Abstract
Massoia lactone could be released from liamocins produced by Aureobasidium melanogenum M39. The obtained Massoia lactone was very stable and highly active against many fungal crop pathogens which cause many plant diseases and food unsafety. Massoia lactone treatment not only could effectively inhibit their hyphal growth and spore germination, but also caused pore formation in cell membrane, reduction of ergosterol content, rise in intracellular ROS levels, and leakage of intracellular components, consequently leading to cellular necrosis and cell death. The direct contact of Massoia lactone with Fusarium graminearum spores could stop the development of Fusarium head blight symptom in the diseased wheats. Therefore, Massoia lactone could be a promising candidate for development as an effective and green bio-fungicide because of its high anti-fungal activity and the multiplicity of mode of its action.
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References
Zhang J, Chen J, Hu L, Jia R, Ma JQ (2020) Antagonistic action of Streptomyces pratensis S10 on Fusarium graminearum and its complete genome sequence. Environ Microbiol: https://doi.org/10.1111/1462-2920.15282
Albayrak CB (2019) Bacillus species as biocontrol agents for fungal plant pathogens. Springer Nature Switzerland AG In: M. T. Islam et al. (eds.), Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol, Bacilli in Climate Resilient Agriculture Bioprospectives Pp: 239–264
Chattapadhyay TK, Dureja P (2006) Antifungal activity of 4-methyl-6-alkyl-2H-pyran-2-ones. J Agri Food Chem 54:2129–2133
Aswathi A, Pandey A, Sukumaran RK (2019) Rapid degradation of the organophosphate pesticide–Chlorpyrifos by a novel strain of Pseudomonas nitroreducens AR-3. Biore Technol 292:122025
Kumar LR, NdaoValéro AL, Tyagi RD (2019) Production of Bacillus thuringiensis based biopesticide formulation using starch industry wastewater (SIW) as substrate: a techno-economic evaluation. Biores Technol 294:122144
Daguerre Y, Edel-Hermann V, Steinberg C (2017) Fungal genes and metabolites associated with the biocontrol of soil-borne plant pathogenic fungi. In: J.-M. Mérillon, K.G. Ramawat (eds.), Fungal Metabolites, Reference Series in Phytochemistry, ©Springer International Publishing Switzerland, pp: 33–82.
Qian S, Lu H, Sun J, Zhang C, Zhao H (2016) Antifungal activity mode of Aspergillus ochraceus by bacillomycin D and its inhibition of ochratoxin A (OTA) production in food samples. Food Control 60:281–288
Volpon L, Besson F, Lancelin JM (2000) NMR structure of antibiotics plipastatins A and B from Bacillus subtilis inhibitors of phospholipase A2. FEBS Lett 485:76–80
Wang F, Saito S, Michailides TJ, Xiao CL (2021) Postharvest use of natamycin to control Alternaria rot on blueberry fruit caused by Alternaria alternata and A. arborescens. Postharv Biol Technol 172:111383
Senol M, Nadaroglu H, Dikbas N, Kotan R (2014) Purification of Chitinase enzymes from Bacillus subtilis bacteria TV-125, investigation of kinetic properties and antifungal activity against Fusarium culmorum. Ann Clin Microbiol Antimicrob 13:35
Chaves-López C, Serio A, Gianotti A, Sacchetti G, Ndagijimana M, Ciccarone C (2015) Diversity of food-borne Bacillus volatile compounds and influence on fungal growth. J Appl Microbiol 119:487–499
El-Hasan A, Walker F, Buchenauer H (2008) Trichoderma harzianum and its metabolite 6-pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J Phytopathol 156:79–87
Park JH, Choi GJ, Jang KS, Lim HK, Kim HT (2005) Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. FEMS Microbiol Lett 252:309–313
Park JH, Choi GL, Lee HB, Kim KM, Jung HS (2005) Griseofulvin from Xylaria sp strain F0010, an endophytic fungus of Abies holophylla and its antifungal activity against plant pathogenic fungi. J Microbiol Biotechnol 15:112–117
Teichmann B, Labbé C, Lefebvre F, Bölker M, Linne U (2011) Identification of a biosynthesis gene cluster for flocculosin a cellobiose lipid produced by the biocontrol agent Pseudozyma flocculosa. Mole Microbiol 79:1483–1495
Santos A, Marquina D (2004) Killer toxin of Pichia membranifaciens and its possible use as a biocontrol agent against grey mould disease of grapevine. Microbiol 150:2527–2534
Murray FR, Llewellyn DJ, Peacock WJ, Dennis ES (1997) Isolation of the glucose oxidase gene from Talaromyces flavus and characterisation of its role in the biocontrol of Verticillium dahlia. Curr Genet 32:367–375
Haselwandter K, Haninger G, Ganzera M, Haas H, Nicholson R (2013) Linear fusigen as the major hydroxamate siderophore of the ectomycorrhizal Basidiomycota Laccaria laccata and Laccaria bicolor. Biomet 26:969–979
Xue SJ, Liu GL, Chi Z, Gao ZC, Hu Z, Chi ZM (2020) Genetic evidences for the core biosynthesis pathway, regulation, transport and secretion of liamocins in yeast-like fungal cells. Biochem J 477:887–903
Zhang HQ, Chi Z, Liu GL, Zhang M, Hu Z, Chi ZM (2021) Metschnikowia bicuspidate associated with a milky disease in Eriocheir sinensis and its effective treatment by Massoia lactone. Microbiol Res 242:126641
Tang RR, Chi Z, Jiang H, Liu GL, Hu Z, Chi ZM (2018) Overexpression of a pyruvate carboxylase gene enhances extracellular liamocin and intracellular lipid biosynthesis by Aureobasidium melanogenum M39. Proc Biochem 69:64–74
Zeng H, Chen R, Luo XX, Tian J (2016) Isolation and anti-Verticillium dahliae, activity from Bacillus axarquiensis TUBP1 protein. Proc Biochem 51:1691–1698
Zeng H, Chen XP, Liang JN (2015) In vitro antifungal activity and mechanism of essential oil from fennel (Foeniculum vulgare L.) on dermatophyte species. J Med Microbiol 64:93–103
Zhang YB, Cui PF, Wang YH, Zhang SC (2018) Identification and bioactivity analysis of a newly identified defensin from the oyster Magallana gigas. Developmental and Comparative Immunology: Ontogeny, Phylogeny, Aging, The Off J Intern Soc Develop Comparat Immunol 85:177–187
Li G, Zhou J, Jia H, Gao Z, Fan M, Luo Y (2019) Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to fusarium head blight. Nat Genet 51:1106–1112
Jiang L, Zhang M, Meng Z, Xie M (2018) Honokiol kills Candida albicans through ROS accumulation and cell membrane destruction. Acta Microbiol Sin 58:511–519
Lin F, Kong ZX, Zhu SL, Xue JZ, Wu DG (2004) Mapping QTL associated with resistance to fusarium head blight in the nanda2419 x wangshuibai population. I: type II resistance. Theoret Appl Genet 112:1504–1511
Avis TJ, Belanger RR (2001) Specificity and mode of action of the antifungal fatty acid cis-9-heptadecenoic acid produced by Pseudozyma flocculosa. Appl Environ Microbiol 67:956–960
Wang B, Shen Z, Zhang F, Raza W, Yuan J (2016) Bacillus amyloliquefaciens strain W19 can promote growth and yield and suppress Fusarium wilt in banana under greenhouse and field conditions. Pedosphol 26:733–744
Parker SR, Cutler HG, Jacyno JM, Hill RA (1997) Biological activity of 6-pentyl-2H-pyran-2-one and its analogs. J Agri Food Chem 45:2774–2776
Jeleń H, Błaszczyk L, Chełkowski J, Rogowicz K, Strakowska J (2014) Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycol Prog 13:589–600
Meng X, Feng L, Zhang J, Shi M, Wang G (2016) Synthesis of 5-Hydroxy-2-decenoic acid lactone (Massoia Lactone). Chin Acad J Elect Publish Hous 1:114–118
Cao Y, Xu Z, Ling N (2012) Isolation and identification of lipopeptides produced by B. subtilis SQR 9 for suppressing Fusarium wilt of cucumber. Sci Horticult 135:32–39
Luepongpattana S, Thaniyavarn J, Morikawa M (2017) Production of Massoia lactone by Aureobasidium pullulans YTP6-14 isolated from the gulf of Thailand and its fragrant biosurfactant properties. J Appl Microbiol 123:1488–1497
Gong Q, Zhang C, Lu F, Zhao H, Bie X (2014) Identification of bacillomycin D from Bacillus subtilis fmbJ and its inhibition effects against Aspergillus flavus. Food Control 36:8–14
Liu Y, Lu J, Sun J, Lu F, Bie X (2019) Membrane disruption and DNA binding of Fusarium graminearum cell induced by C16-Fengycin A produced by Bacillus amyloliquefaciens. Food Control 102:206–213
Funding
This study was financially supported by the National Natural Science Foundation of China (Grant No. 31970058), the key research and development of Shandong Province (Grant No. 2019GSF107097), Bingtuan Science and Technology Program (Grant No. 2021BC009), and the Fundamental Research Funds for the Central Universities (Grant No. 202066002).
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MZ, ZCG, ZW, and XFL conducted all the experiments. ZC and GLL analyzed data. ZH and ZMC conceived and designed research and wrote the manuscript. All authors read and approved the manuscript.
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Zhang, M., Gao, ZC., Chi, Z. et al. Massoia Lactone Displays Strong Antifungal Property Against Many Crop Pathogens and Its Potential Application. Microb Ecol 84, 376–390 (2022). https://doi.org/10.1007/s00248-021-01885-7
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DOI: https://doi.org/10.1007/s00248-021-01885-7