beauveria bassiana (NATURALIS) and Metarhizium brunneum (BIPESCO5), can promote the growth of wheat following their endophytic establishment within plants through seed treatment. Similar to endophytic B. bassiana which has already been reported as a disease antagonist by several previous studies, the present study demonstrates that M. brunneum can suppress disease pathogens following plant colonization as well.

An upsurge of research hints at the ability of entomopathogenic fungi, almost exclusively considered and used as insect pathogens, to endophytically colonize the internal tissues of a wide array of host plants and subsequently confer numerous benefits including enhancement of plant growth and suppression of disease pathogens. Such an ability has mainly been investigated for Beauveria bassiana. Fewer studies have demonstrated plant growth promotion by Metarhizium brunneum colonization, whereas no studies have reported on the potential of endophytic M. brunneum as a plant disease antagonist. The present study was, therefore, conducted to investigate whether seed treatment with B. bassiana (NATURALIS) and M. brunneum (BIPESCO5) could result in their endophytic establishment in wheat and promote plant growth. The study further examines the effect of the fungal strains as endophytes against Fusarium culmorum, one of the main causal agents of crown and root rot (CRR) in wheat. Both B. bassiana and M. brunneum were able to systemically colonize roots and shoots of wheat, and promote several plant growth parameters (shoot height, root length, and fresh root and shoot weights). Moreover, endophytic colonization of wheat with either fungal entomopathogen resulted in a significant reduction in disease incidence, development and severity. These results support the notion of the multiple ecological roles that could further be played by entomopathogenic fungi. Bearing such additional roles in mind while developing these fungi as microbial agents could improve the value of many commercially available mycoinsecticides.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

IPM:

Integrated pest management

CRR:

Crown and root rot

FRR:

Foot and root rot

FCR:

Fusarium crown rot

FHB:

Fusarium head blight

PDA:

Potato dextrose agar

CRD:

Completely randomized design

DPI:

Days post-inoculation

SAS:

Statistical analysis system

ZYMV:

Zucchini yellow mosaic virus

FCRR:

Fusarium crown and root rot

References

  • Akutse KS, Maniania NK, Fiaboe KKM, 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 Ecol 6:293–301

    Article  Google Scholar 

  • Akutse KS, Fiaboe KKM, Van den Berg J, Ekesi S, Maniania NK (2014) Effects of endophyte colonization of Vicia faba (Fabaceae) plants on the life-history of leafminer parasitoids Phaedrotoma scabriventris (Hymenoptera: Braconidae) and Diglyphus isaea (Hymenoptera: Eulophidae). PLoS One 9(10):e109965

    Article  Google Scholar 

  • Behie SW, Bidochka MJ (2013) Potential agricultural benefits through biotechnological manipulation of plant fungal associations. BioEssays 35:328–331

    Article  Google Scholar 

  • Behie SW, Bidochka MJ (2014) An additional branch of the soil nitrogen cycle: ubiquity of insect-derived nitrogen transfer to plants by endophytic insect pathogenic fungi. Appl Environ Microb 80:1553–1560

    Article  Google Scholar 

  • Benhamou N, 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. Physiol Mol Plant Pathol 58:133–146

    Article  CAS  Google Scholar 

  • Burgess LW, Backhouse D, Summerell BA, Swan LJ (2001) Crown rot of wheat. In: Summerell BA, Leslie JF, Backhouse D, Bryden WL, Burgess LW (eds) Fusarium: Paul E. Nelson memorial symposium. APS Press, St. Paul, pp 271–294

    Google Scholar 

  • Castillo-Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA (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

    Article  Google Scholar 

  • Cook RJ (1980) Fusarium foot rot of wheat and its control in the Pacific Northwest. Plant Dis 64:1061–1066

    Article  Google Scholar 

  • de Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256

    Article  Google Scholar 

  • Fernandez MR, Chen Y (2005) Pathogenicity of Fusarium species on different plant parts of spring wheat under controlled conditions. Plant Dis 89:164–169

    Article  Google Scholar 

  • Gao FK, Dai CC, Liu XZ (2010) Mechanisms of fungal endophytes in plant protection against pathogens. Afr J Microbiol Res 4:1346–1351

    Google Scholar 

  • Garcia JE, Posadas JB, Perticari A, Lecuona RE (2011) Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Adv biol Res 5:22–27

    Google Scholar 

  • Gathage JW, Lagat ZO, Fiaboe KKM, Akutse KS, Ekesi S, Maniania NK (2016) Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. Biocontrol 61:741–753

    Article  Google Scholar 

  • Golo PS, Gardner DR, Grilley MM, Takemoto JY, Krasnoff SB et al (2014) Production of destruxins from Metarhizium spp. fungi in artificial medium and in endophytically colonized cowpea plants. PLoS One 9(8):e104946

    Article  Google Scholar 

  • Gómez-Vidal S, Salinas J, Tena M, Lopez-Llorca LV (2009) Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis 30:2996–3005

    Article  Google Scholar 

  • 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 55:34–41

    Article  Google Scholar 

  • Hirano E, Koike M, Aiuchi D, Tani M (2008) Pre-inoculation of cucumber roots with Verticillium lecanii (Lecanicillium muscarium) induces resistance to powdery mildew. Res Bull Obihiro Univ 29:82–94

    CAS  Google Scholar 

  • Humber RA (1997) Fungi: identification. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, London, pp 153–185

    Chapter  Google Scholar 

  • Jaber LR (2015) Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. Biocontrol 60:103–112

    Article  Google Scholar 

  • Jaber LR, Alananbeh MK (2018) Fungal entomopathogens as endophytes reduce several species of Fusarium causing crown and root rot in sweet pepper (Capsicum annuum L.). Biol Control 126:117–126

    Article  Google Scholar 

  • Jaber LR, Araj SE (2018) 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). Biol Control 116:53–61

    Article  Google Scholar 

  • Jaber LR, Enkerli J (2016) Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biol Control 103:187–195

    Article  CAS  Google Scholar 

  • Jaber LR, Enkerli J (2017) Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Sci Technol 27:28–41

    Article  Google Scholar 

  • Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45

    Article  Google Scholar 

  • Jaber LR, Salem NM (2014) Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Sci Technol 24:1096–1109

    Article  Google Scholar 

  • Jaber LR, Araj SE, Qasem JR (2018) Compatibility of endophytic fungal entomopathogens with plant extracts for the management of sweetpotato whitefly Bemesia tabaci Gennadius (Homoptera: Aleyrodidae). Biol Control 117:164–171

    Article  Google Scholar 

  • Kempf H-J, Wolf G (1989) Erwinia herbicola as a biocontrol agent of Fusarium culmorum and Puccinia recondita f. sp. tritici on wheat. Phytopathology 79:990–994

    Article  Google Scholar 

  • Khan MR, Doohan FM (2009) Bacterium-mediated control of Fusarium head blight disease of wheat and barley and associated mycotoxin contamination of grain. Biol Control 48:42–47

    Article  Google Scholar 

  • Khan MR, Fischer S, Egan D, Doohan FM (2006) Biological control of Fusarium seedling blight disease of wheat and barley. Phytopathology 96:386–394

    Article  CAS  Google Scholar 

  • Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (2012a) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  CAS  Google Scholar 

  • Khan AL, Hamayun M, Khan SA, Kang SM, Shinwari ZK, Kamran M, Ur Rehman S, Kim JG, Lee IJ (2012b) Pure culture of Metarhizium anisopliae LHL07 reprograms soybean to higher growth and mitigates salt stress. World J Microbiol Biotechnol 28:1483–1494

    Article  CAS  Google Scholar 

  • Krell V, Unger S, Jakobs-Schoenwandt D, Patel AV (2018) Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecol 34:43–49

    Article  Google Scholar 

  • Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71

    Article  Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41

    Article  CAS  Google Scholar 

  • 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 89:53–60

    Article  Google Scholar 

  • Luongo L, Galli M, Corazza L, Meekes E, De Haas L, Van der Plas CL, Kohl J (2005) Potential of fungal antagonists for biocontrol of Fusarium spp. in wheat and maize through competition in crop debris. Biocontrol Sci Technol 15:229–242

    Article  Google Scholar 

  • Motallebi P, Alkadri D, Pisi A, Nipoti P, Tonti S, Niknam V, Hashemi M, Prodi A (2015) Pathogenicity and mycotoxin chemotypes of Iranian Fusarium culmorum isolates on durum wheat, and comparisons with Italian and Syrian isolates. Phytopathol Mediterr 54:437–445

    Google Scholar 

  • Ownley BH, Pereira RM, Klingeman WE, Quigley NB, Leckie BM (2004) Beauveria bassiana, a dual purpose biocontrol organism, with activity against insect pests and plant pathogens. In: Lartey RT, Caesar A (eds) Emerging concepts in plant health management. Research Signpost, Kerala, pp 256–269

    Google Scholar 

  • Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 3:267–270

    Article  Google Scholar 

  • Ownley B, Gwinn KD, Vega FE (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol 55:113–128

    Article  Google Scholar 

  • Petrini O, Fisher PJ (1987) Fungal endophytes in Salicornia perennis. Trans Br Mycol Soc 87:647–651

    Article  Google Scholar 

  • Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:749–758

    Article  Google Scholar 

  • Posadas JB, Comerio RM, Mini J, Nussenbaum AL, Lecuona RE (2012) A novel dodine-free selective medium based on the use of cetyl trimethyl ammonium bromide (CTAB) to isolate Beauveria bassiana, Metarhizium anisopliae 169 sensu lato and Paecilomyces lilacinus from soil. Mycologia 104:974–980

    Article  CAS  Google Scholar 

  • Ríos-Moreno A, Garrido-Jurado I, Resquín-Romero G, Arroyo-Manzanares N, Arce L, Quesada-Moraga E (2016) Destruxin A production by Metarhizium brunneum strains during transient endophytic colonization of Solanum tuberosum. Biocontrol Sci Technol 26:1574–1585

    Article  Google Scholar 

  • 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 25:475–480

    Article  Google Scholar 

  • SAS Institute Inc. (2010) SAS OnlineDoc® version 9.1.3, Cary, NC, USA

  • Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107

    Article  Google Scholar 

  • Sasan RK, Bidochka MJ (2013) Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can J Plant Pathol 35:288–293

    Article  CAS  Google Scholar 

  • Scherm B, Balmas V, Spanu F, Pani G, Delogu G, Pasquali M, Migheli Q (2013) Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Mol Plant Pathol 14:323–341

    Article  CAS  Google Scholar 

  • Schulz B, Boyle C (2005) The endophyte continuum. Mycol Res 109:661–686

    Article  Google Scholar 

  • Schulz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227

    Google Scholar 

  • Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531

    Article  CAS  Google Scholar 

  • Strasser H, Forer A, Schinner F (1996) Development of media for the selective isolation and maintenance of virulence of Beauveria brongniartii. In: Jackson TA, Glare TR (eds) Microbial control of soil dwelling pests. AgResearch, Lincoln, pp 125–130

    Google Scholar 

  • Sun BT, Akutse KS, Xia XF, Chen JH, Ai X, Tang Y, Wang Q, Feng BW, Goettel MS, You MS (2018) Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella. Planta (in press)

  • Tall S, Meyling NV (2018) Probiotics for plants? Growth promotion by the entomopathogenic fungus Beauveria bassiana depends on nutrient availability. Microb Ecol 28:1–7

    Google Scholar 

  • Vega FE (2008) Insect pathology and fungal endophytes. J Invertebr Pathol 98:277–279

    Article  Google Scholar 

  • Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzon A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159

    Article  Google Scholar 

  • Verbruggen E, Heijden MG, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109

    Article  Google Scholar 

  • Wagacha JM, Muthomi JW (2007) Fusarium culmorum: infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Prot 26:877–885

    Article  CAS  Google Scholar 

  • Wilson D (1995) Endophyte—the evolution of a term, and clarification of its use and definition. Oikos 73:274–276

    Article  Google Scholar 

  • Yan JF, Broughton SJ, Yang SL, Gange AC (2015) Do endophytic fungi grow through their hosts systemically? Fungal Ecol 13:53–59

    Article  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a research grant (no. 1632) from The University of Jordan provided to the author. The author thanks Dr. Hermann Strasser (Institute of Microbiology, University of Innsbruck, Austria) for providing M. brunneum strain BIPESCO5. Comments of the Editor-in-Chief and four anonymous reviewers are appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lara R. Jaber.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaber, L.R. Seed inoculation with endophytic fungal entomopathogens promotes plant growth and reduces crown and root rot (CRR) caused by Fusarium culmorum in wheat. Planta 248, 1525–1535 (2018). https://doi.org/10.1007/s00425-018-2991-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2991-x

Keywords

Navigation