Snf2 controls pulcherriminic acid biosynthesis and antifungal activity of the biocontrol yeast Metschnikowia pulcherrima
Open accessAbstract
Summary: Metschnikowia pulcherrima synthesises the pigment pulcherrimin, from cyclodileucine (cyclo(Leu‐Leu)) as a precursor, and exhibits strong antifungal activity against notorious plant pathogenic fungi. This yeast therefore has great potential for biocontrol applications against fungal diseases; particularly in the phyllosphere where this species is frequently found. To elucidate the molecular basis of the antifungal activity of M. pulcherrima, we compared a wild‐type strain with a spontaneously occurring, pigmentless, weakly antagonistic mutant derivative. Whole genome sequencing of the wild‐type and mutant strains identified a point mutation that creates a premature stop codon in the transcriptional regulator gene SNF2 in the mutant. Complementation of the mutant strain with the wild‐type SNF2 gene restored pigmentation and recovered the strong antifungal activity. Mass spectrometry (UPLC HR HESI‐MS) proved the presence of the pulcherrimin precursors cyclo(Leu‐Leu) and pulcherriminic acid and identified new precursor and degradation products of pulcherriminic acid and/or pulcherrimin. All of these compounds were identified in the wild‐type and complemented strain, but were undetectable in the pigmentless snf2 mutant strain. These results thus identify Snf2 as a regulator of antifungal activity and pulcherriminic acid biosynthesis in M. pulcherrima and provide a starting point for deciphering the molecular functions underlying the antagonistic activity of this yeast.
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The strong antifungal activity of Metschnikowia species is mediated by competition for nutrients such as amino acids and iron, secretion of glucanases and chitinases, and production of volatile organic compounds.
“The strong antifungal activity of Metschnikowia species is mediated by a range of mechanisms that involve competition for nutrients (e.g.; amino acids, iron), secretion of glucanases and chitinases, and the production of volatile organic compounds”
From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Gore-Lloyd et al. 2019
The Introduction (page unavailable) describes strong antifungal activity in M. pulcherrima and says iron depletion is thought to mediate antimicrobial activity. It does not establish amino-acid competition, glucanase or chitinase secretion, or volatile organic compounds as mechanisms. The Discussion (page unavailable) says the mechanisms contributing to its antifungal activity remain largely unknown. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe peculiar red color of M. pulcherrima colonies is due to the formation of a cyclic dipeptide, pulcherriminic acid, that complexes iron.
“The peculiar red color of M. pulcherrima colonies is due to the formation of a cyclic dipeptide, pulcherriminic acid, that complexes iron (Gore-Lloyd et al. 2019).”
From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Gore-Lloyd et al. 2019
Mutants lacking the ability to synthesise pulcherriminic acid still inhibited filamentous fungi strongly, suggesting that the antifungal activity was not only due to iron deprivation.
“However, mutants lacking the ability to synthesise pulcherriminic acid still inhibited filamentous fungi strongly, suggesting that the antifungal activity was not only due to iron deprivation (Gore-Lloyd et al. 2019).”
From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Gore-Lloyd et al. 2019
Pigmentless M. pulcherrima mutants exhibit reduced antifungal activity, and iron deprivation of the fungal pathogen was suggested as one of several mechanisms by which this yeast antagonises plant pathogenic fungi.
“Pigmentless M. pulcherrima mutants were shown to exhibit reduced antifungal activity and iron deprivation of the fungal pathogen was suggested as one of several mechanisms by which this yeast antagonises plant pathogenic fungi (Gore-Lloyd et al. 2019; Sipiczki 2006).”
From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Gore-Lloyd et al. 2019
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Sipiczki, M. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01275-06 · Cited by 291 · see citing works
Saravanakumar, D., Ciavorella, A., Spadaro, D., Garibaldi, A., & Gullino, M. L. (2008) · Postharvest Biology and Technology · doi:10.1016/j.postharvbio.2007.11.006 · Cited by 224 · see citing works
Functional Metabolomics Describes the Yeast Biosynthetic Regulome
Mülleder, M., Calvani, E., Alam, M. T., Wang, R. K., Eckerstorfer, F., Zelezniak, A., & Ralser, M. (2016) · Cell · doi:10.1016/j.cell.2016.09.007 · Cited by 178 · see citing works
Bar-Shimon, M., Yehuda, H., Cohen, L., Weiss, B., Kobeshnikov, A., Daus, A., Goldway, M., Wisniewski, M., & Droby, S. (2004) · Current Genetics · doi:10.1007/s00294-003-0471-7 · Cited by 140 · see citing works
Hilber-Bodmer, M., Schmid, M., Ahrens, C. H., & Freimoser, F. M. (2017) · BMC Microbiology · doi:10.1186/s12866-016-0908-z · Cited by 106 · cited 17× · see citing works
“The wild-type isolate APC 1.2 (CCOS978; Culture Collection of Switzerland) was originally isolated from apple flowers in Switzerland (Hilber-Bodmer et al., 2017) and was assigned to UNITE SH180747.”
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Research works printed but not linked: 70
- Abarenkov, K., Nilsson, R.H., Larsson, K.H., Alexander, I.J., Eberhardt, U., Erland, S., et al. (2010) The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytologist, 186, 281– 285. 20409185
- Agaimy, A. and Foulkes, W.D. (2018) Hereditary SWI/SNF complex deficiency syndromes. Seminars in Diagnostic Pathology, 35, 193– 198. 29397238
- Banani, H., Spadaro, D., Zhang, D., Matic, S., Garibaldi, A. and Gullino, M.L. (2014) Biocontrol activity of an alkaline serine protease from Aureobasidium pullulans expressed in Pichia pastoris against four postharvest pathogens on apple. International Journal of Food Microbiology, 182–183, 1– 8. 24854386
- Biegel, J.A., Busse, T.M. and Weissman, B.E. (2014) SWI/SNF chromatin remodeling complexes and cancer. American Journal of Medical Genetics Part C: Seminars in Medical Genetics, 166C, 350– 366. PMC4516040 25169151
- Butler, G., Rasmussen, M.D., Lin, M.F., Santos, M.A., Sakthikumar, S., Munro, C.A., et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, 459, 657– 662. 19465905 PMC2834264
- Byrne, K.P. and Wolfe, K.H. (2005) The yeast gene order browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Research, 15, 1456– 1461. 16169922 PMC1240090
- Carlson, M., Osmond, B.C. and Botstein, D. (1981) Mutants of yeast defective in sucrose utilization. Genetics, 98, 25– 40. 7040163 PMC1214432
- Chai, B., Huang, J., Cairns, B.R. and Laurent, B.C. (2005) Distinct roles for the RSC and Swi/Snf ATP‐dependent chromatin remodelers in DNA double‐strand break repair. Genes & Development, 19, 1656– 1661. 16024655 PMC1176001
- Chantasuban, T., Santomauro, F., Gore‐Lloyd, D., Parsons, S., Henk, D., Scott Roderick, J. and Chuck, C. (2018) Elevated production of the aromatic fragrance molecule, 2‐phenylethanol, using Metschnikowia pulcherrima through both de novo and ex novo conversion in batch and continuous modes. Journal of Chemical Technology and Biotechnology, 93, 2118– 2130. 30069076 PMC6055805
- Chen, I.A., Markowitz, V.M., Chu, K., Palaniappan, K., Szeto, E., Pillay, M., et al. (2017) IMG/M: integrated genome and metagenome comparative data analysis system. Nucleic Acids Research, 45, D507– D516. 27738135 PMC5210632
- Contreras, A., Hidalgo, C., Henschke, P.A., Chambers, P.J., Curtin, C. and Varela, C. (2014) Evaluation of non‐Saccharomyces yeasts for the reduction of alcohol content in wine. Applied and Environment Microbiology, 80, 1670– 1678. PMC3957604 24375129
- Contreras, A., Curtin, C. and Varela, C. (2015) Yeast population dynamics reveal a potential 'collaboration' between Metschnikowia pulcherrima and Saccharomyces uvarum for the production of reduced alcohol wines during Shiraz fermentation. Applied Microbiology and Biotechnology, 99, 1885– 1895. 25388943
- Cook, A.H. and Slater, C.A. (1954) Metabolism of ‘wild’ yeasts. I. The chemical nature of pulcherrimin. Journal of the Institute of Brewing, 60, 213– 217.
- Cryle, M.J., Bell, S.G. and Schlichting, I. (2010) Structural and biochemical characterization of the cytochrome P450 CypX (CYP134A1) from Bacillus subtilis: a cyclo‐L‐leucyl‐L‐leucyl dipeptide oxidase. Biochemistry, 49, 7282– 7296. 20690619
- De Curtis, F., de Felice, D.V., Ianiri, G., De Cicco, V. and Castoria, R. (2012) Environmental factors affect the activity of biocontrol agents against ochratoxigenic Aspergillus carbonarius on wine grape. International Journal of Food Microbiology, 159, 17– 24. 22921968
- Dudley, A.M., Janse, D.M., Tanay, A., Shamir, R. and Church, G.M. (2005) A global view of pleiotropy and phenotypically derived gene function in yeast. Molecular Systems Biology, 1, E1– E11. PMC1681449 16729036
- Dutta, A., Sardiu, M., Gogol, M., Gilmore, J., Zhang, D., Florens, L., et al. (2017) Composition and function of mutant Swi/Snf complexes. Cell Reports, 18, 2124– 2134. 28249159 PMC5837817
- Edgar, R., Domrachev, M. and Lash, A.E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research, 30, 207– 210. 11752295 PMC99122
- Enyenihi, A.H. and Saunders, W.S. (2003) Large‐scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae. Genetics, 163, 47– 54. 12586695 PMC1462418
- Gietz, R.D. and Woods, R.A. (2002) Transformation of yeast by lithium acetate/single‐stranded carrier DNA/polyethylene glycol method. Methods in Enzymology, 350, 87– 96. 12073338
- Gondry, M., Sauguet, L., Belin, P., Thai, R., Amouroux, R., Tellier, C., et al. (2009) Cyclodipeptide synthases are a family of tRNA‐dependent peptide bond‐forming enzymes. Nature Chemical Biology, 5, 414– 420. 19430487
- Gouy, M., Guindon, S. and Gascuel, O. (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27, 221– 224. 19854763
- Gross, S., Kunz, L., Muller, D.C., Santos Kron, A. and Freimoser, F.M. (2018) Characterization of antagonistic yeasts for biocontrol applications on apples or in soil by quantitative analyses of synthetic yeast communities. Yeast, 35, 559– 566. 29752875 PMC6220783
- Janisiewicz, W.J., Tworkoski, T.J. and Kurtzman, C.P. (2001) Biocontrol potential of Metchnikowia pulcherrima strains against blue mold of apple. Phytopathology, 91, 1098– 1108. 18943447
- Kántor, A., Hutková, J., Petrová, J., Hleba, L. and Kacániová, M. (2015) Antimicrobial activity of pulcherrimin pigment produced by Metschnikowia pulcherrima against various yeast species. Journal of Microbiology, Biotechnology and Food Sciences, 5, 282– 285.
- Kluyver, A.J., Vanderwalt, J.P. and Vantriet, A.J. (1953) Pulcherrimin, the pigment of Candida pulcherrima. Proceedings of the National Academy of Sciences, 39, 583– 593. PMC1063828 16589308
- Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H. and Phillippy, A.M. (2017) Canu: scalable and accurate long‐read assembly via adaptive k‐mer weighting and repeat separation. Genome Research, 27, 722– 736. 28298431 PMC5411767
- Krause, D.J., Kominek, J., Opulente, D.A., Shen, X.‐X., Zhou, X., Langdon, Q.K., et al. (2018) Functional and evolutionary characterization of a secondary metabolite gene cluster in budding yeasts. Proceedings of the National Academy of Sciences, 115(43), 11030– 11035. PMC6205458 30297402
- Kupfer, D.G., Uffen, R.L. and Canale‐Parola, E. (1967) The role of iron and molecular oxygen in pulcherrimin synthesis by bacteria. Archiv fϋr Mikrobiologie, 56, 9– 21. 4968608
- Laur, J., Ramakrishnan, G.B., Labbe, C., Lefebvre, F., Spanu, P.D. and Belanger, R.R. (2018) Effectors involved in fungal‐fungal interaction lead to a rare phenomenon of hyperbiotrophy in the tritrophic system biocontrol agent‐powdery mildew‐plant. New Phytologist, 217, 713– 725. 29044534 PMC6079639
- Laurent, B.C., Treich, I. and Carlson, M. (1993a) Role of yeast SNF and SWI proteins in transcriptional activation. Cold Spring Harbor Symposia on Quantitative Biology, 58, 257– 263. 7956037
- Laurent, B.C., Treich, I. and Carlson, M. (1993b) The yeast SNF2/SWI2 protein has DNA‐stimulated ATPase activity required for transcriptional activation. Genes & Development, 7, 583– 591. 8458575
- Leverentz, B., Conway, W.S., Janisiewicz, W., Abadias, M., Kurtzman, C.P. and Camp, M.J. (2006) Biocontrol of the food‐borne pathogens Listeria monocytogenes and Salmonella enterica serovar Poona on fresh‐cut apples with naturally occurring bacterial and yeast antagonists. Applied and Environment Microbiology, 72, 1135– 1140. PMC1392892 16461659
- Li, H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA‐MEM. arXiv:1303.3997v2. · arXiv
- Li, X., Wang, D., Cai, D., Zhan, Y., Wang, Q. and Chen, S. (2017) Identification and high‐level production of pulcherrimin in Bacillus licheniformis DW2. Applied Biochemistry and Biotechnology, 183, 1323– 1335. 28523413
- Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. (2009) The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078– 2079. 19505943 PMC2723002
- Liu, X., Li, M., Xia, X., Li, X. and Chen, Z. (2017) Mechanism of chromatin remodelling revealed by the Snf2‐nucleosome structure. Nature, 544, 440– 445. 28424519
- MacDonald, J.C. (1963) The structure of pulcherriminic acid. Canadian Journal of Chemistry, 41, 165– 172.
- MacDonald, J.C. (1965) Biosynthesis of pulcherriminic acid. The Biochemical Journal, 96, 533– 538. 5837792 PMC1207072
- Maguire, S.L., OhEigeartaigh, S.S., Byrne, K.P., Schroder, M.S., O'Gaora, P., Wolfe, K.H. and Butler, G. (2013) Comparative genome analysis and gene finding in Candida species using CGOB. Molecular Biology and Evolution, 30, 1281– 1291. 23486613 PMC3649674
- Melvydas, V., Staneviciene, R., Balynaite, A., Vaiciuniene, J. and Garjonyte, R. (2016) Formation of self‐organized periodic patterns around yeasts secreting a precursor of a red pigment. Microbiological Research, 193, 87– 93. 27825489
- Neigeborn, L. and Carlson, M. (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics, 108, 845– 858. 6392017 PMC1224269
- Nilsson, R.H., Larsson, K.H., Taylor, A.F.S., Bengtsson‐Palme, J., Jeppesen, T.S., Schigel, D., et al. (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research, 47(D1), D259– D264. PMC6324048 30371820
- Orij, R., Urbanus, M.L., Vizeacoumar, F.J., Giaever, G., Boone, C., Nislow, C., et al. (2012) Genome‐wide analysis of intracellular pH reveals quantitative control of cell division rate by pH(c) in Saccharomyces cerevisiae. Genome Biology, 13, R80. 23021432 PMC3506951
- Oro, L., Ciani, M. and Comitini, F. (2014) Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. Journal of Applied Microbiology, 116, 1209– 1217. 24443784
- Ortiz‐Merino, R.A., Varela, J.A., Coughlan, A.Y., Hoshida, H., da Silveira, W.B., Wilde, C., et al. (2018) Ploidy variation in Kluyveromyces marxianus separates dairy and non‐dairy isolates. Front Genet, 9, 94. 29619042 PMC5871668
- Parafati, L., Vitale, A., Restuccia, C. and Cirvilleri, G. (2015) Biocontrol ability and action mechanism of food‐isolated yeast strains against Botrytis cinerea causing post‐harvest bunch rot of table grape. Food Microbiology, 47, 85– 92. 25583341
- Patro, R., Duggal, G., Love, M.I., Irizarry, R.A. and Kingsford, C. (2017) Salmon provides fast and bias‐aware quantification of transcript expression. Nature Methods, 14, 417– 419. 28263959 PMC5600148
- Pelliccia, C., Antonielli, L., Corte, L., Bagnetti, A., Fatichenti, F. and Cardinali, G. (2011) Preliminary prospection of the yeast biodiversity on apple and pear surfaces from Northern Italy orchards. Annals of Microbiology, 61, 965– 972.
- Peterson, C.L. and Tamkun, J.W. (1995) The SWI‐SNF complex: a chromatin remodeling machine? Trends in Biochemical Sciences, 20, 143– 146. 7770913
- Piombo, E., Sela, N., Wisniewski, M., Hoffmann, M., Gullino, M.L., Allard, M.W., et al. (2018) Genome sequence, assembly and characterization of two Metschnikowia fructicola strains used as biocontrol agents of postharvest diseases. Frontiers in Microbiology, 9, 593. 29666611 PMC5891927
- Prasad, P., Lennartsson, A. and Ekwall, K. (2015) The roles of SNF2/SWI2 nucleosome remodeling enzymes in blood cell differentiation and leukemia. BioMed Research International, 2015, 347571. 25789315 PMC4348595
- Proux‐Wera, E., Armisen, D., Byrne, K.P. and Wolfe, K.H. (2012) A pipeline for automated annotation of yeast genome sequences by a conserved‐synteny approach. BMC Bioinformatics, 13, 237. 22984983 PMC3507789
- Randazzo, P., Aubert‐Frambourg, A., Guillot, A. and Auger, S. (2016) The MarR‐like protein PchR (YvmB) regulates expression of genes involved in pulcherriminic acid biosynthesis and in the initiation of sporulation in Bacillus subtilis. BMC Microbiology, 16, 190. 27542896 PMC4992311
- Reddy, K.R., Spadaro, D., Gullino, M.L. and Garibaldi, A. (2011) Potential of two Metschnikowia pulcherrima (yeast) strains for in vitro biodegradation of patulin. Journal of Food Protection, 74, 154– 156. 21219780
- Riley, R., Haridas, S., Wolfe, K.H., Lopes, M.R., Hittinger, C.T., Goker, M., et al. (2016) Comparative genomics of biotechnologically important yeasts. Proceedings of the National Academy of Sciences, 113, 9882– 9887. PMC5024638 27535936
- Ruiz‐Moyano, S., Martin, A., Villalobos, M.C., Calle, A., Serradilla, M.J., Cordoba, M.G. and Hernandez, A. (2016) Yeasts isolated from figs (Ficus carica L.) as biocontrol agents of postharvest fruit diseases. Food Microbiology, 57, 45– 53. 27052701
- Santamauro, F., Whiffin, F.M., Scott, R.J. and Chuck, C.J. (2014) Low‐cost lipid production by an oleaginous yeast cultured in non‐sterile conditions using model waste resources. Biotechnology for Biofuels, 7, 34. 24593824 PMC4016040
- Serviene, E., Luksa, J., Orentaite, I., Lafontaine, D.L. and Urbonavicius, J. (2012) Screening the budding yeast genome reveals unique factors affecting K2 toxin susceptibility. PLoS ONE, 7, e50779. 23227207 PMC3515549
- Sipiczki, M., Pfliegler, W.P. and Holb, I.J. (2013) Metschnikowia species share a pool of diverse rRNA genes differing in regions that determine hairpin‐Loop structures and evolve by reticulation. PLoS ONE, 8, e67384. 23805311 PMC3689696
- Sipiczki, M., Horvath, E. and Pfliegler, W.P. (2018) Birth‐and‐death evolution and reticulation of ITS segments of Metschnikowia andauensis and Metschnikowia fructicola rDNA repeats. Frontiers in Microbiology, 9, 1193. 29946303 PMC6005844
- Slavikova, E., Vadkertiova, R. and Vranova, D. (2007) Yeasts colonizing the leaf surfaces. Journal of Basic Microbiology, 47, 344– 350. 17645279
- Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312– 1313. 24451623 PMC3998144
- Stern, M., Jensen, R. and Herskowitz, I. (1984) Five SWI genes are required for expression of the HO gene in yeast. Journal of Molecular Biology, 178, 853– 868. 6436497
- Turkel, S., Korukluoglu, M. and Yavuz, M. (2014) Biocontrol activity of the local strain of Metschnikowia pulcherrima on different postharvest pathogens. Biotechnology Research International, 2014, 397167. 24860671 PMC4016867
- Uffen, R.L. and Canale‐Parola, E. (1972) Synthesis of pulcherriminic acid by Bacillus subtilis. Journal of Bacteriology, 111, 86– 93. 4204912 PMC251243
- Vadkertiova, R., Molnarova, J., Vranova, D. and Slavikova, E. (2012) Yeasts and yeast‐like organisms associated with fruits and blossoms of different fruit trees. Canadian Journal of Microbiology, 58, 1344– 1352. 23210991
- Venkatesh, A., Murray, A.L., Boyle, A.B., Quinn Farrington, L., Maher, T.J., O'Gaora, P., et al. (2018) Draft genome sequence of a highly heterozygous yeast strain from the Metschnikowia pulcherrima subclade, UCD127. Genome Announc, 6, e00550‐18. 29930059 PMC6013633
- Wang, D., Zhan, Y., Cai, D., Li, X., Wang, Q. and Chen, S. (2018) Regulation of the synthesis and secretion of the iron chelator cyclodipeptide pulcherriminic acid in Bacillus licheniformis. Applied and Environment Microbiology, 84, e00262‐00218. PMC6007100 29703732
- Wilson, B.G. and Roberts, C.W. (2011) SWI/SNF nucleosome remodellers and cancer. Nature Reviews Cancer, 11, 481– 492. 21654818
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Biocontrol yeasts: mechanisms and applications
Freimoser, F. M., Rueda-Mejia, M. P., Tilocca, B., & Migheli, Q. (2019) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-019-2728-4 · Cited by 462 · see citing works
Self-citation
- Authors
- Gore‐Lloyd, D., Sumann, I., Brachmann, A. O., Schneeberger, K., Ortiz‐Merino, R. A., Moreno‐Beltrán, M., Schläfli, M., Kirner, P., Santos Kron, A., Rueda‐Mejia, M. P., Somerville, V., Wolfe, K. H., Piel, J., Ahrens, C. H., Henk, D., & Freimoser, F. M.
- Affiliations
- University of Bath (GB)
- Agroscope (CH)
- ETH Zurich (CH)
- Competence Division Method Development and Analytics Müller‐Thurgau‐Strasse 29 8820 Wädenswil Switzerland
- University College Dublin (IE)
- Agroscope, Research Division Plant Protection Müller‐Thurgau‐Strasse 29 8820 Wädenswil Switzerland
- SIB Swiss Institute of Bioinformatics (CH)
- Corresponding author
- Freimoser, Florian M.
- ORCID
- Venue
- Molecular Microbiology
- Publisher
- Wiley
- Published
- 2019-05-20
- Volume
- 112
- Issue
- 1
- Pages
- 317-332
- ISSN
- 0950-382X (ISSN-L)
- 1365-2958
- PMC
- PMC6851878
- OpenAlex
- W2945945765
- Cited by
- 102
- References
- 5
- Citations by year
- 2026: 17 · 2025: 13 · 2024: 11 · 2023: 15 · 2022: 13 · 2021: 17 · 2020: 12 · 2019: 3 · 2018: 1
- FWCI
- 6.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular Microbiology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc)
- ETH Zürich Research Collection
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_175665 / 1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Metabolism and Applications
- Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- Metschnikowia pulcherrima, SnF2, antifungal activity, biocontrol yeast, transcription factors, pigment synthesis, phyllosphere, plant pathogenic fungi, gene complementation, yeast antagonism
- MeSH terms
- Adenosine Triphosphatases, Antibiosis, Antifungal Agents, Fungi, Pyrazines, Saccharomyces cerevisiae, Transcription Factors, Saccharomyces cerevisiae Proteins, Metschnikowia
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