[en] Apple scab, caused by the hemibiotrophic fungus Venturia inaequalis, is currently the most common and damaging disease in apple orchards. Two strains of V. inaequalis (S755 and Rs552) with different sensitivities to azole fungicides and the bacterial metabolite fengycin were compared to determine the mechanisms responsible for these differences. Antifungal activity tests showed that Rs552 had reduced sensitivity to tebuconazole and tetraconazole, as well as to fengycin alone or in a binary mixture with other lipopeptides (iturin A, pumilacidin, lichenysin). S755 was highly sensitive to fengycin, whose activity was close to that of tebuconazole. Unlike fengycin, lipopeptides from the iturin family (mycosubtilin, iturin A) had similar activity on both strains, while those from the surfactin family (lichenysin, pumilacidin) were not active, except in binary mixtures with fengycin. The activity of lipopeptides varies according to their family and structure. Analyses to determine the difference in sensitivity to azoles (which target the CYP51 enzyme involved in the ergosterol biosynthesis pathway) showed that the reduced sensitivity in Rs552 is linked to (i) a constitutive increased expression of the Cyp51A gene caused by insertions in the upstream region and (ii) greater efflux by membrane pumps with the involvement of ABC transporters. Microscopic observations revealed that fengycin, known to interact with plasma membranes, induced morphological and cytological changes in cells from both strains. Sterol and phospholipid analyses showed a higher level of ergosta-7,22-dien-3-ol and a lower level of PI(C16:0/C18:1) in Rs552 compared with S755. These differences could therefore influence the composition of the plasma membrane and explain the differential sensitivity of the strains to fengycin. However, the similar antifungal activities of mycosubtilin and iturin A in the two strains indirectly indicate that sterols are probably not involved in the fengycin resistance mechanism. This leads to the conclusion that different mechanisms are responsible for the difference in susceptibility to azoles or fengycin in the strains studied.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Leconte, Aline ; Université de Liège - ULiège > TERRA Research Centre
Jacquin, Justine; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France
Duban, Matthieu; University of Lille, UMRt BioEcoAgro 1158-INRAE, Microbial Secondary Metabolites team, Charles Viollette Institute, Lille F-59000, France
Deweer, Caroline; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France
Trapet, Pauline; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France
Laruelle, Frédéric; Unité de Chimie Environnementale et Interactions sur le Vivant (EA 4492), Université Littoral Côte d'Opale, CEDEX CS 80699, Calais 62228, France
Farce, Amaury; Université Lille, Inserm, CHU Lille, U1286 - INFINITE - Institut de recherche translationnelle sur l'inflammation, Lille F-59000, France
Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution
Sahmer, Karin; Université Lille, IMT Lille Douai, Univ. Artois, JUNIA, ULR 4515 - LGCgE, Laboratoire de Génie Civil et geo-Environnement, Lille F-59000, France
Fiévet, Valentin; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France
Hoste, Alexis ; Université de Liège - ULiège > Département GxABT > Microbial technologies
Siah, Ali; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France
Lounès-Hadj Sahraoui, Anissa; Unité de Chimie Environnementale et Interactions sur le Vivant (EA 4492), Université Littoral Côte d'Opale, CEDEX CS 80699, Calais 62228, France
Jacques, Philippe ; Université de Liège - ULiège > TERRA Research Centre
Coutte, François; University of Lille, UMRt BioEcoAgro 1158-INRAE, Microbial Secondary Metabolites team, Charles Viollette Institute, Lille F-59000, France
Deleu, Magali ; Université de Liège - ULiège > TERRA Research Centre > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Muchembled, Jérôme; JUNIA, UMRt BioEcoAgro 1158-INRAE, Plant Secondary Metabolites Team, Charles Viollette Institute, Lille F-59000, France. Electronic address: jerome.muchembled@junia.com
This work was supported by the Hauts-de-France Regional Council (France), the CPER BiHauts Eco de France (France), with co-funding from Junia (France), the FNRS (Belgium) and the University of Li\u00E8ge (Belgium).This work was supported by the Hauts-de-France Regional Council (France), the CPER BiHauts Eco de France (France), with co-funding from Junia (France), the University of Li\u00E8ge (Belgium) (project PHENIX biocontrol, FEDER program 2021-2027) and the F.R.S-FNRS (Belgium) (PDR Project Surfasymm, grant T.0063.19).
Aranda, F.J., Teruel, J.A., Ortiz, A., Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochim. Biophys. Acta Biomembr. 1713 (2005), 51–56, 10.1016/j.bbamem.2005.05.003.
Aranda, F.J., Teruel, J.A., Ortiz, A., Recent advances on the interaction of glycolipid and lipopeptide biosurfactants with model and biological membranes. Curr. Opin. Colloid Interface Sci., 68, 2023, 101748, 10.1016/j.cocis.2023.101748.
Bailey, T.L., Elkan, C., 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36. PMID: 7584402.
Bechet, M., Guy-Castera, J., Guez, J.S., Chihib, N., Coucheney, F., Coutte, F., Fickers, P., Leclere, V., Wathelet, B., Jacques, P., Production of a novel mixture of mycosubtilins by mutant of Bacillus subtilis mutants. Bioresour. Technol. 145 (2013), 264–270, 10.1016/j.biortech.2013.03.123.
Bedart, C., Renault, N., Chavatte, P., Porcherie, A., Lachgar, A., Capron, M., Farce, A., SINAPs: a software tool for analysis and visualization of interaction networks of molecular dynamics simulations. J. Chem. Inf. Model. 62 (2022), 1425–1436, 10.1021/acs.jcim.1c00854.
Blosser, S.J., Cramer, R.A., SREBP-dependent triazole susceptibility in aspergillus fumigatus is mediated through direct transcriptional regulation of erg11A (cyp51A). Antimicrob. Agents Chemother. 56 (2012), 248–257, 10.1128/aac.05027-11.
Botcazon, C., Bergia, T., Lecouturier, D., Dupuis, C., Rochex, A., Acket, S., Nicot, P., Leclère, V., Sarazin, C., Rippa, S., Rhamnolipids and fengycins, very promising amphiphilic antifungal compounds from bacteria secretomes, act on Sclerotiniaceae fungi through different mechanisms. Front. Microbiol., 13, 2022, 977633, 10.3389/fmicb.2022.977633.
Bowen, J.K., Mesarich, C.H., Bus, V.G.M., Beresford, R.M., Plummer, K.M., Templeton, M.D., Venturia inaequalis: the causal agent of apple scab. Mol. Plant Pathol. 12 (2011), 105–122, 10.1111/j.1364-3703.2010.00656.x.
Buske, F.A., Bodén, M., Bauer, D.C., Bailey, T.L., Assigning roles to DNA regulatory motifs using comparative genomics. Bioinform 26 (2010), 860–866, 10.1093/bioinformatics/btq049.
Case, D.A., Ben-Shalom, I.Y., Brozell, S.R., Cerutti, D.S., Cheatham III, T.E., Cruzeiro, V.W.D., Darden, T.A., Duke, R.E., Ghoreishi, D., Giambasu, G., Giese, T., Gilson, M.K., Gohlke, H., Goetz, A.W., Greene, D., Harris, R., Homeyer, N., Huang, Y., Izadi, S., Kovalenko, A., Krasny, R., Kurtzman, T., Lee, T.S., LeGrand, S., Li, P., Lin, C., Liu, J., Luchko, T., Luo, R., Man, V., Mermelstein, D.J., Merz, K.M., Miao, Y., Monard, G., Nguyen, C., Nguyen, H., Onufriev, A., Pan, F., Qi, R., Roe, D.R., Roitberg, A., Sagui, C., Schott-Verdugo, S., Shen, J., Simmerling, C.L., Smith, J., Swails, J., Walker, R.C., Wang, J., Wei, H., Wilson, L., Wolf, R.M., Wu, X., Xiao, L., Xiong, Y., York, D.M., Kollman, P.A., 2019. AMBER 2019, University of California, San Francisco.
Cawoy, H., Mariutto, M., Henry, G., Fisher, C., Vasilyeva, N., Thonart, P., Dommes, J., Ongena, M., Plant defense stimulation by natural isolates of bacillus depends on efficient surfactin production. Mol. Plant Microbe Interact. 27 (2014), 87–100, 10.1094/MPMI-09-13-0262-R.
Chatzidimopoulos, M., Zambounis, A., Lioliopoulou, F., Vellios, E., Detection of Venturia inaequalis Isolates with Multiple Resistance in Greece. Microorganisms, 10, 2022, 2354, 10.3390/microorganisms10122354.
Cheval, P., Siah, A., Bomble, M., Popper, A.D., Reignault, P., Halama, P., Evolution of QoI resistance of the wheat pathogen Zymoseptoria tritici in northern France. Crop Prot. 92 (2017), 131–133, 10.1016/j.cropro.2016.10.017.
Chowdhury, S.P., Uhl, J., Grosch, R., Alquéres, S., Pittroff, S., Dietel, K., Schmitt-Kopplin, P., Borriss, R., Hartmann, A., Cyclic lipopeptides of bacillus amyloliquefaciens subsp. plantarum colonizing the lettuce rhizosphere enhance plant defense responses toward the bottom rot pathogen rhizoctonia solani. Mol. Plant Microbe Interact. 28 (2015), 984–995, 10.1094/MPMI-03-15-0066-R.
Chung, D., Barker, B.M., Carey, C.C., Merriman, B., Werner, E.R., Lechner, B.E., Dhingra, S., Cheng, C., Xu, W., Blosser, S.J., Morohashi, K., Mazurie, A., Mitchell, T.K., Haas, H., Mitchell, A.P., Cramer, R.A., ChIP-seq and in vivo transcriptome analyses of the aspergillus fumigatus SREBP SrbA reveals a new regulator of the fungal hypoxia response and virulence. PLoS Pathog., 10, 2014, e1004487, 10.1371/journal.ppat.1004487.
Colby, S.R., Calculating synergistic and antagonistic responses of herbicide combinations. Weeds 15 (1967), 20–22, 10.2307/4041058.
Cools, H.J., Fraaije, B.A., Update on mechanisms of azole resistance in Mycosphaerella graminicola and implications for future control. Pest Manag. Sci. 69 (2013), 150–155, 10.1002/ps.3348.
Cordero-Limon, L., Shaw, M.W., Passey, T.A., Robinson, J.D., Xu, X., Cross-resistance between myclobutanil and tebuconazole and the genetic basis of tebuconazole resistance in Venturia inaequalis. Pest Manag. Sci. 77 (2020), 844–850, 10.1002/ps.6088.
Das, D., Dey, S., Brewster, R.C., Choubey, S., Effect of transcription factor resource sharing on gene expression noise. PLoS Comput. Biol., 13(4), 2017, e1005491, 10.1371/journal.pcbi.1005491.
Deleu, M., Paquot, M., Nylander, T., Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. J. Colloid Interface Sci. 283 (2005), 358–365, 10.1016/j.jcis.2004.09.036.
Deleu, M., Paquot, M., Nylander, T., Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophys. J. 94 (2008), 2667–2679, 10.1529/biophysj.107.114090.
Desmyttere, H., Deweer, C., Muchembled, J., Sahmer, K., Jacquin, J., Coutte, F., Jacques, P., Antifungal activities of Bacillus subtilis lipopeptides against two Venturia inaequalis strains with different sensitivity to tebuconazole. Front. Microbiol., 10, 2019, 2327, 10.3389/fmicb.2019.02327.
Dussert, E., Tourret, M., Dupuis, C., Noblecourt, A., Behra-Miellet, J., Flahaut, C., Ravallec, R., Coutte, F., Evaluation of Antiradical and Antioxidant Activities of Lipopeptides Produced by Bacillus subtilis Strains. Front. Microbiol., 13, 2022, 914713, 10.3389/fmicb.2022.914713.
El-Bacha, T., Torres, A.G., 2016. Phospholipids: Physiology, in: Caballero, B., Finglas, P.M., Toldrá, F. (Eds.), Encyclopedia of Food and Health. Academic Press, Oxford, pp. 352-359. https://doi.org/10.1016/B978-0-12-384947-2.00540-7.
Ermakova, E., Zuev, Y., Effect of ergosterol on the fungal membrane properties. All-atom and coarse-grained molecular dynamics study. Chem. Phys. Lipids 209 (2017), 45–53, 10.1016/j.chemphyslip.2017.11.006.
Falardeau, J., Wise, C., Novitsky, L., Avis, T.J., Ecological and mechanistic insights into the direct and indirect antimicrobial properties of bacillus subtilis lipopeptides on plant pathogens. J. Chem. Ecol. 39 (2013), 869–878, 10.1007/s10886-013-0319-7.
Hagiwara, D., Miura, D., Shimizu, K., Paul, S., Ohba, A., Gonoi, T., Watanabe, A., Kamei, K., Shintani, T., Moye-Rowley, W.S., Kawamoto, S., Gomi, K., A novel transcription factor Zn2-Cys6 AtrR plays a key role in an azole resistance mechanism of Aspergillus fumigatus by coregulating cyp51A and cdr1B expressions. PLoS Pathog., 13, 2017, e1006096, 10.1371/journal.ppat.1006096.
Hamamoto, H., Hasegawa, K., Nakaune, R., Lee, Y.J., Makizumi, Y., Akutsu, K., Hibi, T., Tandem repeat of a transcriptional enhancer upstream of the sterol 14α-demethylase gene (CYP51) in penicillium digitatum. Appl. Environ. Microbiol. 66 (2000), 3421–3426, 10.1128/aem.66.8.3421-3426.2000.
Harayama, T., Riezman, H., Understanding the diversity of membrane lipid composition. Nat. Rev. Mol. Cell Biol. 19 (2018), 281–296, 10.1038/nrm.2017.138.
Hayashi, K., Schoonbeek, H.-J., De Waard, M.A., Bcmfs1, a novel major facilitator superfamily transporter from Botrytis cinerea, provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Appl. Environ. Microbiol. 68 (2002), 4996–5004, 10.1128/AEM.68.10.4996-5004.2002.
Hayashi, K., Schoonbeek, H., De Waard, M.A., Modulators of membrane drug transporters potentiate the activity of the DMI fungicide oxpoconazole against Botrytis cinerea. Pest. Manag. Sci. 59 (2003), 294–302, 10.1002/ps.637.
Hayashi, K., Schoonbeek, H., Waard, M., Expression of the ABC transporter BcatrD from Botrytis cinerea reduces sensitivity to sterol demethylation inhibitor fungicides. Pestic. Biochem. Phys. 73 (2002), 110–121, 10.1016/S0048-3575(02)00015-9.
He, H., Yang, M., Li, S., Zhang, G., Ding, Z., Zhang, L., Shi, G., Li, Y., Mechanisms and biotechnological applications of transcription factors. Syn. Syst. Biotechnol. 8:4 (2023), 565–577, 10.1016/j.synbio.2023.08.006.
Hoffmeister, M., Zito, R., Böhm, J., Stammler, G., Mutations in Cyp51 of Venturia inaequalis and their effects on DMI sensitivity. J. Plant Dis. Prot. 128 (2021), 1467–1478, 10.1007/s41348-021-00516-0.
Hulvey, J., Popko, J.T., Sang, H., Berg, A., Jung, G., Overexpression of ShCYP51B and ShatrD in sclerotinia homoeocarpa isolates exhibiting practical field resistance to a demethylation inhibitor fungicide. Appl. Environ. Microbiol. 78 (2012), 6674–6682, 10.1128/AEM.00417-12.
Jacques, P., 2011. Surfactin and Other Lipopeptides from Bacillus spp, in: Soberón-Chávez, G. (Ed.), Biosurfactants, Microbiology Monographs. Springer Berlin, Berlin, Heidelberg, pp. 57-91. https://doi.org/10.1007/978-3-642-14490-5_3.
Jones, G., Willett, P., Glen, R.C., Molecular recognition of receptor sites using a genetic algorithm with a description of desolvation. J. Mol. Biol. 245 (1995), 43–53, 10.1016/S0022-2836(95)80037-9.
Khajuria, Y.P., Akhoon, B.A., Kaul, S., Dhar, M.K., Secretomic insight into the pathophysiology of Venturia inaequalis: the Causative Agent of Scab, a Devastating Apple Tree Disease. Pathogens, 12(1), 2022, 66 https://doi: 10.3390/pathogens12010066.
Kretschmer, M., Leroch, M., Mosbach, A., Walker, A.-S., Fillinger, S., Mernke, D., Schoonbeek, H.-J., Pradier, J.-M., Leroux, P., De Waard, M.A., Hahn, M., Fungicide-Driven Evolution and Molecular Basis of Multidrug Resistance in Field Populations of the Grey Mould Fungus Botrytis cinerea. PLoS Pathog., 5, 2009, e1000696, 10.1371/journal.ppat.1000696.
Leconte, A., Tournant, L., Muchembled, J., Paucellier, J., Héquet, A., Deracinois, B., Deweer, C., Krier, F., Deleu, M., Oste, S., Jacques, P., Coutte, F., Assesment of lipopeptides mixtures produced by Bacillus subtilis as biocontrol products against apple scab (Venturia inaequalis). Microorganisms, 10, 2022, 1810, 10.3390/microorganisms10091810.
Leroux, P., Walker, A.-S., Multiple mechanisms account for resistance to sterol 14α-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest. Manag. Sci. 67 (2010), 44–59, 10.1002/ps.2028.
Leroux, P., Walker, A.-S., Activity of fungicides and modulators of membrane drug transporters in field strains of Botrytis cinerea displaying multidrug resistance. Eur. J. Plant Pathol. 135 (2013), 683–693, 10.1007/s10658-012-0105-3.
Lichtner, F.J., Jurick, W.M., Ayer, K.M., Gaskins, V.L., Villani, S.M., Cox, K.D., A genome resource for several north american venturia inaequalis isolates with multiple fungicide resistance phenotypes. Phytopathology 110 (2020), 544–546, 10.1094/PHYTO-06-19-0222-A.
Linde, J., Hortschansky, P., Fazius, E., Brakhage, A.A., Guthke, R., Haas, H., Regulatory interactions for iron homeostasis in Aspergillus fumigatus inferred by a Systems Biology approach. BMC Syst. Biol., 6, 2012, 6, 10.1186/1752-0509-6-6.
Liu, C.H., Chen, X., Liu, T.T., Lian, B., Gu, Y., Caer, V., Xue, Y.R., Wang, B.T., Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Appl. Microbiol. Biotechnol. 76 (2007), 459–466, 10.1007/s00253-007-1010-0.
Maget-Dana, R., Peypoux, F., Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87 (1994), 151–174, 10.1016/0300-483X(94)90159-7.
Maget-Dana, R., Thimon, L., Peypoux, F., Ptak, M., Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74 (1992), 1047–1051, 10.1016/0300-9084(92)90002-V.
Mantil, E., Buznytska, I., Daly, G., Lanoul, A., Avis, T.J., Role of lipid composition in the interaction and activity of the antimicrobial compound Fengycin with complex membrane models. J. Membr. Biol. 252 (2019), 627–638, 10.1007/s00232-019-00100-6.
Mantil, E., Crippin, T., Avis, T.J., Supported lipid bilayers using extracted microbial lipids: domain redistribution in the presence of fengycin. Colloids Surf. B: Biointerfaces 178 (2019), 94–102, 10.1016/j.colsurfb.2019.02.050.
Mantil, E., Crippin, T., Avis, T.J., Domain redistribution within ergosterol-containing model membranes in the presence of the antimicrobial compound fengycin. Biochim. Biophys. Acta Biomembr. 1861 (2019), 738–747, 10.1016/j.bbamem.2019.01.003.
Marmorstein, R., Carey, M., Ptashne, M., Harrison, S.C., DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356 (1992), 408–414, 10.1038/356408a0.
Mejri, S., Siah, A., Coutte, F., Magnin-Robert, M., Randoux, B., Tisserant, B., Krier, F., Jacques, P., Reignault, P., Halama, P., Biocontrol of the wheat pathogen Zymoseptoria tritici using cyclic lipopeptides from Bacillus subtilis. Environ. Sci. Pollut. Res. 25 (2018), 29822–29833, 10.1007/s11356-017-9241-9.
Moyne, A.L., Shelby, R., Cleveland, T.E., Tuzun, S., Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. J. Appl. Microbiol. 90 (2001), 622–629, 10.1046/j.1365-2672.2001.01290.x.
Mu, F., Chen, X., Fu, Z., Wang, X., Guo, J., Zhao, X., Zhang, B., Genome and transcriptome analysis to elucidate the biocontrol mechanism of Bacillus amyloliquefaciens XJ5 against Alternaria solani. Microorganisms, 11, 2023, 2055, 10.3390/microorganisms11082055.
Muchembled, J., Deweer, C., Sahmer, K., Halama, P., Antifungal activity of essential oils on two Venturia inaequalis strains with different sensitivities to tebuconazole. Environ. Sci. Pollut. Res. 25 (2018), 29921–29928, 10.1007/s11356-017-0507-z.
Nasir, M.N., Besson, F., Interactions of the antifungal mycosubtilin with ergosterol-containing interfacial monolayers. Biochim. Biophys. Acta Biomembr. 1818:5 (2012), 1302–1308, 10.1016/j.bbamem.2012.01.020.
Omrane, S., Sghyer, H., Audéon, C., Lanen, C., Duplaix, C., Walker, A.-S., Fillinger, S., Fungicide efflux and the MgMFS1 transporter contribute to the multidrug resistance phenotype in Zymoseptoria tritici field isolates. Environ. Microbiol. 17 (2015), 2805–2823, 10.1111/1462-2920.12781.
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J.L., Thonart, P., Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9:4 (2007), 1084–1090, 10.1111/j.1462-2920.2006.01202.x.
Pan, J., Hu, C., Yu, J.-H., Lipid biosynthesis as an antifungal target. J. Fungi, 4, 2018, 50, 10.3390/jof4020050.
Rahman, A., Uddin, W., Wenner, N.G., Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semi-purified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol. Plant Pathol. 16 (2015), 546–558, 10.1111/mpp.12209.
Richter, M., Rosselló-Móra, R., Oliver Glöckner, F., Peplies, J., JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32 (2016), 929–931, 10.1093/bioinformatics/btv681.
Rocafort, M., Srivastava, V., Bowen, J.K., Díaz-Moreno, S.M., Guo, Y., Bulone, V., Plummer, K.M., Sutherland, P.W., Anderson, M.A., Bradshaw, R.E., Mesarich, C.H., Cell Wall Carbohydrate Dynamics during the Differentiation of Infection Structures by the Apple Scab Fungus, Venturia inaequalis. Microbiol. Spectr., 11(3), 2023, e0421922, 10.1128/spectrum.04219-22.
Romero, D., de Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.-W., Arrebola, E., Cazorla, F.M., Kuipers, O.P., Paquot, M., Pérez-García, A., The Iturin and Fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis towards Podosphaera fusca. Mol. Plant Microbe Interact. 20 (2007), 430–440, 10.1094/MPMI-20-4-0430.
Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3 (2008), 1101–1108, 10.1038/nprot.2008.73.
Schnabel, G., Jones, A.L., 2001. The 14α-Demethylase (CYP51A1) Gene is Overexpressed in Venturia inaequalis Strains Resistant to Myclobutanil. Phytopathology 91, 102-110. https://doi.org/10.1094/PHYTO.2001.91.1.102.
Shirane, N., Takenaka, H., Ueda, K., Hashimoto, Y., Katoh, K., Ishii, H., Sterol analysis of DMI-resistant and sensitive strains of Venturia inaequalis. Phytochemistry 41 (1996), 1301–1308, 10.1016/0031-9422(95)00787-3.
Siah, A., Tisserant, B., El Chartouni, L., Duyme, F., Deweer, C., Roisin-Fichter, C., Sanssené, J., Durand, R., Reignault, P., Halama, P., 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 (2010), 980–990, 10.1016/j.funbio.2010.09.008.
Stammler, G., Cordero, J., Koch, A., Semar, M., Schlehuber, S., Role of the Y134F mutation in cyp51 and overexpression of cyp51 in the sensitivity response of Puccinia triticina to epoxiconazole. Crop Prot. 28 (2009), 891–897, 10.1016/j.cropro.2009.05.007.
Stephenson, S.L., 2010. The Kingdom fungi: the biology of mushrooms, molds, and lichens. Timber Press, Portland.
Sun, X., Xu, Q., Ruan, R., Zhang, T., Zhu, C., Li, H., PdMLE1, a specific and active transposon acts as a promoter and confers Penicillium digitatum with DMI resistance. Environ. Microbiol. Rep. 5 (2013), 135–142, 10.1111/1758-2229.12012.
Talebi, A., de Laat, V., Spotbeen, X., Dehairs, J., Rambow, F., Rogiers, A., Vanderhoydonc, F., Rizotto, L., Planque, M., Doglioni, G., Motamedi, S., Nittner, D., Roskams, T., Agostinis, P., Bechter, O., Boecxstaens, V., Garmyn, M., O'Farrell, M., Wagman, A., Kemble, G., Leucci, E., Fendt, S.-M., Marine, J.-C., Swinnen, J.V., Pharmacological induction of membrane lipid polyunsaturation sensitizes melanoma to ROS inducers and overcomes acquired resistance to targeted therapy. J. Exp. Clin. Cancer Res., 42, 2023, 92, 10.1186/s13046-023-02664-7.
Tan, S.T., Ramesh, T., Toh, X.R., Nguyen, L.N., Emerging roles of lysophospholipids in health and disease. Prog. Lipid Res., 80, 2020, 101068, 10.1016/j.plipres.2020.101068.
Todd, B.L., Stewart, E.V., Burg, J.S., Hughes, A.L., Espenshade, P.J., Sterol regulatory element binding protein is a principal regulator of anaerobic gene expression in fission yeast. Mol. Cell Biol. 26 (2006), 2817–2831, 10.1128/MCB.26.7.2817-2831.2006.
Van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 (2008), 112–124, 10.1038/nrm2330.
Vanittanakom, N., Loeffler, W., Koch, U., Jung, G., Fengycin-A novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J. Antibiot. 39 (1986), 888–901, 10.7164/antibiotics.39.888.
Vassaux, A., Rannou, M., Peers, S., Daboudet, T., Jacques, P., Coutte, F., Impact of the purification process on the spray-drying performance of three families of lipopeptide biosurfactants produced by Bacillus subtilis. Front. Bioeng. Biotechnol., 9, 2021, 815337, 10.3389/fbioe.2021.815337.
Vijaya Palani, P., Lalithakumari, D., Resistance of Venturia inaequalis to the sterol biosynthesis inhibiting fungicide, penconazole [1-(2-(2,4-dichlorophenyl) pentyl)-1H-1,2,4-triazole. Mycol. Res. 103 (1999), 1157–1164, 10.1017/S0953756299008321.
Villani, S.M., Biggs, A.R., Cooley, D.R., Raes, J.J., Cox, K.D., Prevalence of myclobutanil resistance and difenoconazole insensitivity in populations of Venturia inaequalis. Plant Dis. 99 (2015), 1526–1536, 10.1094/PDIS-01-15-0002-RE.
Villani, S.M., Hulvey, J., Hily, J.-M., Cox, K.D., Overexpression of the CYP51A1 gene and repeated elements are associated with differential sensitivity to DMI fungicides in Venturia inaequalis. Phytopathology 106 (2016), 562–571, 10.1094/PHYTO-10-15-0254-R.
Weete, J.D., 2012. Lipid Biochemistry of Fungi and Other Organisms. Springer New York.
Willger, S.D., Puttikamonkul, S., Kim, K.-H., Burritt, J.B., Grahl, N., Metzler, L.J., Barbuch, R., Bard, M., Lawrence, C.B., Jr, R.A.C., A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus. PLoS Pathog., 4, 2008, e1000200, 10.1371/journal.ppat.1000200.
Wise, C., Falardeau, J., Hagberg, I., Avis, T.J., Cellular Lipid Composition Affects Sensitivity of Plant Pathogens to Fengycin, an Antifungal Compound Produced by Bacillus subtilis Strain CU12. Phytopathology 104 (2014), 1036–1041, 10.1094/PHYTO-12-13-0336-R.
Xu, X.-M., Gao, L.-Q., Yang, J.-R., Are insensitivities of Venturia inaequalis to myclobutanil and fenbuconazole correlated. Crop Prot. 29 (2010), 183–189, 10.1016/j.cropro.2009.07.002.
Xue, J., Sun, L., Xu, H., Gu, Y., Lei, P., Bacillus atrophaeus NX-12 utilizes exosmotic glycerol from Fusarium oxysporum f. sp. cucumerinum for fengycin production. J. Agric. Food Chem. 71 (2023), 10565–10574, 10.1021/acs.jafc.3c01276.
Yaegashi, H., Hirayama, K., Akahira, T., Ito, T., Point mutation in CYP51A1 of Venturia inaequalis is associated with low sensitivity to sterol demethylation inhibitors. J. Gen. Plant Pathol. 86 (2020), 245–249, 10.1007/s10327-020-00924-4.
Yang, X., Zhang, L., Xiang, Y., Du, L., Huang, X., Liu, Y., Comparative transcriptome analysis of Sclerotinia sclerotiorum revealed its response mechanisms to the biological control agent, Bacillus amyloliquefaciens. Sci. Rep., 10, 2020, 12576, 10.1038/s41598-020-69434-9.
