DOI QR코드

DOI QR Code

Antifungal Activity of an Endophytic Fungus Aspergillus versicolor DYSJ3 from Aphanamixis grandifolia Blume against Colletotrichum musae

  • Li, Xiaoyu (School of Life Sciences, Hainan University) ;
  • Wu, Yateng (School of Life Sciences, Hainan University) ;
  • Liu, Zhiqiang (School of Life Sciences, Hainan University)
  • Received : 2020.11.19
  • Accepted : 2021.09.02
  • Published : 2021.10.31

Abstract

An endophytic fungus strain DYSJ3 was isolated from a stem of Aphanamixis grandifolia Blume, which was identified as Aspergillus versicolor based on the morphological characteristics, internal transcribed spacer (ITS) and calmodulin gene sequences analyses. A. versicolor DYSJ3 exhibited strong antagonistic activity against Colletotrichum musae, C. gloeosporioides and Fusarium oxysporum f. sp. cubense with the inhibition rates of 61.9, 51.2 and 55.3% respectively. The antifungal metabolites mainly existed in the mycelium of A. versicolor DYSJ3, and its mycelial crude extract (CE) had broad-spectrum antifungal activities against plant pathogenic fungi. The CE had a good thermal stability, and the inhibition rate of 100 mg/mL CE against C. musae was above 70.0% after disposing at 120 ℃ for 1 h. Five secondary metabolites were isolated from the CE and identified as averufanin, ergosterol peroxide, versicolorin B, averythrin and sterigmatocystin. Activity evaluation showed versicolorin B exhibited inhibitory effects on the mycelial growth and conidial germination of C. musae, and sterigmatocystin had a weak inhibitory effect on the mycelial growth of C. musae.

Keywords

Acknowledgement

This work was financially supported by the Natural Science Foundation of Hainan Province [2019RC074] and the National Natural Science Foundation of China [31860480].

References

  1. Zhang R, He H, Di Y, et al. Chemical constituents from Aphanamixis grandifolia. Fitoterapia. 2014; 92:100-104. https://doi.org/10.1016/j.fitote.2013.10.014
  2. Zhang Y, Wang J, Gu Y, et al. Diverse prieurianin-type limonoid derivatives from the fruits of Aphanamixis grandifolia and their absolute configuration determination. Tetrahedron. 2014;70(37): 6594-6606. https://doi.org/10.1016/j.tet.2014.07.006
  3. Astulla A, Hirasawa Y, Rahman A, et al. Melidianolic acid a and B, new antimalarial acyclic diterpenes from Aphanamixis grandifolia. Nat Prod Commun. 2011;6:323-326.
  4. Yang SP, Chen HD, Liao SG, et al. Aphanamolide A, a new limonoid from Aphanamixis polystachya. Org Lett. 2011;13(1):150-153. https://doi.org/10.1021/ol102745h
  5. Zeng Q, Guan B, Ren J, et al. Aphanamgrandiol A, a new triterpenoid with a unique carbon skeleton from Aphanamixis grandifolia. Fitoterapia. 2013;86:217-221. https://doi.org/10.1016/j.fitote.2013.02.011
  6. Clay K, Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat. 2002;160(Suppl S4):S99-S127. https://doi.org/10.1086/342161
  7. Guo ZY, Tan MH, Liu CX, et al. Aspergoterpenins a(-)D: four new antimicrobial bisabolane sesquiterpenoid derivatives from an endophytic fungus Aspergillus versicolor. Molecules. 2018;23:1291. https://doi.org/10.3390/molecules23061291
  8. Deng M, Liu Y, Huang Y, et al. New bioactive secondary metabolites from the Anoectochilus roxburghii endophytic fungus Aspergillus versicolor. Fitoterapia. 2020;143:104532. https://doi.org/10.1016/j.fitote.2020.104532
  9. Cui H, Liu Y, Li T, et al. 3-Arylisoindolinone and sesquiterpene derivatives from the mangrove endophytic fungi Aspergillus versicolor SYSU-SKS025. Fitoterapia. 2018;124:177-181. https://doi.org/10.1016/j.fitote.2017.11.006
  10. Miao FP, Li XD, Liu XH, et al. Secondary metabolites from an algicolous Aspergillus versicolor strain. Mar Drugs. 2012;10(1):131-139. https://doi.org/10.3390/md10010131
  11. El-Gendy M, Yahya S, Hamed AR, et al. Phylogenetic analysis and biological evaluation of marine endophytic fungi derived from Red Sea sponge Hyrtios erectus. Appl Biochem Biotechnol. 2018;185(3):755-777. https://doi.org/10.1007/s12010-017-2679-x
  12. Williamson SM, Guzman M, Marin DH, et al. Evaluation of Pseudomonas syringae strain ESC-11 for biocontrol of crown rot and anthracnose of banana. Biol Control. 2008;46(3):279-286. https://doi.org/10.1016/j.biocontrol.2008.05.016
  13. Samson RA, Visagie CM, Houbraken J, et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol. 2014;78:141-173. https://doi.org/10.1016/j.simyco.2014.07.004
  14. Talbot NJ, Salch YP, Ma M, et al. Karyotypic variation within clonal lineages of the rice blast fungus, Magnaporthe grisea. Appl Environ Microbiol. 1993;59(2):585-593. https://doi.org/10.1128/aem.59.2.585-593.1993
  15. White TJ, Bruns T, Lee S, et al. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. (Innis MA, Gelfand DH, Shinsky TJ, White TJ, eds). Academic Press Inc, 1990. New York:315-322.
  16. Hong SB, Go SJ, Shin HD, et al. Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia. 2005;97(6):1316-1329. https://doi.org/10.1080/15572536.2006.11832738
  17. Jurjevic Z, Peterson SW, Horn BW. Aspergillus section Versicolores: nine new species and multilocus DNA sequence based phylogeny. IMA Fungus. 2012;3(1):59-79. https://doi.org/10.5598/imafungus.2012.03.01.07
  18. Sakai K, Ohte S, Ohshiro T, et al. Selective inhibition of acyl-CoA:cholesterol acyltransferase 2 isozyme by flavasperone and sterigmatocystin from Aspergillus species. J Antibiot. 2008;61(9):568-572. https://doi.org/10.1038/ja.2008.76
  19. Krzyczkowski W, Malinowska E, Suchocki P, et al. Isolation and quantitative determination of ergosterol peroxide in various edible mushroom species. Food Chem. 2009;113(1):351-355. https://doi.org/10.1016/j.foodchem.2008.06.075
  20. Hamasaki T, Hatsuda Y, Terasaima N, et al. Studies on the metabolites of Aspergillus versicolor (vuillemin) tiraboschi. Part V. Isolation and structures of three new metabolites, versicolorins A, B and C. Agric Biol Chem. 1967;31:11-17. https://doi.org/10.1271/bbb1961.31.11
  21. Birkinshaw JH, Roberts JC, Roffey P. Studies in mycological chemistry. Part XIX. "product B" (averantin) [1,3,6,8-tetrahydroxy-2-(1-hydroxyhexyl)anthraquinone], a pigment from Aspergillus versicolor (vuillemin) tiraboschi. J Chem Soc Perkin Trans. 1966;9:855-857.
  22. Lee YM, Li H, Hong J, et al. Bioactive metabolites from the sponge-derived fungus Aspergillus versicolor. Arch Pharm Res. 2010;33(2):231-235. https://doi.org/10.1007/s12272-010-0207-4
  23. Zhang H, Yuan C, Cao M, et al. New acyclic diterpenoids from the fruits of Aphanamixis grandifolia and structure revision of nemoralisin B. Phytochem Lett. 2014;8:81-85. https://doi.org/10.1016/j.phytol.2014.02.005
  24. Ye Y, Xia C, Yang J, et al. Isocoumarins from the fermentation products of an endophytic fungus of Aspergillus versicolor. Phytochem Lett. 2014;10: 215-218. https://doi.org/10.1016/j.phytol.2014.09.016
  25. Nakayama T. Biocontrol of powdery scab of potato by seed tuber application of an antagonistic fungus, Aspergillus versicolor, isolated from potato roots. J Gen Plant Pathol. 2017;83(4):253-263. https://doi.org/10.1007/s10327-017-0716-9
  26. Liu W, Wang L, Wang B, et al. Diketopiperazine and diphenylether derivatives from marine algae-derived Aspergillus versicolor OUCMDZ-2738 by epigenetic activation. Mar Drugs. 2018;17(1):6. https://doi.org/10.3390/md17010006
  27. Liu Z, Zhang K, Ke Z, et al. Optimisation of medium and culture conditions for the production of antifungal substances to Colletotrichum musae by Trametes elegans SR06. Biocontrol Sci Techn. 2016;26(11):1538-1551. https://doi.org/10.1080/09583157.2016.1218441
  28. Wang W, Chen R, Luo Z, et al. Antimicrobial activity and molecular docking studies of a novel anthraquinone from a marine-derived fungus Aspergillus versicolor. Nat Prod Res. 2018;32(5): 558-563. https://doi.org/10.1080/14786419.2017.1329732
  29. Zhou M, Miao MM, Du G, et al. Aspergillines A-E, highly oxygenated hexacyclic indole-tetrahydrofuran-tetramic acid derivatives from Aspergillus versicolor. Org Lett. 2014;16(19):5016-5019. https://doi.org/10.1021/ol502307u
  30. Salendra L, Luo X, Lin X, et al. Versispiroketal A, an unusual tetracyclic bridged spiroketal from the sponge-associated fungus Aspergillus versicolor SCSIO 41013. Org Biomol Chem. 2019;17(8): 2182-2186. https://doi.org/10.1039/c9ob00110g
  31. Li XB, Zhou YH, Zhu RX, et al. Identification and biological evaluation of secondary metabolites from the endolichenic fungus Aspergillus versicolor. Chem Biodivers. 2015;12(4):575-592. https://doi.org/10.1002/cbdv.201400146
  32. Wang M, Sun M, Hao H, et al. Avertoxins A-D, prenyl asteltoxin derivatives from Aspergillus versicolor Y10, an endophytic fungus of Huperzia serrata. J Nat Prod. 2015;78(12):3067-3070. https://doi.org/10.1021/acs.jnatprod.5b00600
  33. Hou XM, Zhang YH, Hai Y, et al. Aspersymmetide A, a new centrosymmetric cyclohexapeptide from the marine-derived fungus Aspergillus versicolor. Mar Drugs. 2017;15:363. https://doi.org/10.3390/md15110363
  34. Ozkaya FC, Ebrahim W, El-Neketi M, et al. Induction of new metabolites from sponge-associated fungus Aspergillus carneus by OSMAC approach. Fitoterapia. 2018;131:9-14. https://doi.org/10.1016/j.fitote.2018.10.008
  35. Liu K, Zheng Y, Miao C, et al. The antifungal metabolites obtained from the rhizospheric Aspergillus sp. YIM PH30001 against pathogenic fungi of Panax notoginseng. Nat Prod Res. 2014; 28(24):2334-2337. https://doi.org/10.1080/14786419.2014.935941
  36. Hu J, Li Z, Gao J, et al. New diketopiperazines from a marine-derived fungus strain Aspergillus versicolor MF180151. Mar Drugs. 2019;17:262. https://doi.org/10.3390/md17050262

Cited by

  1. Metabolites Produced by Fungi against Fungal Phytopathogens: Review, Implementation and Perspectives vol.11, pp.1, 2021, https://doi.org/10.3390/plants11010081