Arroyave-Toro, J. J., Mosquera, S., and Villegas-Escobar, V. (2017). Biocontrol activity of Bacillus subtilis EA-CB0015 cells and lipopeptides against postharvest fungal pathogens. Biol. Control 114, 195–200. doi: 10.1016/j.biocontrol.2017. 08.014
Béchet, M., Castéra-Guy, J., Guez, J.-S., Chihib, N.-E., Coucheney, F., Coutte, F., 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
Bowen, J. K., Mesarich, C. H., Bus, V. G. M., Beresford, R. M., Plummer, K. M., and Templeton, M. D. (2011). V. inaequalis: the causal agent of apple scab. Mol. Plant. Pathol. 12, 105–122. doi: 10.1111/j.1364-3703.2010.00656.x
Brun, L., Didelot, F., and Parisi, L. (2008). Effects of apple cultivar susceptibility to V. inaequalis on scab epidemics in apple orchards. Crop Prot. 27, 1009–1019. doi: 10.1016/j.cropro.2007.12.009
Braun, P. G., and McRae, K. B. (1992). Composition of a population of V. inaequalis resistant to myclobutanil. Can. J. Plant Pathol. 14, 215–220. doi: 10.1080/07060669209500878
Buchoux, S., Lai-Kee-Him, J., Garnier, M., Tsan, P., Besson, F., Brisson, A., et al. (2008). Surfactin-triggered small vesicle formation of negatively charged membranes: a novel membrane-lysis mechanism. Biophys. J. 95, 3840–3849. doi: 10.1529/biophysj.107.128322
Carisse, O., and Jobin, T. (2012). Managing summer apple scab epidemics using leaf scab incidence threshold values for fungicide sprays. Crop Prot. 35, 36–40. doi: 10.1016/j.cropro.2011.12.014
Carisse, O., and Pelletier, J. R. (1994). Sensitivity distribution of V. inaequalis to fenarimol in Québec apple orchards. Phytoprotection 75, 35–43.
Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., and Mahillon, J. (2019). Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front. Microbiol. 10:302. doi: 10.3389/fmicb.2019.00302
Cochrane, S. A., and Vederas, J. C. (2014). Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Med. Res. Rev. 36, 4–31. doi: 10.1002/med.21321
Cools, H. J., Hawkins, N. J., and Fraaije, B. A. (2013). Constraints on the evolution of azole resistance in plant pathogenic fungi. Plant Pathol. 62, 36–42. doi: 10.1111/ppa.12128
Coutte, F., Leclère, V., Béchet, M., Guez, J.-S., Lecouturier, D., Chollet-Imbert, 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
Coutte, F., Lecouturier, D., Ait Yahia, S., Leclère, V., Béchet, M., and Jacques, P. (2010b). Production of surfactin and fengycin by Bacillus subtilis in a bubbleless membrane bioreactor. Appl. Microbiol. Biot. 87, 499–507. doi: 10.1007/s00253-010-2504-8
Deising, H. B., Reimann, S., and Pascholati, S. F. (2008). Mechanisms and significance of fungicide resistance. Braz. J. Microbiol. 39, 286–295. doi: 10.1590/S1517-838220080002000017
Deleu, M., Bouffioux, O., Razafindralambo, H., Paquot, M., Hbid, C., Thonart, P., et al. (2003). Interaction of surfactin with membranes: a computational approach. Langmuir 19, 3377–3385. doi: 10.1021/la026543z
Deleu, M., Paquot, M., and Nylander, T. (2005). Fengycin Interaction with lipid monolayers at the air–aqueous interface-implications for the effect of fengycin on biological membranes. J. Colloid Interface Sci. 283, 358–365. doi: 10.1016/j. jcis.2004.09.036
Deleu, M., Paquot, M., and Nylander, T. (2008). Effect of fengycin, a lipopeptide produced by bacillus subtilis, on model biomembrance. Biophys. J. 94, 2667–2679. doi: 10.1529/biophysj.107.114090
Deravel, J., Lemière, S., Coutte, F., Krier, F., Van Hese, N., Béchet, M., et al. (2014). Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl. Microbiol. Biot. 98, 6255–6264. doi: 10.1007/s00253-014-5663-1
Dunlap, C. A., Schisler, D. A., Price, N. P., and Vaughn, S. F. (2011). Cyclic lipopeptide profile of three Bacillus subtilis strains; antagonists of fusarium head blight. J. Microbiol. 49, 603–609. doi: 10.1007/s12275-011-1044-y
European Food Safety Authority [EFSA] (2013). Conclusion of the peer review of the pesticide risk assessment of confirmatory data submitted for the active substance copper (I), copper (II) variants namely copper hydroxide, copper oxychloride, tribasic copper sulphate, copper (I) oxide. Bordeaux mixture. EFSA J. 11, 3235–3275.
Falardeau, J., Wise, C., Novitsky, L., and Avis, T. J. (2013). Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J. Chem. Ecol. 39, 869–878. doi: 10.1007/s10886-013-0319-7
Farace, G., Fernandez, O., Jacquens, L., Coutte, F., Krier, F., Jacques, P., 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
Gao, L., Berrie, A., Yang, J., and Xu, X. (2009). Within-and between-orchard variability in the sensitivity of V. inaequalis to myclobutanil, a DMI fungicide, in the UK. Pest Manag. Sci. 65, 1241–1249. doi: 10.1002/ps.1816
Gonzalez-Jaramillo, L. M., Aranda, F. J., Teruel, J. A., Villegas-Escobar, V., and Ortiz, A. (2017). Antimycotic activity of fengycin C biosurfactant and its interaction with phosphatidylcholine model membranes. Colloid Surf. B 156, 114-22. doi: 10.1016/j.colsurfb.2017.05.021
Hamley, I. W., Dehsorkhi, A., Jauregi, P., Seitsonen, J., Ruokolainen, J., Coutte, F., et al. (2013). Self-assembly of three bacterially-derived bioactive lipopeptides. Soft Matter 9, 9572–9578.
Heerklotz, H., and Seelig, J. (2007). Leakage and lysis of lipid membranes induced by the lipopeptide surfactin. Eur. Biophys. J. 36, 305–314. doi: 10.1007/s00249-006-0091-5
Hildebrand, P. D., Lockhart, C. L., Newbery, R. J., and Ross, R. G. (1988). Resistance of V. inaequalis to bitertanol and other demethylation-inhibiting fungicides. Can. J. Plant Pathol. 10, 311–316. doi: 10.1080/07060668809501704
Inès, M., and Dhouha, G. (2015). Lipopeptide surfactants: production, recovery and pore forming capacity. Peptides 71, 100-112. doi: 10.1016/j.peptides.2015. 07.006
Jacques, P. (2011). “Surfactin and other lipopeptides from Bacillus spp.,” in Microbiology Monographs, vol 20, eds Edn, ed. G. Soberón-Chávez (Berlin: Springer).
Jauregi, P., Coutte, F., Catiau, L., Lecouturier, D., and Jacques, P. (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
Juhaniewicz-Dębińska, J., Tymecka, D., and Sęk, S. (2019). Diverse effect of cationic lipopeptide on negatively charged and neutral lipid bilayers supported on gold electrodes. Electrochim. Acta 298, 735-44.
Kim, P. I., Ryu, J., Kim, Y. H., and Chi, Y. T. (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.
Köller, W., Parker, D. M., and Reynolds, K. L. (1991). Baseline sensitivities of V. inaequalis to sterol demethylation inhibitors. Plant Dis. 75, 726–728. doi: 10.1094/PHYTO.1997.87.12.1272
Köller, W., Smith, F. D., Reynolds, J. K. L., Wilcox, W. F., and Burri, J. A. (1995). Seasonal changes of sensitivities to sterol demethylation inhibitors in V. inaequalis populations. Mycol. Res. 99, 689–692. doi: 10.1016/s0953-7562(09)80529-7
Krishnan, N., Velramar, B., and Velu, R. K. (2019). Investigation of antifungal activity of surfactin against mycotoxigenic phytopathogenic fungus fusarium moniliforme and its impact in seed germination and mycotoxicosis. Pestic. Biochem. Phys. 155, 101-7. doi: 10.1016/j.pestbp.2019.01.010
Kunz, S., Deising, H., and Mendgen, K. (1997). Acquisition of resistance to sterol demethylation inhibitors by populations of V. inaequalis. Phytopathology 87, 1272–1278. doi: 10.1094/PHYTO.1997.87.12.1272
Leclère, V., Bechet, M., Adam, A., Guez, J.-S., Wathelet, B., Ongena, M., et al. (2005). Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Appl. Environ. Microb. 71, 4577–4584. doi: 10.1128/aem.71.8.4577-4584.2005
Leroux, P., Bach, J., Debieu, D., Fillinger, S., Fritz, R., et al. (2008). “Mode of action of biosynthesis inhibitors and resistance phenomena in fungi,” in Modern Fungicides and Antifungal Compounds V, eds H. W. Dehne, H. B. Deising, U. Gisi, K. H. Kuck, P. E. Russell, and H. Lyr (Germany: Deutsche Phytomedizinische Gesellschaft e.V. Verlag), 45–51.
Liu, J., Hagberg, I., Novitsky, L., Hadj-Moussa, H., and Avis, T. J. (2014). Interaction of antimicrobial cyclic lipopeptides from Bacillus subtilis influences their effect on spore germination and membrane permeability in fungal plant pathogens. Fungal Biol. 118, 855–861. doi: 10.1016/j.funbio.2014.07.004
MacHardy, W. E. (1996). Apple Scab, Biology, Epidemiology, and Management. St. Paul, Minn, USA: APS.
Maget-Dana, R., Thimon, L., Peypoux, F., and Ptak, M. (1992). Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74, 1047–1051. doi: 10.1016/0300-9084(92) 90002-v
Maget-Dana, R., and Peypoux, F. (1994). Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87, 151–174. doi: 10.1016/0300-483x(94)90159-7
Mantil, E., Crippin, T., and Avis, T. J. (2019). Domain redistribution within ergosterol-containing model membranes in the presence of the antimicrobial compound fengycin. Biochim. Biophys. Acta 1861, 738-47. doi: 10.1016/j. bbamem.2019.01.003
Mejri, S., Siah, A., Coutte, F., Magnin-Robert, M., Randoux, B., Tisserant, B., et al. (2017). Biocontrol of the wheat pathogen zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis. Environ. Sci. Pollut. Res. 25, 29822–29833. doi: 10.1007/s11356-017-9241-9
Mihalache, G., Balaes, T., Gostin, I., Stefan, M., Coutte, F., and Krier, F. (2017). Lipopeptides produced by Bacillus subtilis as new biocontrol products against fusariosis in ornamental plants. Environ. Sci. Pollut. Res. 25, 29784–29793. doi: 10.1007/s11356-017-9162-7
Mondino, P., Casanova, L., Celio, A., Bentancur, O., Leoni, C., and Alaniz, S. (2015). Sensitivity of V. Inaequalis to trifloxystrobin and difenoconazole in uruguay. J. Phytopathol. 163, 1–10. doi: 10.1111/jph.12274
Muchembled, J., Deweer, C., Sahmer, K., and Halama, P. (2018). Antifungal activity of essential oils on two Venturia inaequalis strains with different sensitivities to tebuconazole. Environ. Sci. Pollut. Res. 25, 29921–29928. doi: 10.1007/s11356-017-0507-z
Muñoz, M., Rodríguez, A., Graciani, M., and Moyá, M. L. (2004). Conductometric, surface tension, and kinetic studies in mixed SDS-Tween 20 and SDS-SB3-12 micellar solutions. Langmuir 20, 10858–10867. doi: 10.1021/la048247n
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., 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
Ongena, M., and Jacques, P. (2008). Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16, 115–125. doi: 10.1016/j.tim.2007. 12.009
Parisi, L., Fouillet, V., Schouten, H. J., Groenwold, R., Laurens, F., Didelot, F., et al. (2004). Variability of the pathogenicity of Venturia inaequalis in Europe. Acta Hortic. 663, 107–113. doi: 10.17660/ActaHortic.2004.663.13
Park, G., Nam, J., Kim, J., Song, J., Kim, P. I, Min, H. J., et al. (2019). Structure and mechanism of surfactin peptide from Bacillus velezensis antagonistic to fungi plant pathogens. Bull. Korean Chem. Soc. 40, 704–709. doi: 10.1002/bkcs.11757
Parker, J., Warrilow, A., Price, C., Mullins, J., Kelly, D., and Kelly, S. (2014). Resistance to antifungals that target CYP51. J. Chem. Biol. 7, 143–161. doi: 10.1007/s12154-014-0121-1
Patel, H., Tscheka, C., Edwards, K., Karlsson, G., and Heerklotz, H. (2011). All-or-none membrane permeabilization by fengycin-type lipopeptides from Bacillus subtilis QST713. Biochim. Biophys. Acta 1808, 2000–2008. doi: 10.1016/j.bbamem.2011.04.008
Pérez-Garcia, A., Romero, D., and De Vicente, A. (2011). Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotech. 22, 187–193. doi: 10.1016/j.copbio.2010.12. 003
Pfeufer, E. E., and Ngugi, H. K. (2012). Orchard factors associated with resistance and cross resistance to sterol demethylation inhibitor fungicides in populations of Venturia inaequalis from Pennsylvania. Phytopathology 102, 272–282. doi: 10.1094/PHYTO-04-11-0117
Price, C. L., Parker, J. E., Warrilow, A. G. S., Kelly, D. E., and Kelly, S. L. (2015). Azole fungicides-understanding resistance mechanisms in agricultural fungal pathogens. Pest Manag. Sci. 71, 1054–1058. doi: 10.1002/ps.4029
R Core Team (2016). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at: https://www.R-project.org/
Razafindralambo, H., Dufour, S., Paquot, M., and Deleu, M. (2009). Thermodynamic studies of the binding interactions of surfactin analogues to lipid vesicles. J. Therm. Anal. Calorim. 95, 817–821. doi: 10.1007/s10973-008-9403-6
Ritz, C., and Streibig, J. C. (2008). Nonlinear Regression with R. New York, NY: Springer.
Romero, D., De Vicente, A., Olmos, J. L., Dávila, J. C., and Pérez-García, A. (2007a). Effect of lipopeptides of antagonistic strains of Bacillus subtilis on the morphology and ultrastructure of the cucurbit fungal pathogen Podosphaera fusca. J. Appl. Microbiol. 103, 969–976. doi: 10.1111/j.1365-2672.2007. 03323.x
Romero, D., De Vicente, A., Rakotoaly, R. H., Dufour, S. E., Veening, J.-W., Arrebola, E., et al. (2007b). 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
Schnabel, G., and Jones, A. L. (2001). The 14α-demethylase (CYP51A1) gene is overexpressed in V. inaequalis strains resistant to myclobutanil. Phytopathology 91, 102–110. doi: 10.1094/PHYTO.2001.91.1.102
Sharma, N., Gruszewski, H. A., Park, S. W., Holm, D. G., and Vivanco, J. M. (2004). Purification of an isoform of patatin with antimicrobial activity against Phytophthora infestans. Plant Physiol. Bioch. 42, 647–655. doi: 10.1016/j.plaphy. 2004.05.010
Shirane, N., Takenaka, H., Ueda, K., Hashimoto, Y., Katoh, K., and Ishii, H. (1996). Sterol analysis of DMI-resistant and –sensitive strains of V. inaequalis. Phytochemistry 41, 1301–1308. doi: 10.1016/0031-9422(95)00787-3
Stein, T. (2005). Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol. Microbiol. 56, 845–857. doi: 10.1111/j.1365-2958.2005.04587.x
Tao, Y., Bie, X. M., Lv, F. X., Zhao, H. Z., and Lu, Z. X. (2011). Antifungal activity and mechanism of fengycin in the presence and absence of commercial surfactin against Rhizopus stolonifer. J. Microbiol. 49, 146–150. doi: 10.1007/s12275-011-0171-9
Touré, Y., Ongena, M., Jacques, P., Guiro, A., and Thonart, P. (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
Vanittanakom, N., Loeffler, W., Koch, U., and Jung, G. (1986). Fengycin-a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. 39, 888–901. doi: 10.7164/antibiotics.39.888
Vijaya Palani, P., and Lalithakumari, D. (1999). Resistance of V. inaequalis to the sterol biosynthesis inhibiting fungicide, penconazole [1-(2-(2,4-dichlorophenyl) pentyl)-1H-1,2,4-triazole]. Mycol. Res. 103, 1157–1164. doi: 10.1017/s0953756299008321
Villani, S. M., Biggs, A. R., Cooley, D. R., Raes, J. J., and Cox, K. D. (2015). Prevalence of myclobutanil resistance and difenoconazole insensitivity in populations of V. inaequalis. Plant Dis. 99, 1526–1536. doi: 10.1094/PDIS-01-15-0002-RE
Villani, S. M., Hulvey, J., Hily, J. M., and Cox, K. D. (2016). Overexpression of the CYP51A1 gene and repeated elements are associated with differential sensitivity to DMI fungicides in Venturia inaequalis. Phytopathology 106, 562-71. doi: 10.1094/PHYTO-10-15-0254-R
Xu, X. M., Gao, L. Q., and Yang, J. R. (2010). Are insensitivities of Venturia inaequalis to myclobutanil and fenbuconazole correlated?. Crop Prot. 29, 183–189. doi: 10.1016/j.cropro.2009.07.002
Yoshida, Y., and Aoyama, Y. (1987). Interaction of azole antifungal agents with cytochrome P-45014DM purified from Saccharomyces cerevisiae microsomes. Biochem. Pharmacol. 36, 229–235. doi: 10.1016/0006-2952(87)90694-0