Fungal endophytes of Taxus species and regulatory effect of two strains on taxol synthesis.
Taxus
Correlation analysis
Diversity
Endophytic fungi
ITS sequencing
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
03 Aug 2024
03 Aug 2024
Historique:
received:
06
04
2024
accepted:
26
07
2024
medline:
4
8
2024
pubmed:
4
8
2024
entrez:
3
8
2024
Statut:
epublish
Résumé
Taxol, derived from Taxus trees, is a valuable natural resource for the development of anticancer drugs. Endophytic fungi from Taxus trees are a promising alternative source of Taxol. However, the impact of plant-endophytic microbial interaction on the host's Taxol biosynthesis is largely unknown. In the current study, the diversity of endophytic fungi in three different Taxus species was analyzed using Internal Transcribed Spacer sequencing. A total of 271 Operational Taxonomic Units (OTUs) were identified, grouping into 2 phyla, 8 classes, 16 orders, 19 families, and 19 genera. Alpha and beta diversity analysis indicated significant differences in endophytic fungal communities among the various Taxus trees. At the genus level, Alternaria and Davidiella were predominantly found in T. mairei and T. media, respectively. By utilizing a previously published dataset, a Pearson correlation analysis was conducted to predict the taxol biosynthesis-related fungal genera. Following screening, two isolates of Alternaria (L7 and M14) were obtained. Effect of inoculation with Alternaria isolates on the gene expression and metabolite accumulation of T. mairei was determined by transcriptomic and untargeted metabolomic studies. The co-inoculation assay suggests that the two Alternaria isolates may have a negative regulatory effect on taxol biosynthesis by influencing hormone signaling pathways. Our findings will serve as a foundation for advancing the production and utilization of Taxus and will also aid in screening endophytic fungi related to taxol production.
Sections du résumé
BACKGROUND
BACKGROUND
Taxol, derived from Taxus trees, is a valuable natural resource for the development of anticancer drugs. Endophytic fungi from Taxus trees are a promising alternative source of Taxol. However, the impact of plant-endophytic microbial interaction on the host's Taxol biosynthesis is largely unknown.
RESULTS
RESULTS
In the current study, the diversity of endophytic fungi in three different Taxus species was analyzed using Internal Transcribed Spacer sequencing. A total of 271 Operational Taxonomic Units (OTUs) were identified, grouping into 2 phyla, 8 classes, 16 orders, 19 families, and 19 genera. Alpha and beta diversity analysis indicated significant differences in endophytic fungal communities among the various Taxus trees. At the genus level, Alternaria and Davidiella were predominantly found in T. mairei and T. media, respectively. By utilizing a previously published dataset, a Pearson correlation analysis was conducted to predict the taxol biosynthesis-related fungal genera. Following screening, two isolates of Alternaria (L7 and M14) were obtained. Effect of inoculation with Alternaria isolates on the gene expression and metabolite accumulation of T. mairei was determined by transcriptomic and untargeted metabolomic studies. The co-inoculation assay suggests that the two Alternaria isolates may have a negative regulatory effect on taxol biosynthesis by influencing hormone signaling pathways.
CONCLUSION
CONCLUSIONS
Our findings will serve as a foundation for advancing the production and utilization of Taxus and will also aid in screening endophytic fungi related to taxol production.
Identifiants
pubmed: 39097685
doi: 10.1186/s12866-024-03445-8
pii: 10.1186/s12866-024-03445-8
doi:
Substances chimiques
Paclitaxel
P88XT4IS4D
DNA, Fungal
0
DNA, Ribosomal Spacer
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
291Subventions
Organisme : Postgraduate Research Innovation Project, Hangzhou Normal University
ID : 2022HSDYJSKY217
Organisme : Science and Technology Innovation Activity Plan (New Talent Plan) of Zhejiang Province
ID : 2023R445029
Organisme : National Natural Science Foundation of China
ID : 32271905
Organisme : Zhejiang Provincial Natural Science Foundation of China
ID : LY23C160001
Informations de copyright
© 2024. The Author(s).
Références
Yu C, Huang J, Wu Q, Zhang C, Li XL, Xu X, Feng S, Zhan X, Chen Z, Wang H, et al. Role of female-predominant MYB39-bHLH13 complex in sexually dimorphic accumulation of taxol in Taxus media. Hortic Res. 2022;9:uhac062.
pubmed: 35769613
pmcid: 9233167
doi: 10.1093/hr/uhac062
Zhan X, Zang Y, Ma R, Lin W, Li XL, Pei Y, Shen C, Jiang Y. Mass Spectrometry-imaging analysis of active ingredients in the leaves of Taxus cuspidata. ACS Omega. 2024;9(16):18634–42.
pubmed: 38680336
pmcid: 11044248
doi: 10.1021/acsomega.4c01440
Shao F, Wilson IW, Qiu D. The research progress of Taxol in Taxus. Curr Pharm Biotechnol. 2021;22(3):360–6.
pubmed: 32564747
doi: 10.2174/18734316MTA3oNTEc1
Yu C, Hou K, Zhang H, Liang X, Chen C, Wang Z, Wu Q, Chen G, He J, Bai E, et al. Integrated mass spectrometry imaging and single-cell transcriptome atlas strategies provide novel insights into taxoid biosynthesis and transport in Taxus mairei stems. Plant J. 2023;115(5):1243–60.
pubmed: 37219365
doi: 10.1111/tpj.16315
Qiao X, Zhang J, Wang Z, Xu Y, Zhou T, Mi X, Cao M, Ye W, Jin G, Hao Z, et al. Foundation species across a latitudinal gradient in China. Ecology. 2021;102(2):e03234.
pubmed: 33107020
doi: 10.1002/ecy.3234
Long T, Wu X, Wang Y, Chen J, Xu C, Li J, Li J, Zang R. The population status and threats of Taxus cuspidata, a plant species with extremely small populations in China. Global Ecol Conserv. 2021;26:e01495.
doi: 10.1016/j.gecco.2021.e01495
Zhan X, Qiu T, Zhang H, Kailin H, Liang X, Chen C, Wang Z, Wu Q, Wang X, Li XL et al. Mass spectrometry imaging and single-cell transcriptional profiling reveal the tissue-specific regulation of bioactive ingredient biosynthesis in Taxus leaves. Plant Commun 2023:100630.
Feng S, Kailin H, Zhang H, Chen C, Huang J, Wu Q, Zhang Z, Gao Y, Wu X, Wang H, et al. Investigation of the role of TmMYB16/123 and their targets (TmMTP1/11) in the tolerance of Taxus media to cadmium. Tree Physiol. 2023;43(6):1009–22.
pubmed: 36808461
doi: 10.1093/treephys/tpad019
Saloustros E, Mavroudis D, Georgoulias V. Paclitaxel and Docetaxel in the treatment of breast cancer. Expert Opin Pharmacother. 2008;9(15):2603–16.
pubmed: 18803448
doi: 10.1517/14656566.9.15.2603
Yang YH, Mao JW, Tan XL. Research progress on the source, production, and anti-cancer mechanisms of paclitaxel. Chin J Nat Med. 2020;18(12):890–7.
pubmed: 33357719
Malhadas C, Malheiro R, Pereira JA, de Pinho PG, Baptista P. Antimicrobial activity of endophytic fungi from olive tree leaves. World J Microbiol Biotechnol. 2017;33(3):46.
pubmed: 28168624
doi: 10.1007/s11274-017-2216-7
Zhan X, Chen Z, Chen R, Shen C. Environmental and genetic factors involved in plant protection-associated secondary metabolite biosynthesis pathways. Front Plant Sci. 2022;13:877304.
pubmed: 35463424
pmcid: 9024250
doi: 10.3389/fpls.2022.877304
Tian Y, Amand S, Buisson D, Kunz C, Hachette F, Dupont J, Nay B, Prado S. The fungal leaf endophyte paraconiothyrium variabile specifically metabolizes the host-plant metabolome for its own benefit. Phytochemistry. 2014;108:95–101.
pubmed: 25446235
doi: 10.1016/j.phytochem.2014.09.021
Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda Mdel C, Glick BR. Plant growth-promoting bacterial endophytes. Microbiol Res. 2016;183:92–9.
pubmed: 26805622
doi: 10.1016/j.micres.2015.11.008
Stierle A, Strobel G, Stierle D, Grothaus P, Bignami G. The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew, Taxus brevifolia. J Nat Prod. 1995;58(9):1315–24.
pubmed: 7494141
doi: 10.1021/np50123a002
Kumar P, Singh B, Thakur V, Thakur A, Thakur N, Pandey D, Chand D. Hyper-production of taxol from Aspergillus Fumigatus, an endophytic fungus isolated from Taxus sp. of the Northern Himalayan region. Biotechnol Rep (Amst). 2019;24:e00395.
pubmed: 31799144
doi: 10.1016/j.btre.2019.e00395
Kasaei A, Mobini-Dehkordi M, Mahjoubi F, Saffar B. Isolation of Taxol-producing endophytic fungi from Iranian yew through novel molecular approach and their effects on human breast cancer cell line. Curr Microbiol. 2017;74(6):702–9.
pubmed: 28332162
doi: 10.1007/s00284-017-1231-0
Somjaipeng S, Medina A, Kwasna H, Ordaz Ortiz J, Magan N. Isolation, identification, and ecology of growth and taxol production by an endophytic strain of paraconiothyrium variabile from English yew trees (Taxus baccata). Fungal Biol. 2015;119(11):1022–31.
pubmed: 26466877
doi: 10.1016/j.funbio.2015.07.007
Stadler M, Kolarik M. Taxol is NOT produced sustainably by endophytic fungi ! – a case study for the damage that scientific papermills can cause for the scientific communities. Fungal Biology Reviews. 2024;49:100367.
doi: 10.1016/j.fbr.2024.100367
Sadeghi F, Samsampour D, Seyahooei MA, Bagheri A, Soltani J. Diversity and spatiotemporal distribution of fungal endophytes associated with Citrus reticulata cv. Siyahoo. Curr Microbiol. 2019;76(3):279–89.
pubmed: 30689005
doi: 10.1007/s00284-019-01632-9
Hao DC, Song SM, Mu J, Hu WL, Xiao PG. Unearthing microbial diversity of Taxus Rhizosphere via MiSeq high-throughput amplicon sequencing and isolate characterization. Sci Rep. 2016;6:22006.
pubmed: 27080869
pmcid: 4832182
doi: 10.1038/srep22006
Soca-Chafre G, Rivera-Orduna FN, Hidalgo-Lara ME, Hernandez-Rodriguez C, Marsch R, Flores-Cotera LB. Molecular phylogeny and paclitaxel screening of fungal endophytes from Taxus Globosa. Fungal Biol. 2011;115(2):143–56.
pubmed: 21315312
doi: 10.1016/j.funbio.2010.11.004
Xiong ZQ, Yang YY, Zhao N, Wang Y. Diversity of endophytic fungi and screening of fungal paclitaxel producer from Anglojap yew, Taxus x media. BMC Microbiol. 2013;13:71.
pubmed: 23537181
pmcid: 3618195
doi: 10.1186/1471-2180-13-71
Gauchan DP, Kandel P, Tuladhar A, Acharya A, Kadel U, Baral A, Shahi AB, Garcia-Gil MR. Evaluation of antimicrobial, antioxidant and cytotoxic properties of bioactive compounds produced from endophytic fungi of Himalayan yew (Taxus wallichiana) in Nepal. F1000Res 2020, 9:379.
Liu K, Ding X, Deng B, Chen W. Isolation and characterization of endophytic taxol-producing fungi from Taxus Chinensis. J Ind Microbiol Biotechnol. 2009;36(9):1171–7.
pubmed: 19484278
doi: 10.1007/s10295-009-0598-8
Mao Z, Zhang W, Wu C, Feng H, Peng Y, Shahid H, Cui Z, Ding P, Shan T. Diversity and antibacterial activity of fungal endophytes from Eucalyptus exserta. BMC Microbiol. 2021;21(1):155.
pubmed: 34044780
pmcid: 8157698
doi: 10.1186/s12866-021-02229-8
Salehi M, Moieni A, Safaie N, Farhadi S. Whole fungal elicitors boost paclitaxel biosynthesis induction in Corylus avellana cell culture. PLoS ONE. 2020;15(7):e0236191.
pubmed: 32673365
pmcid: 7365444
doi: 10.1371/journal.pone.0236191
Cao X, Xu L, Wang J, Dong M, Xu C, Kai G, Wan W, Jiang J. Endophytic fungus pseudodidymocyrtis lobariellae KL27 promotes taxol biosynthesis and accumulation in Taxus Chinensis. BMC Plant Biol. 2022;22(1):12.
pubmed: 34979929
pmcid: 8722197
doi: 10.1186/s12870-021-03396-6
Wang C, Wu J, Mei X. Enhancement of taxol production and excretion in Taxus chinensis cell culture by fungal elicitation and medium renewal. Appl Microbiol Biotechnol. 2001;55(4):404–10.
pubmed: 11398918
doi: 10.1007/s002530000567
Stierle A, Strobel G, Stierle D. Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science. 1993;260(5105):214–6.
pubmed: 8097061
doi: 10.1126/science.8097061
Shen C, Xue J, Sun T, Guo H, Zhang L, Meng Y, Wang H. Succinyl-proteome profiling of a high taxol containing hybrid Taxus species (Taxus x media) revealed involvement of succinylation in multiple metabolic pathways. Sci Rep. 2016;6:21764.
pubmed: 26902839
pmcid: 4763222
doi: 10.1038/srep21764
Zhou T, Luo X, Zhang C, Xu X, Yu C, Jiang Z, Zhang L, Yuan H, Zheng B, Pi E, et al. Comparative metabolomic analysis reveals the variations in taxoids and flavonoids among three Taxus species. BMC Plant Biol. 2019;19(1):529.
pubmed: 31783790
pmcid: 6884900
doi: 10.1186/s12870-019-2146-7
Wang Y, Xu X, Liu T, Wang H, Yang Y, Chen X, Zhu S. Analysis of bacterial and fungal communities in continuous-cropping ramie (Boehmeria nivea L. Gaud) fields in different areas in China. Sci Rep. 2020;10(1):3264.
pubmed: 32094349
pmcid: 7039886
doi: 10.1038/s41598-020-58608-0
Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26(2):266–7.
pubmed: 19914921
doi: 10.1093/bioinformatics/btp636
Yan L, Zhu J, Zhao X, Shi J, Jiang C, Shao D. Beneficial effects of endophytic fungi colonization on plants. Appl Microbiol Biotechnol. 2019;103(8):3327–40.
pubmed: 30847542
Wang Z, Zhu Y, Li N, Liu H, Zheng H, Wang W, Liu Y. High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of saline-alkali tolerant rice. Microbiol Res. 2021;250:126794.
pubmed: 34062342
doi: 10.1016/j.micres.2021.126794
Wu LS, Dong WG, Si JP, Liu JJ, Zhu YQ. Endophytic fungi, host genotype, and their interaction influence the growth and production of key chemical components of Dendrobium catenatum. Fungal Biology. 2020;124(10):864–76.
pubmed: 32948274
doi: 10.1016/j.funbio.2020.07.002
Wu L, Han T, Li W, Jia M, Xue L, Rahman K, Qin L. Geographic and tissue influences on endophytic fungal communities of Taxus chinensis var. Mairei in China. Curr Microbiol. 2013;66(1):40–8.
pubmed: 23053484
doi: 10.1007/s00284-012-0235-z
Liu L, Ma M, Liu Z, Zhang L, Zhou J. Community structure of fungal pathogens causing spikelet rot disease of naked oat from different ecological regions of China. Sci Rep. 2021;11(1):1243.
pubmed: 33441827
pmcid: 7806892
doi: 10.1038/s41598-020-80273-6
Rafiq M, Nadeem S, Hassan N, Hayat M, Sajjad W, Zada S, Sajjad W, Hasan F. Fungal recovery and characterization from Hindu Kush mountain range, Tirich Mir glacier, and their potential for biotechnological applications. J Basic Microbiol. 2020;60(5):444–57.
pubmed: 32147851
doi: 10.1002/jobm.201900608
Sreekanth D, Sushim GK, Syed A, Khan BM, Ahmad A. Molecular and morphological characterization of a taxol-producing endophytic fungus, gliocladium sp., from Taxus baccata. Mycobiology. 2011;39(3):151–7.
pubmed: 22783096
pmcid: 3385112
doi: 10.5941/MYCO.2011.39.3.151
Deng Z, Li C, Luo D, Teng P, Guo Z, Tu X, Zou K, Gong D. A new cinnamic acid derivative from plant-derived endophytic fungus pyronema sp. Nat Prod Res. 2017;31(20):2413–9.
pubmed: 28391728
doi: 10.1080/14786419.2017.1311890
Fatima N, Kondratyuk TP, Park EJ, Marler LE, Jadoon M, Qazi MA, Mehboob Mirza H, Khan I, Atiq N, Chang LC, et al. Endophytic fungi associated with Taxus fuana (West Himalayan Yew) of Pakistan: potential bio-resources for cancer chemopreventive agents. Pharm Biol. 2016;54(11):2547–54.
pubmed: 27159021
doi: 10.3109/13880209.2016.1170154
Mao Z, Xue M, Gu G, Wang W, Li D, Lai D, Zhou L. Lophiostomin A-D: new 3,4-dihydroisocoumarin derivatives from the endophytic fungus lophiostoma sp. Sigrf10. RSC Adv. 2020;10(12):6985–91.
pubmed: 35493878
pmcid: 9049733
doi: 10.1039/D0RA00538J
Zhou X, Zhu H, Liu L, Lin J, Tang K. A review: recent advances and future prospects of taxol-producing endophytic fungi. Appl Microbiol Biotechnol. 2010;86(6):1707–17.
pubmed: 20358192
doi: 10.1007/s00253-010-2546-y
Fu Y, Li X, Yuan X, Zhang Z, Wei W, Xu C, Song J, Gu C. Alternaria alternata F3, a novel taxol-producing endophytic fungus isolated from the fruits of Taxus cuspidata: isolation, characterization, taxol yield improvement, and antitumor activity. Appl Biochem Biotechnol. 2023;196(4):2246–69.
pubmed: 37498379
doi: 10.1007/s12010-023-04661-0
Liu Q, Li L, Chen Y, Wang S, Xue L, Meng W, Jiang J, Cao X. Diversity of endophytic microbes in Taxus yunnanensis and their potential for plant growth promotion and taxane accumulation. Microorganisms. 2023;11(7):1645.
pubmed: 37512818
pmcid: 10383522
doi: 10.3390/microorganisms11071645
Zheng H, Fu X, Shao J, Tang Y, Yu M, Li L, Huang L, Tang K. Transcriptional regulatory network of high-value active ingredients in medicinal plants. Trends Plant Sci. 2023;28(4):429–46.
pubmed: 36621413
doi: 10.1016/j.tplants.2022.12.007
Demidova E, Globa E, Klushin A, Kochkin D, Nosov A. Effect of methyl jasmonate on the growth and biosynthesis of C13- and C14-hydroxylated taxoids in the cell culture of yew (Taxus Wallichiana Zucc.) Of different ages. Biomolecules. 2023;13(6):969.
pubmed: 37371549
pmcid: 10296447
doi: 10.3390/biom13060969
Cao X, Xu L, Li L, Wan W, Jiang J. TcMYB29a, an ABA-responsive R2R3-MYB transcriptional factor, upregulates Taxol biosynthesis in Taxus Chinensis. Front Plant Sci. 2022;13:804593.
pubmed: 35310663
pmcid: 8931530
doi: 10.3389/fpls.2022.804593