Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Diversity and Isolation of Endophytic Fungi in Panax japonicus and Biotransformation Activity on Saponins

Author(s): Pengfei Li, Xiaofeng Ling, Shujuan Zhao, Lili Xu* and Rufeng Wang*

Volume 25, Issue 9, 2024

Published on: 25 September, 2023

Page: [1199 - 1208] Pages: 10

DOI: 10.2174/0113892010247700230919053439

Price: $65

conference banner
Abstract

Objective: This study reports the diversity and community structure differences of the endophytic fungi of Panax japonicus of different ages to obtain novel endophytic fungi with glycoside hydrolytic activity for rare saponins production.

Methods: This study used the high-throughput sequencing method to analyze the diversity and community structure of endophytic fungi of P. japonicus. The endophytic fungi were processed by traditional isolation, culture, conservation, and ITS rDNA sequence analyses. Then the total saponins of P. japonicus were used as the substrate to evaluate the glycoside hydrolytic activity.

Results: The composition analysis of the community structure showed that the abundance, evenness, and diversity of endophytic fungi of nine-year-old P. japonicus were the best among all samples. A total of 210 endophytic fungi were isolated from P. japonicus samples and further annotated by sequencing the internal transcribed spacer. Then the biotransformation activity of obtained strains was further examined on total saponins of P. japonicus (TSPJ), with a strain identified as Fusarium equiseti (No.30) from 7-year-old P. japonicus showing significant glycoside hydrolytic activity on TSPJ, including ginsenoside Ro→zinglbroside R1, pseudoginsenoside RT1→pseudoginsenoside RP1, chikusetsusaponin IV→tarasaponin VI and chikusetsusaponin IVa →calenduloside E.

Conclusion: These results reveal the diversity and community structure differences of the endophytic fungi of P. japonicus with different ages and establish a resource library of endophytic fungi of P. japonicus. More importantly, we identified a valuable endophytic fungus with glycoside hydrolytic activity and provided a promising convenient microbial transformation approach to produce minor deglycosylated ginsenosides.

« Previous
Graphical Abstract

[1]
Shu, G.; Jiang, S.; Mu, J.; Yu, H.; Duan, H.; Deng, X. Antitumor immunostimulatory activity of polysaccharides from Panax japonicus C. A. Mey: Roles of their effects on CD4 + T cells and tumor associated macrophages. Int. J. Biol. Macromol., 2018, 111, 430-439.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.01.011] [PMID: 29317237]
[2]
He, H.; Xu, J.; Xu, Y.; Zhang, C.; Wang, H.; He, Y.; Wang, T.; Yuan, D. Cardioprotective effects of saponins from Panax japonicus on acute myocardial ischemia against oxidative stress-triggered damage and cardiac cell death in rats. J. Ethnopharmacol., 2012, 140(1), 73-82.
[http://dx.doi.org/10.1016/j.jep.2011.12.024] [PMID: 22226974]
[3]
Guo, X.; Ji, J.; Jose, K.S.G.S.; Hou, X.; Luo, Y.; Fu, X.; Mei, Z.; Feng, Z. Computational prediction of antiangiogenesis synergistic mechanisms of total saponins of Panax japonicus against rheumatoid arthritis. Front. Pharmacol., 2020, 11, 566129.
[http://dx.doi.org/10.3389/fphar.2020.566129] [PMID: 33324204]
[4]
Yang, W.; Hu, Y.; Wu, W.; Ye, M.; Guo, D. Saponins in the genus Panax L. (Araliaceae): A systematic review of their chemical diversity. Phytochemistry, 2014, 106, 7-24.
[http://dx.doi.org/10.1016/j.phytochem.2014.07.012] [PMID: 25108743]
[5]
Yamahara, J.; Kubomura, Y.; Miki, K.; Fujimura, H. Anti-ulcer action of Panax japonicus rhizome. J. Ethnopharmacol., 1987, 19(1), 95-101.
[http://dx.doi.org/10.1016/0378-8741(87)90141-3] [PMID: 3586698]
[6]
Yang, B.R.; Yuen, S.C.; Fan, G.Y.; Cong, W.H.; Leung, S.W.; Lee, S.M.Y. Identification of certain Panax species to be potential substitutes for Panax notoginseng in hemostatic treatments. Pharmacol. Res., 2018, 134, 1-15.
[http://dx.doi.org/10.1016/j.phrs.2018.05.005] [PMID: 29772270]
[7]
Sun, Q.; Sun, Q.; Liu, Y.; Sun, X.; Tao, H. Anti-apoptotic effect of hyperbaric oxygen preconditioning on a rat model of myocardial infarction. J. Surg. Res., 2011, 171(1), 41-46.
[http://dx.doi.org/10.1016/j.jss.2010.01.036] [PMID: 20421116]
[8]
Gao, Y.; Yuan, D.; Gai, L.; Wu, X.; Shi, Y.; He, Y.; Liu, C.; Zhang, C.; Zhou, G.; Yuan, C. Saponins from Panax japonicus ameliorate age-related renal fibrosis by inhibition of inflammation mediated by NF-κB and TGF-β1/Smad signaling and suppression of oxidative stress via activation of Nrf2-ARE signaling. J. Ginseng Res., 2021, 45(3), 408-419.
[http://dx.doi.org/10.1016/j.jgr.2020.08.005] [PMID: 34025134]
[9]
Yun, T.K. Brief introduction of Panax ginseng C.A. Meyer. J. Korean Med. Sci., 2001, 16, S3-S5.
[http://dx.doi.org/10.3346/jkms.2001.16.S.S3] [PMID: 11748372]
[10]
Xia, P.; Bai, Z.; Liang, T.; Yang, D.; Liang, Z.; Yan, X.; Liu, Y. High-performance liquid chromatography based chemical fingerprint analysis and chemometric approaches for the identification and distinction of three endangered Panax plants in Southeast Asia. J. Sep. Sci., 2016, 39(20), 3880-3888.
[http://dx.doi.org/10.1002/jssc.201600460] [PMID: 27550557]
[11]
Yoshizaki, K.; Devkota, H.P.; Fujino, H.; Yahara, S. Saponins composition of rhizomes, taproots, and lateral roots of Satsuma-ninjin (Panax japonicus). Chem. Pharm. Bull., 2013, 61(3), 344-350.
[http://dx.doi.org/10.1248/cpb.c12-00764] [PMID: 23291557]
[12]
Cui, L.; Wu, S.; Zhao, C.; Yin, C. Microbial conversion of major ginsenosides in ginseng total saponins by Platycodon grandiflorum endophytes. J. Ginseng Res., 2016, 40(4), 366-374.
[http://dx.doi.org/10.1016/j.jgr.2015.11.004] [PMID: 27746689]
[13]
Yang, W.; Zhou, J.; Harindintwali, J.D.; Yu, X. Production of minor ginsenosides by combining Stereum hirsutum and cellulase. PLoS One, 2021, 16(8), e0255899.
[http://dx.doi.org/10.1371/journal.pone.0255899] [PMID: 34358262]
[14]
Xu, H.L.; Chen, G.H.; Wu, Y.T.; Xie, L.P.; Tan, Z.B.; Liu, B.; Fan, H.J.; Chen, H.M.; Huang, G.Q.; Liu, M.; Zhou, Y.C. Ginsenoside Ro, an oleanolic saponin of Panax ginseng, exerts anti-inflammatory effect by direct inhibiting toll like receptor 4 signaling pathway. J. Ginseng Res., 2022, 46(1), 156-166.
[http://dx.doi.org/10.1016/j.jgr.2021.05.011] [PMID: 35058732]
[15]
Zhang, X.H.; Xu, X.X.; Xu, T. Ginsenoside Ro suppresses interleukin-1β-induced apoptosis and inflammation in rat chondrocytes by inhibiting NF-κB. Chin. J. Nat. Med., 2015, 13(4), 283-289.
[http://dx.doi.org/10.1016/S1875-5364(15)30015-7] [PMID: 25908625]
[16]
Zheng, S.; Xiao, S.; Wang, J.; Hou, W.; Wang, Y. Inhibitory effects of ginsenoside ro on the growth of B16F10 melanoma via its metabolites. Molecules, 2019, 24(16), 2985.
[http://dx.doi.org/10.3390/molecules24162985] [PMID: 31426477]
[17]
Li, W.N.; Fan, D.D. Biocatalytic strategies for the production of ginsenosides using glycosidase: Current state and perspectives. Appl. Microbiol. Biotechnol., 2020, 104(9), 3807-3823.
[http://dx.doi.org/10.1007/s00253-020-10455-9] [PMID: 32125478]
[18]
Kim, S.Y.; Lee, H.N.; Hong, S.J.; Kang, H.J.; Cho, J.Y.; Kim, D.; Ameer, K.; Kim, Y.M. Enhanced biotransformation of the minor ginsenosides in red ginseng extract by Penicillium decumbens β-glucosidase. Enzyme Microb. Technol., 2022, 153, 109941.
[http://dx.doi.org/10.1016/j.enzmictec.2021.109941] [PMID: 34785432]
[19]
Petrini, O.; Sieber, T.N.; Toti, L.; Viret, O. Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat. Toxins, 1993, 1(3), 185-196.
[http://dx.doi.org/10.1002/nt.2620010306] [PMID: 1344919]
[20]
Qin, J.C.; Zhang, Y.M.; Gao, J.M.; Bai, M.S.; Yang, S.X.; Laatsch, H.; Zhang, A.L. Bioactive metabolites produced by Chaetomium globosum, an endophytic fungus isolated from Ginkgo biloba. Bioorg. Med. Chem. Lett., 2009, 19(6), 1572-1574.
[http://dx.doi.org/10.1016/j.bmcl.2009.02.025] [PMID: 19246197]
[21]
Joshee, S.; Paulus, B.C.; Park, D.; Johnston, P.R. Diversity and distribution of fungal foliar endophytes in New Zealand Podocarpaceae. Mycol. Res., 2009, 113(9), 1003-1015.
[http://dx.doi.org/10.1016/j.mycres.2009.06.004] [PMID: 19539758]
[22]
Porras-Alfaro, A.; Bayman, P. Hidden fungi, emergent properties: Endophytes and microbiomes. Annu. Rev. Phytopathol., 2011, 49(1), 291-315.
[http://dx.doi.org/10.1146/annurev-phyto-080508-081831] [PMID: 19400639]
[23]
Zhao, J.; Shan, T.; Mou, Y.; Zhou, L. Plant-derived bioactive compounds produced by endophytic fungi. Mini Rev. Med. Chem., 2011, 11(2), 159-168.
[http://dx.doi.org/10.2174/138955711794519492] [PMID: 21222580]
[24]
Ren, C.G.; Dai, C.C. Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. BMC Plant Biol., 2012, 12(1), 128.
[http://dx.doi.org/10.1186/1471-2229-12-128] [PMID: 22856333]
[25]
Jia, M.; Chen, L.; Xin, H.L.; Zheng, C.J.; Rahman, K.; Han, T.; Qin, L.P. A friendly relationship between endophytic fungi and medicinal plants: A systematic review. Front. Microbiol., 2016, 7, 906.
[http://dx.doi.org/10.3389/fmicb.2016.00906] [PMID: 27375610]
[26]
Deshmukh, S.; Gupta, M.; Prakash, V.; Saxena, S. Endophytic fungi: A source of potential antifungal compounds. J. Fungi., 2018, 4(3), 77.
[http://dx.doi.org/10.3390/jof4030077] [PMID: 29941838]
[27]
Gupta, S.; Chaturvedi, P.; Kulkarni, M.G.; Van Staden, J. A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechnol. Adv., 2020, 39, 107462.
[http://dx.doi.org/10.1016/j.biotechadv.2019.107462] [PMID: 31669137]
[28]
Agusta, A.; Maehara, S.; Ohashi, K.; Simanjuntak, P.; Shibuya, H. Stereoselective oxidation at C-4 of flavans by the endophytic fungus Diaporthe sp. isolated from a tea plant. Chem. Pharm. Bull., 2005, 53(12), 1565-1569.
[http://dx.doi.org/10.1248/cpb.53.1565] [PMID: 16327190]
[29]
Shibuya, H.; Kitamura, C.; Maehara, S.; Nagahata, M.; Winarno, H.; Simanjuntak, P.; Kim, H.S.; Wataya, Y.; Ohashi, K. Transformation of Cinchona alkaloids into 1-N-oxide derivatives by endophytic Xylaria sp isolated from Cinchona pubescens. Chem. Pharm. Bull., 2003, 51(1), 71-74.
[http://dx.doi.org/10.1248/cpb.51.71] [PMID: 12520132]
[30]
Cheng, L.; Zhang, H.; Cui, H.; Davari, M.D.; Wei, B.; Wang, W.; Yuan, Q. Efficient enzyme-catalyzed production of diosgenin: Inspired by the biotransformation mechanisms of steroid saponins in Talaromyces stollii CLY-6. Green Chem., 2021, 23(16), 5896-5910.
[http://dx.doi.org/10.1039/D0GC04152A]
[31]
Luo, S.L.; Dang, L.Z.; Li, J.F.; Zou, C.G.; Zhang, K.Q.; Li, G.H. Biotransformation of saponins by endophytes isolated from Panax notoginseng. Chem. Biodivers., 2013, 10(11), 2021-2031.
[32]
Guo, C.L.; Yang, X.Y.; Chen, Z.M.; Wu, S.; Wang, C.X.; Huang, L.Q.; Cui, X.M. The content determination of biotransformation of Rb1 in the total saponins of Panax notoginseng by a plant endophyte Coniochaeta sp. Zhong Yao Cai, 2016, 39(5), 1075-1078.
[PMID: 30133192]
[33]
Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A.; Holmes, S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods, 2016, 13(7), 581-583.
[http://dx.doi.org/10.1038/nmeth.3869] [PMID: 27214047]
[34]
Bokulich, N.A.; Kaehler, B.D.; Rideout, J.R.; Dillon, M.; Bolyen, E.; Knight, R.; Huttley, G.A.; Gregory Caporaso, J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome, 2018, 6(1), 90.
[http://dx.doi.org/10.1186/s40168-018-0470-z] [PMID: 29773078]
[35]
Tan, G.; Hu, M.; Li, X.; Pan, Z.; Li, M.; Li, L.; Yang, M. High-throughput sequencing and metabolomics reveal differences in bacterial diversity and metabolites between red and white sufu. Front. Microbiol., 2020, 11, 758.
[http://dx.doi.org/10.3389/fmicb.2020.00758] [PMID: 32390991]
[36]
Han, Y.; Sun, B.; Hu, X.; Zhang, H.; Jiang, B.; Spranger, M.I.; Zhao, Y. Transformation of bioactive compounds by Fusarium sacchari fungus isolated from the soil-cultivated ginseng. J. Agric. Food Chem., 2007, 55(23), 9373-9379.
[http://dx.doi.org/10.1021/jf070354a] [PMID: 17935295]
[37]
Quan, L.H.; Jin, Y.; Wang, C.; Min, J.W.; Kim, Y.J.; Yang, D.C. Enzymatic transformation of the major ginsenoside Rb2 to minor compound Y and compound K by a ginsenoside-hydrolyzing β-glycosidase from Microbacterium esteraromaticum. J. Ind. Microbiol. Biotechnol., 2012, 39(10), 1557-1562.
[http://dx.doi.org/10.1007/s10295-012-1158-1] [PMID: 22717707]
[38]
Tian, Y.; Wang, S.; Shang, H.; Wang, W.Q.; Wang, B.Q.; Zhang, X.; Xu, X.D.; Sun, G.B.; Sun, X.B. The clickable activity-based probe of anti-apoptotic calenduloside E. Pharm. Biol., 2019, 57(1), 133-139.
[http://dx.doi.org/10.1080/13880209.2018.1557699] [PMID: 30843752]
[39]
Tian, Y.; Du, Y.Y.; Shang, H.; Wang, M.; Sun, Z.H.; Wang, B.Q.; Deng, D.; Wang, S.; Xu, X.D.; Sun, G.B.; Sun, X.B. Calenduloside E analogues protecting H9c2 cardiomyocytes against HO-induced apoptosis: Design, synthesis and biological evaluation. Front. Pharmacol., 2017, 8, 862-888.
[http://dx.doi.org/10.3389/fphar.2017.00862] [PMID: 29218010]
[40]
Li, L.; Wang, D.; Sun, C.; Li, Y.; Lu, H.; Wang, X. Comprehensive lipidome and metabolome profiling investigations of Panax quinquefolius and application in different growing regions using liquid chromatography coupled with mass spectrometry. J. Agric. Food Chem., 2021, 69(23), 6710-6719.
[http://dx.doi.org/10.1021/acs.jafc.1c02241] [PMID: 34080852]
[41]
Gómez, O.C.; Luiz, J.H.H. Endophytic fungi isolated from medicinal plants: Future prospects of bioactive natural products from Tabebuia/Handroanthus endophytes. Appl. Microbiol. Biotechnol., 2018, 102(21), 9105-9119.
[http://dx.doi.org/10.1007/s00253-018-9344-3] [PMID: 30203146]
[42]
Yan, L.; Zhao, H.; Zhao, X.; Xu, X.; Di, Y.; Jiang, C.; Shi, J.; Shao, D.; Huang, Q.; Yang, H.; Jin, M. Production of bioproducts by endophytic fungi: Chemical ecology, biotechnological applications, bottlenecks, and solutions. Appl. Microbiol. Biotechnol., 2018, 102(15), 6279-6298.
[http://dx.doi.org/10.1007/s00253-018-9101-7] [PMID: 29808328]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy