Abstract
Botrytis cinerea is a highly destructive and widespread phytopathogen in fruits. The widespread use of chemical antifungal agents on fruits has aided in disease control while their long-term use has resulted in the emergence of resistant fungal strains. Flavonoids have a specific antifungal effect. The inhibitory effect and underlying mechanism of flavonoids from Sedum aizoon L. (FSAL) on B. cinerea were determined in this study. The results showed that the minimum inhibitory concentration of FSAL against B. cinerea was 1.500 mg/mL. FSAL treatment caused leakage of macromolecules such as nucleic acids, led to accumulation of malondialdehyde and relative oxygen species, and disrupted the ultrastructure of B. cinerea. The transcriptome results indicated that compared with the control group, there were 782 and 1330 genes identified as being substantially upregulated and downregulated, respectively, in the FSAL-treated group. The identified genes and metabolites were mostly involved in redox processes and glycerolipid and amino acid metabolism pathways. FSAL offer a promising choice for food prevention and safety.
Key points
• FSAL negatively affects the glycerolipid metabolism of B. cinerea
• FSAL minimum inhibitory concentration against B. cinerea was 1.500 mg/mL
• FSAL could be utilized as a new prevention strategy for gray mold in fruits
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The data sets generated and/or analyzed during this study can be reasonably requested from the corresponding authors.
References
Alsharairi NA (2021) Scutellaria baicalensis and their natural flavone compounds as potential medicinal drugs for the treatment of nicotine-induced non-small-cell lung cancer and asthma. Int J Environ Res Public Health 18:5243. https://doi.org/10.3390/ijerph18105243
Aminifard MH, Mohammadi S (2013) Essential oils to control Botrytis cinerea in vitro and in vivo on plum fruits. J Sci Food Agric 93(2):348–353. https://doi.org/10.1002/jsfa.5765
Athenstaedt K (2021) Phosphatidic acid biosynthesis in the model organism yeast Saccharomyces cerevisiae - a survey. BBA-Mol Cell Biol L 1866(6):158907. https://doi.org/10.1016/j.bbalip.2021.158907
Benghezal M, Roubaty C, Veepuri V, Knudsen J, Conzelmann A (2007) SLC1 and SLC4 encode partially redundant acyl-coenzyme A 1-acylglycerol-3-phosphate O-acyltransferases of budding yeast. J Biol Chem 282(42):30845–30855. https://doi.org/10.1074/jbc.M702719200
Cui H, Zhang C, Li C, Lin L (2019) Antibacterial mechanism of oregano essential oil. Ind Crops Prod 139:111498. https://doi.org/10.1016/j.indcrop.2019.111498
Cui X, Ma D, Liu X, Zhang Z, Li B, Xu Y, Chen T, Tian S (2021) Magnolol inhibits gray mold on postharvest fruit by inducing autophagic activity of Botrytis cinerea. Postharvest Biol Tec 180:111596. https://doi.org/10.1016/j.postharvbio.2021.111596
Da X, Nishiyama Y, Tie D, Hein KZ, Yamamoto O, Morita E (2019) Antifungal activity and mechanism of action of Ou-gon (Scutellaria root extract) components against pathogenic fungi. Sci Rep 9:1683. https://doi.org/10.1038/s41598-019-38916-w
Das MR, Sarma RK, Borah S, Kumari R, Saikia R, Deshmukh AB, Shelke MV, Sengupta P, Szunerits S, Boukherroub R (2013) The synthesis of citrate-modified silver nanoparticles in an aqueous suspension of graphene oxide nanosheets and their antibacterial activity. Colloids Surf B 105:128–136. https://doi.org/10.1016/j.colsurfb.2012.12.033
Gioti A, Simon A, Pêcheur PL, Giraud C, Pradier JM, Viaud M, Levis C (2006) Expression profiling of Botrytis cinerea genes identifies three patterns of up-regulation in planta and an FKBP12 protein affecting pathogenicity. J Mol Biol 358(2):372–386. https://doi.org/10.1016/j.jmb.2006.01.076
Huang X, You Z, Luo Y, Yang C, Ren J, Liu Y, Wei G, Dong P, Ren M (2021) Antifungal activity of chitosan against Phytophthora infestans, the pathogen of potato late blight. Int J Biol Macromol 166:1365–1376. https://doi.org/10.1016/j.ijbiomac.2020.11.016
Li Z, Shao X, Wei Y, Dai K, Xu J, Xu F, Wang H (2020) Transcriptome analysis of Botrytis cinerea in response to tea tree oil and its two characteristic components. Appl Microbiol Biotechnol 104(5):2163–2178. https://doi.org/10.1007/s00253-020-10382-9
Liu G, Ren G, Zhao L, Cheng L, Wang C, Sun B (2017) Antibacterial activity and mechanism of bifidocin A against Listeria monocytogenes. Food Control 73:854–861. https://doi.org/10.1016/j.foodcont.2016.09.036
Low WL, Martin C, Hill DJ, Kenward MA (2011) Antimicrobial efficacy of silver ions in combination with tea tree oil against Pseudomonas aeruginosa, Staphylococcus aureus and Candida albicans. Int J Antimicrob Agents 37:162–165. https://doi.org/10.1016/j.ijantimicag.2010.10.015
Luo J, Xu F, Zhang X, Shao X, Wei Y, Wang H (2020) Transcriptome analysis of Penicillium italicum in response to the flavonoids from Sedum aizoon L. World J Microbiol Biotechnol 36:62. https://doi.org/10.1007/s11274-020-02836-z
Ma D, Ji D, Zhang Z, Li B, Qin G, Xu Y, Chen T, Tian S (2019) Efficacy of rapamycin in modulating autophagic activity of Botrytis cinerea for controlling gray mold. Postharvest Biol Tec 150:158–165. https://doi.org/10.1016/j.postharvbio.2019.01.005
Manrique JA, Santana CW (2008) Flavonoids, antibacterial and antioxidant activities of propolis of stingless bees, Melipona quadrifasciata, Melipona compressipes, Tetragonisca angustula, and Nannotrigona sp. from Brazil and Venezuela. Zootecnia Tropical 26(2):157–166
Martos GI, Minahk CJ, Font G, de Valdez MR (2007) Effects of protective agents on membrane fluidity of freeze-dried Lactobacillus delbrueckii ssp. bulgaricus. Lett Appl Microbiol 45:282–288. https://doi.org/10.1111/j.1472-765X.2007.02188.x
Nunes CA (2011) Biological control of postharvest diseases of fruit. Eur J Plant Pathol 133:181–196. https://doi.org/10.1007/s10658-011-9919-7
Pedrotti C, Marcon AR, Longaray Delamare AP, Echeverrigaray S, da Silva Ribeiro RT, Schwambach J (2019) Alternative control of grape rots by essential oils of two Eucalyptus species. J Sci Food Agric 99:6552–6561. https://doi.org/10.1002/jsfa.9936
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Sanchez E, Garcia S, Heredia N (2010) Extracts of edible and medicinal plants damage membranes of Vibrio cholerae. Appl Environ Microbiol 76:6888–6894. https://doi.org/10.1128/AEM.03052-09
Sant DG, Tupe SG, Ramana CV, Deshpande MV (2016) Fungal cell membrane-promising drug target for antifungal therapy. J Appl Microbiol 121:1498–1510. https://doi.org/10.1111/jam.13301
Tamaki H, Shimada A, Ito Y, Ohya M, Takase J, Miyashita M, Miyagawa H, Nozaki H, Nakayama R, Kumagai H (2007) LPT1 encodes a membrane-bound O-acyltransferase involved in the acylation of lysophospholipids in the yeast Saccharomyces cerevisiae. J Biol Chem 282(47):34288–34298. https://doi.org/10.1074/jbc.M704509200
Wang J, Chi Z, Zhao K, Wang H, Zhang X, Xu F, Shao X, Wei Y (2020) A transcriptome analysis of the antibacterial mechanism of flavonoids from Sedum aizoon L. against Shewanella putrefaciens. World J Microbiol Biotechnol 36:94. https://doi.org/10.1007/s11274-020-02871-w
Wang J, Xia X, Wang H, Li P, Wang K (2013) Inhibitory effect of lactoferrin against gray mould on tomato plants caused by Botrytis cinerea and possible mechanisms of action. Int J Food Microbiol 161:151–157. https://doi.org/10.1016/j.ijfoodmicro.2012.11.025
Wang Y, Zhai J, Qi Z, Liu W, Cui J, Zhang X, Bai S, Li L, Shui G, Cui S (2022) The specific glycerolipid composition is responsible for maintaining the membrane stability of Physcomitrella patens under dehydration stress. J Plant Physiol 268:153590. https://doi.org/10.1016/j.jplph.2021.153590
Xu F, Wang C, Wang H, Xiong Q, Wei Y, Shao X (2018) Antimicrobial action of flavonoids from Sedum aizoon L. against lactic acid bacteria in vitro and in refrigerated fresh pork meat. J Funct Foods 40:744–750. https://doi.org/10.1016/j.jff.2017.09.030
Xu J, Shao X, Li Y, Wei Y, Xu F, Wang H (2017) Metabolomic analysis and mode of action of metabolites of tea tree oil involved in the suppression of Botrytis cinerea. Front Microbiol 8:1017. https://doi.org/10.3389/fmicb.2017.01017
Xu L, Feng L, Sun J, Mao L, Li X, Jiang Y, Duan X, Li T (2022) Antifungal activities of a natural trisaccharide ester against sour rot in mandarin fruit. Postharvest Biol Tec 191:111981. https://doi.org/10.1016/j.postharvbio.2022.111981
Xu T, Wang Z, Lei T, Lv C, Wang J, Lu J (2015) New flavonoid glycosides from Sedum aizoon L. Fitoterapia 101:125–132. https://doi.org/10.1016/j.fitote.2014.12.014
Yıldırım MA, Goh KI, Cusick M, Barabási AL, Vidal M (2007) Drug-target network. Nat Biotechnol 25:1119–1126. https://doi.org/10.1038/nbt1338
Yin H, Xu L, Poter NA (2011) Free radical lipid peroxidation: mechanisms and analysis. Chem Rev 111(10):5944–5972. https://doi.org/10.1021/cr200084z
Zambounis A, Ganopoulos I, Valasiadis D, Karapetsi L, Madesis P (2020) RNA sequencing-based transcriptome analysis of kiwifruit infected by Botrytis cinerea. Physiol Mol Plant P 111:101514. https://doi.org/10.1016/j.pmpp.2020.101514
Zhao L, He F, Li B, Gu X, Zhang X, Dhanasekaran S, Zhang H (2022) Transcriptomic analysis of the mechanisms involved in enhanced antagonistic efficacy of Meyerozyma guilliermondii by methyl jasmonate and disease resistance of postharvest apples. LWT 160:113323. https://doi.org/10.1016/j.lwt.2022.113323
Zuo X, Li S, Hall J, Mattern MR, Tran H, Shoo J, Tan RB, Weiss SR, Butt TR (2005) Enhanced expression and purification of membrane proteins by SUMO fusion in Escherichia coli. J Struct Funct Genomics 6:103–111. https://doi.org/10.1007/s10969-005-2664-4
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This research was supported through funding from the Public Welfare Applied Research Project of Ningbo City (2022S138 and 2022S154) and Student Research and Innovation Programme of Ningbo University (2021SRIP3607).
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KYW: investigation, formal analysis and writing-original draft. XZ: methodology. XFS: writing—review and editing. YYW: data curation. FX: resources, validation and visualization. HFW: conceptualization, supervision, and project administration.
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Wang, K., Zhang, X., Shao, X. et al. Flavonoids from Sedum aizoon L. inhibit Botrytis cinerea by negatively affecting cell membrane lipid metabolism. Appl Microbiol Biotechnol 106, 7139–7151 (2022). https://doi.org/10.1007/s00253-022-12196-3
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DOI: https://doi.org/10.1007/s00253-022-12196-3