Insights into the Molecular Basis of Biocontrol of Brassica Pathogens by Bacillus Amyloliquefaciens UCMB5113 Lipopeptides

Overview

Journal Ann Bot

Publisher Oxford University Press

Specialty Biology

Date 2017 Sep 30

PMID 28961818

Citations 10

Authors

Shashidar Asari

Marc Ongena

Delphine Debois

Edwin De Pauw

Kunling Chen

Sarosh Bejai

Johan Meijer

Affiliations

Soon will be listed here.

Abstract

Background And Aims: Certain micro-organisms can improve plant protection against pathogens. The protective effect may be direct, e.g. due to antibiotic compounds, or indirect, by priming of plant defence as induced systemic resistance (ISR). The plant growth-promoting rhizobacterium Bacillus amyloliquefaciens UCMB5113 shows potential for disease management of oilseed rape. To investigate the mode of action of this protection, especially in relation to jasmonic acid-dependent ISR, Bacillus UCMB5113 was tested with Arabidopsis thaliana mutants and several important fungal pathogens of Brassica species.

Methods: Secreted lipopeptide fractions from Bacillus UCMB5113, together with synthetic peptide mimics, were evaluated for their effects on fungal phytopathogens and A. thaliana . The structures of secreted lipopeptides were analysed using mass spectrometry. Plant mutants and reporter lines were used to identify signalling steps involved in disease suppression by lipopeptides.

Key Results: In plate tests Bacillus UCMB5113 and lipopeptide extracts suppressed growth of several fungal pathogens infecting Brassica plants. Separation of secreted lipopeptides using reversed-phase high-performance liquid chromatography revealed several fractions that inhibited fungal growth. Analysis by mass spectrometry identified the most potent compounds as novel linear forms of antifungal fengycins, with synthetic peptide mimics confirming the biological activity. Application of the lipopeptide extracts on Arabidopsis roots provided systemic protection against Alternaria brassicicola on leaves. Arabidopsis signalling mutants and PDF1.2 and VSP2 promoter-driven GUS lines indicated that the lipopeptide fraction involved jasmonic-acid-dependent host responses for suppression of fungal growth indicative of ISR.

Conclusions: The ability of Bacillus UCMB5113 to counteract pathogens using both antagonistic lipopeptides and through ISR provides a promising tool for sustainable crop production.

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References

Eeman M, Pegado L, Dufrene Y, Paquot M, Deleu M . Influence of environmental conditions on the interfacial organisation of fengycin, a bioactive lipopeptide produced by Bacillus subtilis. J Colloid Interface Sci. 2008; 329(2):253-64. DOI: 10.1016/j.jcis.2008.10.017. View

Conrath U, Beckers G, Langenbach C, Jaskiewicz M . Priming for enhanced defense. Annu Rev Phytopathol. 2015; 53:97-119. DOI: 10.1146/annurev-phyto-080614-120132. View

Tran H, Ficke A, Asiimwe T, Hofte M, Raaijmakers J . Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol. 2007; 175(4):731-742. DOI: 10.1111/j.1469-8137.2007.02138.x. View

Ongena M, Jacques P . Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 2008; 16(3):115-25. DOI: 10.1016/j.tim.2007.12.009. View

Reva O, Dixelius C, Meijer J, Priest F . Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol. 2009; 48(2):249-59. DOI: 10.1016/j.femsec.2004.02.003. View

Aleti G, Sessitsch A, Brader G . Genome mining: Prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Comput Struct Biotechnol J. 2015; 13:192-203. PMC: 4397504. DOI: 10.1016/j.csbj.2015.03.003. View

Durrant W, Dong X . Systemic acquired resistance. Annu Rev Phytopathol. 2004; 42:185-209. DOI: 10.1146/annurev.phyto.42.040803.140421. View

Souto G, Correa O, Montecchia M, Kerber N, Pucheu N, Bachur M . Genetic and functional characterization of a Bacillus sp. strain excreting surfactin and antifungal metabolites partially identified as iturin-like compounds. J Appl Microbiol. 2004; 97(6):1247-56. DOI: 10.1111/j.1365-2672.2004.02408.x. View

van der Ent S, Verhagen B, van Doorn R, Bakker D, Verlaan M, Pel M . MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol. 2008; 146(3):1293-304. PMC: 2259080. DOI: 10.1104/pp.107.113829. View

10.

Chen X, Koumoutsi A, Scholz R, Borriss R . More than anticipated - production of antibiotics and other secondary metabolites by Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol. 2008; 16(1-2):14-24. DOI: 10.1159/000142891. View

11.

Malfanova N, Franzil L, Lugtenberg B, Chebotar V, Ongena M . Cyclic lipopeptide profile of the plant-beneficial endophytic bacterium Bacillus subtilis HC8. Arch Microbiol. 2012; 194(11):893-9. PMC: 3477485. DOI: 10.1007/s00203-012-0823-0. View

12.

van Loon L, Bakker P, Pieterse C . Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol. 2004; 36:453-83. DOI: 10.1146/annurev.phyto.36.1.453. View

13.

Adie B, Perez-Perez J, Perez-Perez M, Godoy M, Sanchez-Serrano J, Schmelz E . ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell. 2007; 19(5):1665-81. PMC: 1913739. DOI: 10.1105/tpc.106.048041. View

14.

Adam M, Heuer H, Hallmann J . Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS One. 2014; 9(2):e90402. PMC: 3938715. DOI: 10.1371/journal.pone.0090402. View

15.

Strieker M, Tanovic A, Marahiel M . Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol. 2010; 20(2):234-40. DOI: 10.1016/j.sbi.2010.01.009. View

16.

Danielsson J, Reva O, Meijer J . Protection of oilseed rape (Brassica napus) toward fungal pathogens by strains of plant-associated Bacillus amyloliquefaciens. Microb Ecol. 2006; 54(1):134-40. DOI: 10.1007/s00248-006-9181-2. View

17.

Shigenaga A, Argueso C . No hormone to rule them all: Interactions of plant hormones during the responses of plants to pathogens. Semin Cell Dev Biol. 2016; 56:174-189. DOI: 10.1016/j.semcdb.2016.06.005. View

18.

Bhattacharyya P, Jha D . Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol. 2012; 28(4):1327-50. DOI: 10.1007/s11274-011-0979-9. View

19.

Niazi A, Manzoor S, Asari S, Bejai S, Meijer J, Bongcam-Rudloff E . Genome analysis of Bacillus amyloliquefaciens Subsp. plantarum UCMB5113: a rhizobacterium that improves plant growth and stress management. PLoS One. 2014; 9(8):e104651. PMC: 4138018. DOI: 10.1371/journal.pone.0104651. View

20.

Cochrane S, Vederas J . Lipopeptides from Bacillus and Paenibacillus spp.: A Gold Mine of Antibiotic Candidates. Med Res Rev. 2014; 36(1):4-31. DOI: 10.1002/med.21321. View