Abstract
Plant volatile compounds have great potential for preventing and controlling fungal spoilage in post-harvest grains. Recently, we have reported the antifungal effects of trans-anethole, the main volatile constituent of the Illicium verum fruit, on Aspergillus flavus. In this study, the inhibitory mechanisms of trans-anethole against the growth of A. flavus mycelia were investigated using transcriptomic and biochemical analyses. Biochemical and transcriptomic changes in A. flavus mycelia were evaluated after exposure to 0.2 μL/mL trans-anethole. Scanning electron microscopy showed that trans-anethole treatment resulted in the surface wrinkling of A. flavus mycelia, and calcofluor white staining confirmed that trans-anethole treatment disrupted the mycelial cell wall structure. Annexin V-fluorescein isothiocyanate/propidium iodide double staining suggested that trans-anethole induced apoptosis in A. flavus mycelia. Reduced mitochondrial membrane potential and DNA damage were observed in trans-anethole-treated A. flavus mycelia using 5,5′,6,6′-tetrachloro-1,1′,3,3′-tetraethyl-imidacarbocyanine and 4′,6-diamidino-2-phenylindole staining, respectively. 2′,7′- Dichloro-dihydro-fluorescein diacetate staining and biochemical assays demonstrated that trans-anethole treatment cause the accumulation of reactive oxygen species in the A. flavus mycelia. Transcriptome results showed that 1673 genes were differentially expressed in A. flavus mycelia exposed to trans-anethole, which were mainly associated with multidrug transport, oxidative phosphorylation, citric acid cycle, ribosomes, and cyclic adenosine monophosphate signaling. We propose that trans-anethole can inhibit the growth of A. flavus mycelia by disrupting the cell wall structure, blocking the multidrug transport process, disturbing the citric acid cycle, and inducing apoptosis. This study provides new insights into the inhibitory mechanism of trans-anethole on A. flavus mycelia and will be helpful for the development of natural fungicides.
Key points
• Biochemical analyses of A. flavus mycelia exposed to trans-anethole were performed
• Transcriptomic changes in trans-anethole-treated A. flavus mycelia were analyzed
• An inhibitory mechanism of trans-anethole on the growth of A. flavus mycelia was proposed
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Nature Preced 1-1. https://doi.org/10.1038/npre.2010.4282.1
Andrés MT, Acosta-Zaldívar M, Fierro JF (2016) Antifungal mechanism of action of lactoferrin: identification of H+-ATPase (P3A-type) as a new apoptotic-cell membrane receptor. Antimicrob Agents Ch 60(7):4206–4216. https://doi.org/10.1128/AAC.03130-15
Aranda A, Sequedo L, Tolosa L, Quintas G, Burello E, Castell J, Gombau L (2013) Dichloro-dihydro-fluorescein diacetate (DCFH-DA) assay: a quantitative method for oxidative stress assessment of nanoparticle-treated cells. Toxicol In Vitro 27(2):954–963. https://doi.org/10.1016/j.tiv.2013.01.016
Baltussen TJH, van Rhijn N, Coolen JPM, Dijksterhuis J, Verweij PE, Bromley MJ, Melchers WJG (2023) The C2H2 transcription factor SltA is required for germination and hyphal development in Aspergillus fumigatus. mSphere:e0007623. https://doi.org/10.1128/msphere.00076-23
Bammert GF, Fostel JM (2000) Genome-wide expression patterns in Saccharomyces cerevisiae: comparison of drug treatments and genetic alterations affecting biosynthesis of ergosterol. Antimicrob Agents Ch 44(5):1255–1265. https://doi.org/10.1128/aac.44.5.1255-1265.2000
Bard M, Bruner D, Pierson C, Lees N, Biermann B, Frye L, Koegel C, Barbuch R (1996) Cloning and characterization of ERG25, the Saccharomyces cerevisiae gene encoding C-4 sterol methyl oxidase. P Natl Acad Sci 93(1):186–190. https://doi.org/10.1073/pnas.93.1.186
Beere HM (2004) The stress of dying': the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117(13):2641–2651. https://doi.org/10.1242/jcs.01284
Binder U, Oberparleiter C, Meyer V, Marx F (2010) The antifungal protein PAF interferes with PKC/MPK and cAMP/PKA signalling of Aspergillus nidulans. Mol Microbiol 75(2):294–307. https://doi.org/10.1111/j.1365-2958.2009.06936.x
Boyer PD (2002) Catalytic site occupancy during ATP synthase catalysis. FEBS Lett 512(1-3):29–32. https://doi.org/10.1016/s0014-5793(02)02293-7
Chaari F, Chaabouni SE (2019) Fungal β-1, 3-1, 4-glucanases: production, proprieties and biotechnological applications. J Sci Food Agr 99(6):2657–2664. https://doi.org/10.1002/jsfa.9491
Chambers CS, Viktorová J, Řehořová K, Biedermann D, Turková L, Macek T, Křen V, Valentová K (2020) Defying multidrug resistance! modulation of related transporters by flavonoids and flavonolignans. J Agric Food Chem 68(7):1763–1779. https://doi.org/10.1021/acs.jafc.9b00694
Chaudhary PM, Tupe SG, Deshpande MV (2013) Chitin synthase inhibitors as antifungal agents. Mini-Rev Med Chem 13(2):222–236. https://doi.org/10.2174/138955713804805256
Chew SY, Chee WJY, Than LTL (2019) The glyoxylate cycle and alternative carbon metabolism as metabolic adaptation strategies of Candida glabrata: perspectives from Candida albicans and Saccharomyces cerevisiae. J Biomed Sci 26(1):52. https://doi.org/10.1186/s12929-019-0546-5
Dąbrowska M, Zielińska-Bliźniewska H, Kwiatkowski P, Guenther S, Łopusiewicz Ł, Kochan E, Pruss A, Sienkiewicz M (2023) Improved efficacy of eugenol and trans-anethole in combination with octenidine dihydrochloride against Candida albicans and Candida parapsilosis. Ann Agr Env Med 30(1):204–210. https://doi.org/10.26444/aaem/157995
del Mar Blanquer-Rosselló M, Hernández-López R, Roca P, Oliver J, Valle A (2017) Resveratrol induces mitochondrial respiration and apoptosis in SW620 colon cancer cells. BBA-Gen Subjects 1861(2):431-440. https://doi.org/10.1016/j.bbagen.2016.10.009
Du S, Guan Z, Hao L, Song Y, Wang L, Gong L, Liu L, Qi X, Hou Z, Shao S (2014) Fructose-bisphosphate aldolase a is a potential metastasis-associated marker of lung squamous cell carcinoma and promotes lung cell tumorigenesis and migration. PLoS One 9(1):e85804. https://doi.org/10.1371/journal.pone.0085804
Duan W, Qin Y, Zhang S, Zhai H, Lv Y, Wei S, Ma P, Hu Y (2023a) Inhibitory mechanisms of plant volatile 1-octanol on the germination of Aspergillus flavus spores. Food Biophys. https://doi.org/10.1007/s11483-023-09807-5
Duan W, Zhang S, Lei J, Qin Y, Li Y, Lv Y, Zhai H, Cai J, Hu Y (2023b) Protection of postharvest grains from fungal spoilage by biogenic volatiles. Appl Microbiol Biot 107(11):3375–3390. https://doi.org/10.1007/s00253-023-12536-x
Duan W, Zhang S, Lv Y, Zhai H, Wei S, Ma P, Cai J, Hu Y (2023c) Inhibitory effect of (E)-2-heptenal on Aspergillus flavus growth revealed by metabolomics and biochemical analyses. Appl Microbiol Biot 107(1):341–354. https://doi.org/10.1007/s00253-022-12320-3
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198(1):16–32. https://doi.org/10.1111/nph.12145
Duo-Chuan L (2006) Review of fungal chitinases. Mycopathologia 161:345–360. https://doi.org/10.1007/s11046-006-0024-y
Fan L, Wei Y, Chen Y, Jiang S, Xu F, Zhang C, Wang H, Shao X (2023) Epinecidin-1, a marine antifungal peptide, inhibits Botrytis cinerea and delays gray mold in postharvest peaches. Food Chem 403:134419. https://doi.org/10.1016/j.foodchem.2022.134419
Fozo EM, Quivey RG Jr (2004) Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl Environ Microb 70(2):929–936. https://doi.org/10.1128/AEM.70.2.929-936.2004
Gao Q, Fan Y, Wei S, Song S, Guo Y, Wang S, Liu Y, Yan D (2023) Insights into the global transcriptome response of Lentinula edodes mycelia during aging. J Fungi 9(3):379. https://doi.org/10.3390/jof9030379
Garreau H, Hasan RN, Renault G, Estruch F, Boy-Marcotte E, Jacquet M (2000) Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology 146(9):2113–2120. https://doi.org/10.1099/00221287-146-9-2113
Goldstein AS (1996) Synthesis and bioevaluation of Δ7-5-desaturase inhibitors, an enzyme late in the biosynthesis of the fungal sterol ergosterol. J Med Chem 39(26):5092–5099. https://doi.org/10.1021/jm9605851
Hu Z, Yuan K, Zhou Q, Lu C, Du L, Liu F (2021) Mechanism of antifungal activity of Perilla frutescens essential oil against Aspergillus flavus by transcriptomic analysis. Food Control 123:107703. https://doi.org/10.1016/j.foodcont.2020.107703
Huang Y, Zhao J, Zhou L, Wang J, Gong Y, Chen X, Guo Z, Wang Q, Jiang W (2010) Antifungal activity of the essential oil of Illicium verum fruit and its main component trans-anethole. Molecules 15(11):7558–7569. https://doi.org/10.3390/molecules15117558
Ibe C, Munro CA (2021) Fungal cell wall proteins and signaling pathways form a cytoprotective network to combat stresses. J Fungi 7(9):739. https://doi.org/10.3390/jof7090739
Ito Y, Muraguchi H, Seshime Y, Oita S, Yanagi SO (2004) Flutolanil and carboxin resistance in Coprinus cinereus conferred by a mutation in the cytochrome b560 subunit of succinate dehydrogenase complex (Complex II). Mol Genet Genomics 272(3):328–335. https://doi.org/10.1007/s00438-004-1060-2
Ji C, Kuć J (1996) Antifungal activity of cucumber β-1, 3-glucanase and chitinase. Physiol Mol Plant P 49(4):257–265. https://doi.org/10.1006/pmpp.1996.0053
Jordá T, Puig S (2020) Regulation of ergosterol biosynthesis in Saccharomyces cerevisiae. Genes 11(7):795. https://doi.org/10.3390/genes11070795
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30. https://doi.org/10.1093/nar/28.1.27
Kapuscinski J (1995) DAPI: a DNA-specific fluorescent probe. Biotech Histochem 70(5):220–233. https://doi.org/10.3109/10520299509108199
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Kornberg RD (1999) Eukaryotic transcriptional control. Trends Biochem Sci 24(12):M46–M49. https://doi.org/10.1016/S0968-0004(99)01489-9
Lee JM, Lee H, Kang S, Park WJ (2016) Fatty acid desaturases, polyunsaturated fatty acid regulation, and biotechnological advances. Nutrients 8(1):23. https://doi.org/10.3390/nu8010023
Lee SB, Kwon IS, Park J, Lee KH, Ahn Y, Lee C, Kim J, Choi SY, Cho SW, Ahn JY (2010) Ribosomal protein S3, a new substrate of Akt, serves as a signal mediator between neuronal apoptosis and DNA repair. J Biol Chem 285(38):29457–29468. https://doi.org/10.1074/jbc.M110.131367
Lei J, Zhang S, Ding W, Lv Y, Zhai H, Wei S, Ma P, Hu Y (2023) Antifungal effects of trans-anethole, the main constituent of Illicium verum fruit volatiles, on Aspergillus flavus in stored wheat. Food Control 149:109721. https://doi.org/10.1016/j.foodcont.2023.109721
Li Q, Zhao Y, Zhu X, Xie Y (2022a) Antifungal effect of o-vanillin on mitochondria of Aspergillus flavus: ultrastructure and TCA cycle are destroyed. Int J Food Sci Tech 57(5):3142–3149. https://doi.org/10.1111/ijfs.15647
Li S, Zhang S, Lv Y, Zhai H, Hu Y, Cai J (2022b) Transcriptome analysis reveals the underlying mechanism of heptanal against Aspergillus flavus spore germination. Appl Microbiol Biot 106(3):1241–1255. https://doi.org/10.1007/s00253-022-11783-8
Li S, Zhang S, Zhai H, Lv Y, Hu Y, Cai J (2021a) Hexanal induces early apoptosis of Aspergillus flavus conidia by disrupting mitochondrial function and expression of key genes. Appl Microbiol Biot 105:6871–6886. https://doi.org/10.1007/s00253-021-11543-0
Li T, Chen X, Lin S (2021b) Physiological and transcriptomic responses to N-deficiency and ammonium: Nitrate shift in Fugacium kawagutii (Symbiodiniaceae). Sci Total Environ 753:141906. https://doi.org/10.1016/j.scitotenv.2020.141906
Li X, Wang Q, Li H, Wang X, Zhang R, Yang X, Jiang Q, Shi Q (2023) Revealing the mechanisms for linalool antifungal activity against Fusarium oxysporum and its efficient control of fusarium wilt in tomato plants. Int J Mol Sci 24(1):458. https://doi.org/10.3390/ijms24010458
Li Y, Zhang S, Lv Y, Zhai H, Cai J, Hu Y (2022c) Mechanisms underlying the inhibitory effects of linalool on Aspergillus flavus spore germination. Appl Microbiol Biot 106(19-20):6625–6640. https://doi.org/10.1007/s00253-022-12172-x
Ma Y, Yu H, Liu W, Qin Y, Xing R, Li P (2020) Integrated proteomics and metabolomics analysis reveals the antifungal mechanism of the C-coordinated O-carboxymethyl chitosan Cu (II) complex. Int J Biol Macromol 155:1491–1509. https://doi.org/10.1016/j.ijbiomac.2019.11.127
Martínez-Blay V, Taberner V, Pérez-Gago MB, Palou L (2021) Postharvest treatments with sulfur-containing food additives to control major fungal pathogens of stone fruits. Foods 10(9):2115. https://doi.org/10.3390/foods10092115
Mukhopadhyay R, Kumar D (2020) Trichoderma: a beneficial antifungal agent and insights into its mechanism of biocontrol potential. Egypt J Biol Pest Co 30(1):1–8. https://doi.org/10.1186/s41938-020-00333-x
Namiota M, Bonikowski R (2021) The current state of knowledge about essential oil fumigation for quality of crops during postharvest. Int J Mol Sci 22(24):13351. https://doi.org/10.3390/ijms222413351
Nazari M, Minai-Tehrani A, Emamzadeh R (2014) Comparison of different probes based on labeled annexin V for detection of apoptosis. Rsc Adv 4(85):45128–45135. https://doi.org/10.1039/c4ra07577c
Osman F, Bjørås M, Alseth I, Morland I, McCready S, Seeberg E, Tsaneva I (2003) A new Schizosaccharomyces pombe base excision repair mutant, nth1, reveals overlapping pathways for repair of DNA base damage. Mol Microbiol 48(2):465–480. https://doi.org/10.1046/j.1365-2958.2003.03440.x
OuYang Q, Tao N, Zhang M (2018) A damaged oxidative phosphorylation mechanism is involved in the antifungal activity of citral against Penicillium digitatum. Front Microbiol 9:239. https://doi.org/10.3389/fmicb.2018.00239
Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37(18):e123. https://doi.org/10.1093/nar/gkp596
Peng H, Han S, Luo M, Gao J, Liu X, Zhao M (2011) Roles of multidrug transporters of MFS in plant stress responses. J Biochem Mol Biol 1(2):109. https://doi.org/10.7763/IJBBB.2011.V1.20
Polacheck I, Rosenberger R (1977) Aspergillus nidulans mutant lacking α-(1, 3)-glucan, melanin, and cleistothecia. J Bacteriol 132(2):650–656. https://doi.org/10.1128/jb.132.2.650-656.1977
Puri N, Prakash O, Manoharlal R, Sharma M, Ghosh I, Prasad R (2010) Analysis of physico-chemical properties of substrates of ABC and MFS multidrug transporters of pathogenic Candida albicans. Eur J Med Chem 45(11):4813–4826. https://doi.org/10.1016/j.ejmech.2010.07.050
Qin Y, Zhang S, Ding W, Lv Y, Zhai H, Wei S, Ma P, Hu Y (2023) The effect of volatile compounds of Syzygium aromaticum flower buds against Aspergillus flavus growth on wheat grain at postharvest stage. Food Control 145:109450. https://doi.org/10.1016/j.foodcont.2022.109450
Qin Y, Zhang S, Lv Y, Zhai H, Hu Y, Cai J (2022a) The antifungal mechanisms of plant volatile compound 1-octanol against Aspergillus flavus growth. Appl Microbiol Biot 106(13-16):5179–5196. https://doi.org/10.1007/s00253-022-12049-z
Qin Y, Zhang S, Lv Y, Zhai H, Hu Y, Cai J (2022b) Transcriptomics analyses and biochemical characterization of Aspergillus flavus spores exposed to 1-nonanol. Appl Microbiol Biot 106(5-6):2091–2106. https://doi.org/10.1007/s00253-022-11830-4
Rather IA, Sabir JS, Asseri AH, Ali S (2022) Antifungal activity of human cathelicidin LL-37, a membrane disrupting peptide, by triggering oxidative stress and cell cycle arrest in Candida auris. J Fungi 8(2):204. https://doi.org/10.3390/jof8020204
Shinde BH, Inamdar SN, Nalawade SA, Chaudhari SB (2023) A systematic review on antifungal and insecticidal applications of biosynthesized metal nanoparticles. Mater Today: Proceedings 73:412–417. https://doi.org/10.1016/j.matpr.2022.09.548
Shingu-Vazquez M, Traven A (2011) Mitochondria and fungal pathogenesis: drug tolerance, virulence, and potential for antifungal therapy. Eukaryotic cell 10(11):1376–1383. https://doi.org/10.1128/ec.05184-11
Smeitink JA, van den Heuvel LW, Koopman WJ, Nijtmans LG, Ugalde C, Willems PH (2004) Cell biological consequences of mitochondrial NADH: ubiquinone oxidoreductase deficiency. Curr Neurovasc Res 1(1):29–40. https://doi.org/10.2174/1567202043480224
Speers AE, Wu CC (2007) Proteomics of integral membrane proteins theory and application. Chem Rev 107(8):3687–3714. https://doi.org/10.1021/cr068286z
Stenum TS, Kumar AD, Sandbaumhüter FA, Kjellin J, Jerlström-Hultqvist J, Andrén PE, Koskiniemi S, Jansson ET, Holmqvist E (2023) RNA interactome capture in Escherichia coli globally identifies RNA-binding proteins. Nucleic Acids Res 51(9):4572–4587. https://doi.org/10.1093/nar/gkad216
Taillis D, Becissa O, Pébarthé-Courrouilh A, Renouf E, Palos-Pinto A, Richard T, Cluzet S (2023) Antifungal activities of a grapevine byproduct extract enriched in complex stilbenes and stilbenes metabolization by Botrytis cinerea. J Agric Food Chem 71(11):4488–4497. https://doi.org/10.1021/acs.jafc.2c07843
Takahashi-Iniguez T, Aburto-Rodriguez N, Laura Vilchis-Gonzalez A, Elena Flores M (2016) Function, kinetic properties, crystallization, and regulation of microbial malate dehydrogenase. J Zhejiang Univ-Sc B 17(4):247–261. https://doi.org/10.1631/jzus.B1500219
Tang L, Mo J, Guo T, Huang S, Li Q, Ning P, Hsiang T (2020) In vitro antifungal activity of dimethyl trisulfide against Colletotrichum gloeosporioides from mango. World J Microb Biot 36:1–15. https://doi.org/10.1007/s11274-019-2781-z
Tian J, Ban X, Zeng H, He J, Chen Y, Wang Y (2012a) The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLoS One 7(1):e30147. https://doi.org/10.1371/journal.pone.0030147
Tian J, Huang B, Luo X, Zeng H, Ban X, He J, Wang Y (2012b) The control of Aspergillus flavus with Cinnamomum jensenianum Hand.-Mazz essential oil and its potential use as a food preservative. Food Chem 130(3):520–527. https://doi.org/10.1016/j.foodchem.2011.07.061
Ueda N, Puffenbarger RA, Yamamoto S, Deutsch DG (2000) The fatty acid amide hydrolase (FAAH). Chem Phys Lipids 108(1-2):107–121. https://doi.org/10.1016/S0009-3084(00)00190-0
Verstrepen KJ, Reynolds TB, Fink GR (2004) Origins of variation in the fungal cell surface. Nat Rev Microbiol 2(7):533–540. https://doi.org/10.1038/nrmicro927
Wang P, Ma L, Jin J, Zheng M, Pan L, Zhao Y, Sun X, Liu Y, Xing F (2019) The anti-aflatoxigenic mechanism of cinnamaldehyde in Aspergillus flavus. Sci Rep-UK 9(1):10499. https://doi.org/10.1038/s41598-019-47003-z
Wang Z, Hou J, Lu L, Qi Z, Sun J, Gao W, Meng J, Wang Y, Sun H, Gu H (2013) Small ribosomal protein subunit S7 suppresses ovarian tumorigenesis through regulation of the PI3K/AKT and MAPK pathways. PLoS One 8(11):e79117. https://doi.org/10.1371/journal.pone.0079117
Wu C, Zhang J, Wang M, Du G, Chen J (2012) Lactobacillus casei combats acid stress by maintaining cell membrane functionality. J Ind Microbiol Biot 39(7):1031–1039. https://doi.org/10.1007/s10295-012-1104-2
Xie Y, Cao Y, Zhang Y, Liu F, Xu H, Xiao X (2023) Synergistic antifungal properties of lauraldehyde and geraniol against Aspergillus flavus in pistachio. Food Control 2023:109915. https://doi.org/10.1016/j.foodcont.2023.109915
Xu D, Wei M, Peng S, Mo H, Huang L, Yao L, Hu L (2021a) Cuminaldehyde in cumin essential oils prevents the growth and aflatoxin B1 biosynthesis of Aspergillus flavus in peanuts. Food Control 125:107985. https://doi.org/10.1016/j.foodcont.2021.107985
Xu Y, Wei J, Wei Y, Han P, Dai K, Zou X, Jiang S, Xu F, Wang H, Sun J, Shao X (2021b) Tea tree oil controls brown rot in peaches by damaging the cell membrane of Monilinia fructicola. Postharvest Biol Tec 175:111474. https://doi.org/10.1016/j.postharvbio.2021.111474
Yang E, Hsieh Y, Chuang L (2021) Comparison of the phytochemical composition and antibacterial activities of the various extracts from leaves and twigs of Illicium verum. Molecules 26(13):3909. https://doi.org/10.3390/molecules26133909
Yang Q, Zhang X, Solairaj D, Fu Y, Zhang H (2023) Molecular response of Meyerozyma guilliermondii to patulin: transcriptomic-based analysis. J Fungi 9(5):538. https://doi.org/10.3390/jof9050538
Yutani M, Hashimoto Y, Ogita A, Kubo I, Tanaka T, Ki F (2011) Morphological changes of the filamentous fungus Mucor mucedo and inhibition of chitin synthase activity induced by anethole. Phytother Res 25(11):1707–1713. https://doi.org/10.1002/ptr.3579
Zamaraeva MV, Sabirov RZ, Maeno E, Ando-Akatsuka Y, Bessonova SV, Okada Y (2005) Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ 12(11):1390–1397. https://doi.org/10.1038/sj.cdd.4401661
Zhang S, Qin Y, Li S, Lv Y, Zhai H, Hu Y, Cai J (2021) Antifungal mechanism of 1-nonanol against Aspergillus flavus growth revealed by metabolomic analyses. Appl Microbiol Biot 105:7871–7888. https://doi.org/10.1007/s00253-021-11581-8
Zou X, Wei Y, Jiang S, Xu F, Wang H, Zhan P, Shao X (2022) ROS stress and cell membrane disruption are the main antifungal mechanisms of 2-phenylethanol against Botrytis cinerea. J Agric Food Chem 70(45):14468–14479. https://doi.org/10.1021/acs.jafc.2c06187
Acknowledgements
This work was supported by the National Natural Science Foundation of China (grant number 31772023), Scientific and Technological Research Project of Henan Province (grant number 212102110193), Natural Scientific Research Innovation Foundation of Henan University of Technology (grant number 2020ZKCJ01), Cultivation Programme for Young Backbone Teachers in Henan University of Technology, and Key Scientific and Technological Project of Education Department of Henan Province(grant number 23A210007).
Author information
Authors and Affiliations
Contributions
JDL: Experimentation, Writing-original draft, Investigation. QL: Software, Visualization. SBZ: Supervision, Data curation, Writing-review & editing, Resources. YYL: Software, Visualization. HCZ: Methodology, Conceptualization. SW: Software, Visualization. PAM: Software, Visualization. YSH: Visualization, Conceptualization, Validation.
Corresponding author
Ethics declarations
Ethical approval
This article does not contain studies conducted on human participants or animals by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lei, JD., Li, Q., Zhang, SB. et al. Transcriptomic and biochemical analyses revealed antifungal mechanism of trans-anethole on Aspergillus flavus growth. Appl Microbiol Biotechnol 107, 7213–7230 (2023). https://doi.org/10.1007/s00253-023-12791-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-023-12791-y