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Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis

  • Chemistry, Activity and Impact of Plant Biocontrol products
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Abstract

Innovation toward ecofriendly plant protection products compatible with sustainable agriculture and healthy food is today strongly encouraged. Here, we assessed the biocontrol activity of three cyclic lipopeptides from Bacillus subtilis (mycosubtilin, M; surfactin, S; fengycin, F) and two mixtures (M + S and M + S + F) on wheat against Zymoseptoria tritici, the main pathogen on this crop. Foliar application of these biomolecules at a 100-mg L−1 concentration on the wheat cultivars Dinosor and Alixan, 2 days before fungal inoculation, provided significant reductions of disease severity. The best protection levels were recorded with the M-containing formulations (up to 82% disease reduction with M + S on Dinosor), while S and F treatments resulted in lower but significant disease reductions. In vitro and in planta investigations revealed that M-based formulations inhibit fungal growth, with half-maximal inhibitory concentrations of 1.4 mg L−1 for both M and M + S and 4.5 mg L−1 for M + S + F, thus revealing that the observed efficacy of these products may rely mainly on antifungal property. By contrast, S and F had no direct activity on the pathogen, hence suggesting that these lipopeptides act on wheat against Z. tritici as resistance inducers rather than as biofungicides. This study highlighted the efficacy of several lipopeptides from B. subtilis to biocontrol Z. tritici through likely distinct and biomolecule-dependent modes of action.

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References

  • Béchet M, Castéra-Guy J, Guez J-S et al (2013) Production of a novel mixture of mycosubtilins by mutants of Bacillus subtilis. Bioresour Technol 145:264–270. doi:10.1016/j.biortech.2013.03.123

    Article  CAS  Google Scholar 

  • Chandler S, Van Hese N, Coutte F et al (2015) Role of cyclic lipopeptides produced by Bacillus subtilis in mounting induced immunity in rice (Oryza sativa L.) Physiol Mol Plant Path 91:20–30. doi:10.1016/j.pmpp.2015.05.010

    Article  CAS  Google Scholar 

  • Chen XH, Koumoutsi A, Scholz R et al (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140:27–37. doi:10.1016/j.jbiotec.2008.10.011

    Article  CAS  Google Scholar 

  • Cheval P, Siah A, Bomble M et al (2017) Evolution of QoI resistance of the wheat pathogen Zymoseptoria tritici in Northern France. Crop Prot 92:131–133. doi:10.1016/j.cropro.2016.10.017

    Article  CAS  Google Scholar 

  • Coutte F, Leclère V, Béchet M et al (2010a) Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J Appl Microbiol 109:480–491. doi:10.1111/j.1365-2672.2010.04683.x

    Article  CAS  Google Scholar 

  • Coutte F, Lecouturier D, Ait Yahia S et al (2010b) Production of surfactin and fengycin by Bacillus subtilis in a bubbleless membrane bioreactor. Appl Microbiol Biotechnol 87:499–507. doi:10.1007/s00253-010-2504-8

    Article  CAS  Google Scholar 

  • Coutte F, Lecouturier D, Leclère V et al (2013) New integrated bioprocess for the continuous production, extraction and purification of lipopeptides produced by Bacillus subtilis in membrane bioreactor. Process Biochem 48:25–32. doi:10.1016/j.procbio.2012.10.005

    Article  CAS  Google Scholar 

  • Cowger C, Hoffer ME, Mundt CC (2000) Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathol 49:445–451. doi:10.1046/j.1365-3059.2000.00472.x

    Article  Google Scholar 

  • Dean R, Van Kan JA, Pretorius ZA et al (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. doi:10.1111/j.1364-3703.2011.00783.x

    Article  Google Scholar 

  • Deravel J, Lemière S, Coutte F et al (2014) Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl Microbiol Biotechnol 98:6255–6264. doi:10.1007/s00253-014-5663-1

    Article  CAS  Google Scholar 

  • El Chartouni L, Tisserant B, Siah A et al (2011) Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia 103:764–774. doi:10.3852/10-184

    Article  Google Scholar 

  • Farace G, Fernandez O, Jacquens L et al (2015) Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol Plant Pathol 16:177–187. doi:10.1111/mpp.12170

    Article  CAS  Google Scholar 

  • Guo Q, Dong W, Li S et al (2014) Fengycin produced by Bacillus subtilis NCD-2 plays a major role in biocontrol of cotton seedling damping-off disease. Microbiol Res 169:533–540. doi:10.1016/j.micres.2013.12.001

    Article  CAS  Google Scholar 

  • Hamley IW, Dehsorkhi A, Jauregi P et al (2013) Self-assembly of three bacterially-derived bioactive lipopeptides. Soft Matter 9:9572–9578

    Article  CAS  Google Scholar 

  • Han Q, Wu F, Wang X et al (2015) The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity. Environ Microbiol 17:1166–1188. doi:10.1111/1462-2920.12538

    Article  CAS  Google Scholar 

  • Henry G, Deleu M, Jourdan E et al (2011) The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell Microbio 13:1824–1837. doi:10.1111/j.1462-5822.2011.01664.x

    Article  CAS  Google Scholar 

  • Jacques P (2011) Surfactin and other lipopeptides from Bacillus spp. In: Soberon-Chavez G (ed) Biosurfactants microbiology monographs, vol 20. Springer-Verlag, Heidelberg, pp 57–91

    Google Scholar 

  • Jauregi P, Coutte F, Catiau L et al (2013) Micelle size characterization of lipopeptides produced by B. subtilis and their recovery by the two-step ultrafiltration process. Sep Purif Technol 104:175–182. doi:10.1016/j.seppur.2012.11.017

    Article  CAS  Google Scholar 

  • Jørgensen LN, Hovmøller MS, Hansen JG et al (2014) IPM strategies and their dilemmas including an introduction to www.eurowheat.org. J Integr Agric 13:265–281. doi:10.1016/S2095-3119(13)60646-2

    Article  Google Scholar 

  • Jourdan E, Henry G, Duby F et al (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant-Microbe Interact 22:456–468. doi:10.1094/MPMI-22-4-0456

    Article  CAS  Google Scholar 

  • Kema GHJ, Yu D, Rijkenberg FHJ et al (1996) Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777–786. doi:10.1094/Phyto-86-777

    Article  Google Scholar 

  • Kema GHJ, Van der Lee TAJ, Mendes O et al (2008) Large-scale gene discovery in the septoria tritici blotch fungus Mycosphaerella graminicola with a focus on in planta expression. Mol Plant-Microbe Interact 21:1249–1260. doi:10.1094/MPMI-21-9-1249

    Article  CAS  Google Scholar 

  • Kim PI, Ryu J, Kim YH et al (2010) Production of biosurfactant lipopeptides iturin A, fengycin and surfactin a from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20:138–145. doi:10.4014/jmb.0905.05007

    Article  CAS  Google Scholar 

  • Leclère V, Béchet M, Adam A et al (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl Environ Microbiol 71:4577–4584. doi:10.1128/AEM.71.8.4577-4584.2005

    Article  CAS  Google Scholar 

  • Lovell D, Hunter T, Powers S et al (2004) Effect of temperature on latent period of septoria leaf blotch on winter wheat under outdoor conditions. Plant Pathol 53:170–181. doi:10.1111/j.0032-0862.2004.00983.x

    Article  Google Scholar 

  • Olson S (2015) An analysis of the biopesticide market now and where it is going. Outlooks on Pest Management 26:203–206. doi:10.1564/v26_oct_04

    Article  Google Scholar 

  • Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. doi:10.1016/j.tim.2007.12.009

    Article  CAS  Google Scholar 

  • Ongena M, Jourdan E, Adam A et al (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090. doi:10.1111/j.1462-2920.2006.01202.x

    Article  CAS  Google Scholar 

  • Perez-Montaño F, Alías-Villegas C, Bellogín RA et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336. doi:10.1016/j.micres.2013.09.011

    Article  Google Scholar 

  • Ponomarenko A, Goodwin SB, Kema GH (2011) Septoria tritici blotch (STB) of wheat. Plant Health Instructor. doi:10.1094/PHI-I-2011-0407-01

  • Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. doi:10.1111/j.1574-6976.2010.00221.x

    Article  CAS  Google Scholar 

  • Ravensberg W (2015) Crop protection in 2030: towards a natural, efficient, safe and sustainable approach. International Symposium Swansea University 7–9 September 2015

  • Romero D, de Vicente A, Rakotoaly RH et al (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant-Microbe Interact 20:430–440. doi:10.1094/MPMI-20-4-0430

    Article  CAS  Google Scholar 

  • Rückert C, Blom J, Chen X et al (2011) Genome sequence of B. amyloliquefaciens type strain DSM7(T) reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 20:78–85. doi:10.1016/j.jbiotec.2011.01.006

    Article  CAS  Google Scholar 

  • Siah A, Deweer C, Duyme F et al (2010a) Correlation of in planta endo-beta-1,4-xylanase activity with the necrotrophic phase of the hemibiotrophic fungus Mycosphaerella graminicola. Plant Pathol 59:661–670. doi:10.1111/j.1365-3059.2010.02303.x

    Article  Google Scholar 

  • Siah A, Tisserant B, El Chartouni L et al (2010b) Mating type idiomorphs from a French population of the wheat pathogen Mycosphaerella graminicola: widespread equal distribution and low but distinct levels of molecular polymorphism. Fungal Biol 114:980–990. doi:10.1016/j.funbio.2010.09.008

    Article  CAS  Google Scholar 

  • Siah A, Deweer C, Morand E et al (2010c) Azoxystrobin resistance of French Mycosphaerella graminicola strains assessed by four in vitro bioassays and by screening of G143A substitution. Crop Prot 29:737–743. doi:10.1016/j.cropro.2010.02.012

    Article  CAS  Google Scholar 

  • Siah A, Reignault P, Halama P (2013) Genetic diversity of Mycosphaerella graminicola isolates from a single field. Commun Agric Appl Biol Sci 78:437–442

    CAS  Google Scholar 

  • Siah A, Randoux B, Magnin-Robert M, et al (2017) Natural agents inducing plant resistance against diseases. In Natural Antimicrobial Agents, Sustainable Development and Biodiversity series. Edited by Mérillon J.M. and Rivière C. Springer (in press).

  • Stock D, Holloway PJ (1993) Possible mechanisms for surfactant induced foliar uptake of agrochemicals. Pest Manag Sci 38:165–177. doi:10.1002/ps.2780380211

    Article  CAS  Google Scholar 

  • Strieker M, Tanović A, Marahiel MA (2010) Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol 20:234–240. doi:10.1016/j.sbi.2010.01.0

    Article  CAS  Google Scholar 

  • Torriani SFF, Melichar JPE, Mills C et al (2015) Zymoseptoria tritici: a major threat to wheat production, integrated approaches to control. Fungal Genet Biol 79:8–12. doi:10.1016/j.fgb.2015.04.010

    Article  Google Scholar 

  • Touré Y, Ongena M, Jacques P et al (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96:1151–1160. doi:10.1111/j.1365-2672.2004.02252.x

    Article  CAS  Google Scholar 

  • Xun-Chao C, Hui L, Ya-Rong X et al (2013) Study of endophytic Bacillus amyloliquefaciens CC09 and its antifungal cyclic lipopeptides. J Appl Bio Biotechnol. doi:10.7324/JABB.2013.1101

  • Yamamoto S, Shiraishi S, Suzuki S (2015) Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S13-3 responsible for the plant defence response in strawberry against Colletotrichum gloeosporioides? Lett Appl Microbiol 60:325–336. doi:10.1111/lam.12382

    Article  CAS  Google Scholar 

  • Yu GY, Sinclair JB, Hartman GL et al (2002) Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biol Biochem 34:955–963. doi:10.1016/S0038-0717(02)00027-5

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Corentin Duthoo for his technical help during this study and Dr. Gabrielle Chataigné for the HPLC-MS analysis. This research was conducted in the framework of the projects NewBioPest supported by the Hauts-de-France council (France) and both BioProtect and BioScreen supported by INTERREG V SMARTBIOCONTROL (European Union).

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Authors and Affiliations

  1. Institut Charles Viollette (EA 7394), ISA, SFR Condorcet FR CNRS 3417, 48 bd Vauban, BP 41290, 59014, Lille, France

    Samara Mejri, Ali Siah & Patrice Halama

  2. Institut Charles Viollette (EA 7394), Université de Lille, SFR Condorcet FR CNRS 3417, Avenue Paul Langevin, 59655, Villeneuve d’Ascq Cedex, France

    François Coutte, François Krier & Philippe Jacques

  3. UCEIV-EA 4492, Université du Littoral Côte d’Opale, SFR Condorcet FR CNRS 3417, CS 80699, 62228, Calais Cedex, France

    Maryline Magnin-Robert, Béatrice Randoux, Benoit Tisserant & Philippe Reignault

  4. Microbial Processes and Interactions, TERRA Research Centre, Gembloux Agro-Bio Tech, University of Liege, Passage des Déportés, 25030, Gembloux, Belgium

    Philippe Jacques

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  1. Samara Mejri
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  2. Ali Siah
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  3. François Coutte
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Correspondence to Patrice Halama.

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Mejri, S., Siah, A., Coutte, F. et al. Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis . Environ Sci Pollut Res 25, 29822–29833 (2018). https://doi.org/10.1007/s11356-017-9241-9

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