Inhibitory effects of hinokitiol on the development and pathogenicity of Colletotrichum gloeosporioides.
Antifungal activity
Colletotrichum gloeosporioides
Hinokitiol
Postharvest decay
Journal
World journal of microbiology & biotechnology
ISSN: 1573-0972
Titre abrégé: World J Microbiol Biotechnol
Pays: Germany
ID NLM: 9012472
Informations de publication
Date de publication:
25 Oct 2023
25 Oct 2023
Historique:
received:
19
07
2023
accepted:
16
10
2023
medline:
26
10
2023
pubmed:
25
10
2023
entrez:
25
10
2023
Statut:
epublish
Résumé
Postharvest anthracnose of mango fruit caused by Colletotrichum gloeosporioides is a devastating fungal disease, which causes tremendous quality deterioration and economic losses. Hinokitiol, an environmentally friendly natural compound, is effective in controlling a variety of postharvest fungal diseases. However, there is still a lack of research on the inhibitory effect of hinokitiol on C. gloeosporioides and its possible modes of action. In the present study, the activity of hinokitiol against C. gloeosporioides and its potential mechanisms involved have been investigated. We found that hinokitiol treatment could effectively inhibit the virulence of C. gloeosporioides to harvested mango fruit. After treatment with 8 mg/L hinokitiol, the mycelial growth of C. gloeosporioides was completely inhibited. When the concentration of hinokitiol reached 9 mg/L, the spore germination rate of C. gloeosporioides decreased to 2.43% after 9 h of cultivation. The inhibitory effect is mainly due to the attenuation in cell viability, and impairment in plasma membrane followed by leakage of cytoplasmic contents such as nucleic acids, proteins, and soluble carbohydrates, which ultimately leads to the destruction of cell structure. Furthermore, hinokitiol suppressed the expression of pathogenicity-related genes, leading to reduced infection activity. Collectively, these results suggest that hinokitiol may be an excellent bio-fungicides for the management of mango anthracnose.
Identifiants
pubmed: 37878063
doi: 10.1007/s11274-023-03810-1
pii: 10.1007/s11274-023-03810-1
doi:
Substances chimiques
beta-thujaplicin
U5335D6EBI
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
356Subventions
Organisme : National Natural Science Foundation of China
ID : 32202565
Organisme : Natural Science Foundation of Fujian Province
ID : 2022J05151
Organisme : Initial Research Fund of Jimei University
ID : ZQ2022011
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Alkan N, Friedlander G, Ment D, Prusky D, Fluhr R (2015) Simultaneous transcriptome analysis of Colletotrichum gloeosporioides and tomato fruit pathosystem reveals novel fungal pathogenicity and fruit defense strategies. New Phytol 205(2):801–815
pubmed: 25377514
doi: 10.1111/nph.13087
Cerioni L, Volentini SI, Prado FE, Rapisarda VA, Rodriguez-Montelongo L (2010) Cellular damage induced by a sequential oxidative treatment on Penicillium Digitatum. J Appl Microbiol 109(4):1441–1449
pubmed: 20553342
doi: 10.1111/j.1365-2672.2010.04775.x
Chaudhary PM, Tupe SG, Deshpande MV (2013) Chitin synthase inhibitors as antifungal agents. Mini-Rev Med Chem 13(2):222–236
pubmed: 22512590
Chen AW, Zeng GM, Chen GQ, Liu LL, Shang C, Hu XJ, Lu LH, Chen M, Zhou Y, Zhang QH (2014) Plasma membrane behavior, oxidative damage, and defense mechanism in Phanerochaete chrysosporium under cadmium stress. Process Biochem 49(4):589–598
doi: 10.1016/j.procbio.2014.01.014
Chiangsin R, Wanichkul K, Guest DI, Sangchote S (2016) Reduction of anthracnose on ripened mango fruits by chemicals, fruit bagging, and postharvest treatments. Australas Plant Path 45(6):629–635
doi: 10.1007/s13313-016-0456-x
Domon H, Hiyoshi T, Maekawa T, Yonezawa D, Tamura H, Kawabata S, Yanagihara K, Kimura O, Kunitomo E, Terao Y (2019) Antibacterial activity of hinokitiol against both antibiotic-resistant and -susceptible pathogenic bacteria that predominate in the oral cavity and upper airways. Microbiol Immunol 63(6):213–222
pubmed: 31106894
doi: 10.1111/1348-0421.12688
Gao XS, Wang QN, Feng QD, Zhang BB, He CZ, Luo HL, An B (2022) Heat shock transcription factor CgHSF1 is required for melanin biosynthesis, appressorium formation, and pathogenicity in Colletotrichum gloeosporioides. J Fungi (Basel) 8(2):175
pubmed: 35205929
doi: 10.3390/jof8020175
Guo H, Qiao B, Ji X, Wang X, Zhu E (2020) Antifungal activity and possible mechanisms of submicron chitosan dispersions against Alteraria alternata. Postharvest Biol Tec 161:110883
doi: 10.1016/j.postharvbio.2019.04.009
He C, Zhang ZQ, Li BQ, Xu Y, Tian SP (2019) Effect of natamycin on Botrytis Cinerea and Penicillium expansum-postharvest pathogens of grape berries and jujube fruit. Postharvest Biol Tec 151:134–141
doi: 10.1016/j.postharvbio.2019.02.009
Ji D, Chen T, Ma D, Liu J, Xu Y, Tian S (2018) Inhibitory effects of methyl thujate on mycelial growth of Botrytis Cinerea and possible mechanisms. Postharvest Biol Tec 142:46–54
doi: 10.1016/j.postharvbio.2018.04.003
Jian YQ, Li Y, Tang GT, Zheng XJ, Khaskheli MI, Gong GS (2021) Identification of Colletotrichum species associated with anthracnose Disease of strawberry in Sichuan province, China. Plant Dis 105:3205–3036
doi: 10.1094/PDIS-10-20-2114-RE
Jin XY, Zhang M, Lu JH, Duan XM, Chen JY, Liu Y, Chang WQ, Lou HX (2021) Hinokitiol chelates intracellular iron to retard fungal growth by disturbing mitochondrial respiration. J Adv Res 34:65–77
pubmed: 35024181
pmcid: 8655124
doi: 10.1016/j.jare.2021.06.016
Kim DJ, Lee MW, Choi JS, Lee SG, Park JY, Kim SW (2017) Inhibitory activity of hinokitiol against biofilm formation in fluconazoleresistant Candida species. PLoS ONE 12:e0171244
pubmed: 28152096
pmcid: 5289548
doi: 10.1371/journal.pone.0171244
Kong WL, Rui L, Ni H, Wu XQ (2020) Antifungal effects of volatile organic compounds produced by Rahnella aquatilis JZ-GX1 against Colletotrichum gloeosporioides in Liriodendron chinense x tulipifera. Front Microbiol 11:1114
pubmed: 32547526
pmcid: 7271530
doi: 10.3389/fmicb.2020.01114
Lin S, Taylor NJ, Hand FP (2018) Identification and characterization of fungal pathogens causing fruit rot of deciduous holly. Plant Dis 102:2430–2445
pubmed: 30253114
doi: 10.1094/PDIS-02-18-0372-RE
Liu Q, Kong WL, Hu SJ, Kang YC, Zhang YT, Ng TB (2020a) Effects of Oudemansiella radicata polysaccharide on postharvest quality of oyster mushroom (Pleurotus Ostreatus) and its antifungal activity against Penicillium Digitatum. Postharvest Biol Tec 166:111207
doi: 10.1016/j.postharvbio.2020.111207
Liu XY, Li JK, Cui XM, Ji DC, Xu Y, Chen T, Tian SP (2020b) Exogenous bamboo pyroligneous acid improves antioxidant capacity and primes defense responses of harvested apple fruit. LWT-Food Sci Technol 134:110191
doi: 10.1016/j.lwt.2020.110191
Ma DY, Ji DC, Zhang ZQ, Li BQ, Qin GZ, Xu Y, Chen T, Tian SP (2019) Efficacy of rapamycin in modulating autophagic activity of Botrytis Cinerea for controlling gray mold. Postharvest Biol Tec 150:158–165
doi: 10.1016/j.postharvbio.2019.01.005
Meng FY, Liu X, Li C, Peng XD, Wang Q, Xu Q, Sui JL, Zhao GQ, Lin J (2023) Hinokitiol inhibits aspergillus fumigatus by interfering with the cell membrane and cell wall. Front Microbiol 14:1132042
pubmed: 37113218
pmcid: 10128913
doi: 10.3389/fmicb.2023.1132042
Muller C, Staudacher V, Krauss J, Giera M, Bracher F (2013) A convenient cellular assay for the identification of the molecular target of ergosterol biosynthesis inhibitors and quantification of their effects on total ergosterol biosynthesis. Steroids 78(5):483–493
pubmed: 23454215
doi: 10.1016/j.steroids.2013.02.006
Ni YJ, Huang ZN, Li HY, Lee CC, Tyan YC, Yang MH, Pangilinan CR, Wu LH, Chiang YC, Lee CH (2022) Hinokitiol impedes Tumor drug resistance by suppressing protein kinase B/mammalian targets of rapamycin axis. J Cancer 13(6):1725–1733
pubmed: 35399709
pmcid: 8990411
doi: 10.7150/jca.69449
Noar RD, Thomas E, Daub ME (2019) A novel polyketide synthase gene cluster in the plant pathogenic fungus pseudocercospora fijiensis. PLoS ONE 14(2):e0212229
pubmed: 30735556
pmcid: 6368318
doi: 10.1371/journal.pone.0212229
Nosanchuk JD, Casadevall A (2006) Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob Agents Chemother 50(11):3519–3528
pubmed: 17065617
pmcid: 1635213
doi: 10.1128/AAC.00545-06
Pereira EDJ, Panek AD, Eleutherio ECA (2003) Protection against oxidation during dehydration of yeast. Cell Stress Chaperon 8(2):120–124
doi: 10.1379/1466-1268(2003)008<0120:PAODDO>2.0.CO;2
Perumal AB, Sellamuthu PS, Nambiar RB, Sadiku ER (2016) Antifungal activity of five different essential oils in vapour phase for the control of Colletotrichum gloeosporioides and Lasiodiplodia theobromae in vitro and on mango. INT J Food Sci Tech 51(2):411–418
doi: 10.1111/ijfs.12991
Qiao Y, Xu L, Xu G, Cao Y, Gao Y, Wang Y, Feng J (2022) Efficacy and potential mechanism of hinokitiol against postharvest anthracnose of banana caused by Colletotrichum musae. LWT-Food Sci Technol 161:113334
doi: 10.1016/j.lwt.2022.113334
Rezende DC, Fialho MB, Brand SC, Blumer S, Pascholati SF (2015) Antimicrobial activity of volatile organic compounds and their effect on lipid peroxidation and electrolyte loss in Colletotrichum gloeosporioides and Colletotrichum Acutatum Mycelia. Afr J Microbiol Res 9(23):1527–1535
doi: 10.5897/AJMR2015.7425
Shi XQ, Li BQ, Qin GZ, Tian SP (2012) Mechanism of antifungal action of borate against Colletotrichum gloeosporioides related to mitochondrial degradation in spores. Postharvest Biol Tec 67:138–143
doi: 10.1016/j.postharvbio.2012.01.003
Tang LH, Mo JY, Guo TX, Huang SP, Li QL, Ning P, Hsiang T (2020) In vitro antifungal activity of dimethyl trisulfide against Colletotrichum gloeosporioides from mango. World J Microbiol Biotechnol 36(1):4
doi: 10.1007/s11274-019-2781-z
Vanitha T, Thammawong M, Umehara H, Nakamura N, Shiina T (2019) Effect of hinokitiol impregnated sheets on shelf life and quality of KEK-1 tomatoes during storage. Packag Technol Sci 32(12):641–648
doi: 10.1002/pts.2479
Wang WK, Lu MF, Kuan YD, Lee CH (2015) The treatment of mouse Colorectal cancer by oral delivery tumor-targeting Salmonella. Am J Cancer Res 5(7):2222–2228
pubmed: 26328252
pmcid: 4548333
Wang HQ, Fan K, Li DW, Han CM, Qu YY, Qi YK, Wu XQ (2020a) Identification, virulence and fungicide sensitivity of Colletotrichum gloeosporioides s.s. responsible for walnut anthracnose Disease in China. Plant Dis 104:1358–1368
pubmed: 32196416
doi: 10.1094/PDIS-12-19-2569-RE
Wang Y, Liu XY, Chen T, Xu Y, Tian SP (2020b) Antifungal effects of hinokitiol on development of Botrytis Cinerea in vitro and in vivo. Postharvest Biol Tec 159:111038
doi: 10.1016/j.postharvbio.2019.111038
Wang CW, Duan TK, Shi LX, Zhang XQ, Fan WX, Wang MQ, Wang JM, Ren L, Zhao XJ, Wang Y (2022) Characterization of volatile organic compounds produced by Bacillus siamensis YJ15 and their antifungal activity against Botrytis Cinerea. Plant Dis 106(9):2321–2329
pubmed: 35380464
doi: 10.1094/PDIS-01-22-0230-RE
Wang YQ, Wu XX, Lu YQ, Fu HM, Liu SQ, Zhao J, Long CA (2023) Ferric chloride controls citrus anthracnose by inducing the autophagy activity of Colletotrichum gloeosporioides. J Fungi (Basel) 9(2):230
pubmed: 36836344
pmcid: 9962583
doi: 10.3390/jof9020230
Wu Y, Cheng JH, Sun DW (2022) Subcellular damages of Colletotrichum asianum and inhibition of mango anthracnose by dielectric barrier discharge plasma. Food Chem 381:132197
pubmed: 35121319
doi: 10.1016/j.foodchem.2022.132197
Xu XB, Lei HH, Ma XY, Lai TF, Song HM, Shi XQ, Li JK (2017) Antifungal activity of 1-methylcyclopropene (1-MCP) against anthracnose (Colletotrichum gloeosporioides) in postharvest mango fruit and its possible mechanisms of action. Int J Food Microbiol 241:1–6
pubmed: 27728853
doi: 10.1016/j.ijfoodmicro.2016.10.002
Xu HF, Wang GF, Zhang J, Zhang MJ, Fu MR, Xiang K, Zhang MY, Chen X (2022) Identification of phenolic compounds and active antifungal ingredients of walnut in response to anthracnose (Colletotrichum gloeosporioides). Postharvest Biol Tec 192:112019
doi: 10.1016/j.postharvbio.2022.112019
Ye HC, Wang Q, Zhu FD, Feng G, Yan C, Zhang J (2020) Antifungal activity of alpha-mangostin against Colletotrichum gloeosporioides in vitro and in vivo. Molecules 25:22
doi: 10.3390/molecules25225335
Yong HY, Bakar FDA, Illias RM, Mahadi NM, Murad AMA (2013) Cgl-SLT2 is required for appressorium formation, sporulation and pathogenicity in Colletotrichum gloeosporioides. Braz J Microbiol 44(4):1241–1250
pubmed: 24688518
doi: 10.1590/S1517-83822013000400031
Zhao XZ, Tang BZ, Xu J, Wang N, Zhou ZS, Zhang JX (2020) A SET domain-containing protein involved in cell wall integrity signaling and peroxisome biogenesis is essential for appressorium formation and pathogenicity of Colletotrichum gloeosporioides. Fungal Genet Biol 145:103474
pubmed: 33007450
doi: 10.1016/j.fgb.2020.103474