The temporal and spatial endophytic fungal community of Huperzia serrata: diversity and relevance to huperzine A production by the host
Tóm tắt
Plants maintain the steady-state balance of the mutually beneficial symbiosis relationship with their endophytic fungi through secondary metabolites. Meanwhile endophytic fungi can serve as biological inducers to promote the biosynthesis and accumulation of valuable secondary metabolites in host plants through a variety of ways. The composition and structure of endophytic fungal community are affected by many factors, including tissues, seasons and so on. In this work, we studied the community diversity, temporal and spatial pattern of endophytic fungi detected from the roots, stems and leaves of Huperzia serrata in different seasons. The correlation between endophytic fungi and huperzine A (HupA) content in plants was analyzed. A total of 7005 operational taxonomic units were detected, and all strains were identified as 14 phyla, 54 classes, 140 orders, 351 families and 742 genera. Alpha diversity analysis showed that the diversity of endophytic fungi in stem and leaf was higher than that in root, and the diversity in summer (August) was lower than that in other months. NMDS analysis showed that the endophytic fungal communities of leaves, stems and roots were significantly different, and the root and leaf communities were also different between four seasons. Through correlation analysis, it was found that 33 genera of the endophytic fungi of H. serrata showed a significant positive correlation with the content of HupA (p < 0.05), of which 13 genera (Strelitziana, Devriesia, Articulospora, Derxomyces, Cyphellophora, Trechispora, Kurtzmanomyces, Capnobotryella, Erythrobasidium, Camptophora, Stagonospora, Lachnum, Golubevia) showed a highly significant positive correlation with the content of HupA (p < 0.01). These endophytic fungi may have the potential to promote the biosynthesis and accumulation of HupA in plant. This report is the first time to analyze the diversity of endophytic fungi in tissues of H. serrata in different seasons, which proves that there is variability in different tissues and seasonal distribution patterns. These findings provide references to the study of endophytic fungi of H. serrata.
Tài liệu tham khảo
Zhang LB, Kong XX. Taxonomy of Huperzia Bernh. (sen. Str.) sect Serratae (Rothm.) Holub in China. Acta Phytotaxonomica Sinica. 2000;38(1):13–22.
Schuettpelz E, Schneider H, Smith AR, Hovenkamp PH, Prado J, Rouhan G, et al. A community-derived classification for extant lycophytes and ferns. J Syst Evol. 2016;54(6):563–603.
Zhang LB, The PPG. I classification and pteridophytes of China. Biodiversity Science. 2017;25(3):340–2.
Ma X, Tan C, Zhu D, Gang DR, Xiao P. Huperzine A from Huperzia species–an ethnopharmacolgical review. J Ethnopharmacol. 2007;113(1):15–34.
Jiang JH, Liu Y, Wang LQ, Chen YG. Constituents from Huperzia serrata. J Yunnan Norm Univ(Natural Sciences Edition. 2010;30(3):59–65.
Liu JS, Zhu YM, Yu CM, Zhou YQ, Han YQ, Wu FY, et al. The structures of huperzine A and B, two new alkaloids exhibiting marked anticholinesterase activity. Can J Chem. 1986;64:837–9.
Skolnick AA. Old chinese herbal medicine used for fever yields possible new Alzheimer disease therapy. JAMA. 1997;277(10):776.
Liu MY, Liu HC. Intelligence promoting Chinese materia medica. Zhongguo Zhong Xi Yi Jie He Za Zhi. 1995;15(1):59–61.
Qian ZM, Ke Y. Huperzine A: Is it an effective disease-modifying drug for Alzheimer’s disease? Front Aging Neurosci. 2014;6:216.
Ma XQ, Tan CH, Zhu DY, Gang DR. Is there a better source of huperzine A than Huperzia serrata? Huperzine A content of Huperziaceae species in China. J Agric Food Chem. 2005;53(5):1393–8.
Ma XQ, Tan CH, Zhu DY, Gang DR. A survey of potential huperzine A natural resources in China: the Huperziaceae. J Ethnopharmacol. 2006;104(1–2):54–67.
Hong WU, Zhuang P, Feng ZB, Zhang C, Jin CW. Resource investigation and assessment of Huperzia serrata. J Nat Resour. 2005;20(1):59–67.
Ding R, Sun BF, Lin GQ. An efficient total synthesis of (-)-huperzine A. Org Lett. 2012;14(17):4446–9.
Yang Y, Dai L, Wu D, Dong L, Tu Y, Xie J, et al. In vitro propagation, huperzine A content and antioxidant activity of three genotypic Huperzia serrata. Plants (Basel). 2021;10(6):1112.
Petrini O. Fungal endophytes of tree leaves. Microbial Ecology of Leaves. In: Andrews JH, Hirano SS, editors. Microbial Ecology of Leaves. New York: Springer; 1991. p. 179–97.
Clay K, Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat. 2002;160(Suppl 4):S99-s127.
Kamarudin AN, Lai KS, Lamasudin DU, Idris AS, Balia Yusof ZN. Enhancement of thiamine biosynthesis in oil palm seedlings by colonization of endophytic fungus Hendersonia Toruloidea. Front Plant Sci. 2017;8:1799.
Chen HM, Qi Y, He XY, Xu LN, Zhang WY. Endophytic fungus Mucor circinelloides DF20 promote tanshinone biosynthesis and accumulation in Salvia miltiorrhiza root. Plant Sci. 2021;307: 110898.
Liu X, Zhou ZY, Cui JL, Wang ML, Wang JH. Biotransformation ability of endophytic fungi: from species evolution to industrial applications. Appl Microbiol Biotechnol. 2021;105(19):7095–113.
Ju Z, Wang J, Pan SL. Isolation and preliminary identification of the endophytic fungi which produce Hupzine A from four species in Hupziaceae and determination of huperzine A by HPLC. Fudan Univ J Med Sci. 2009;36(4):445–9.
Li W, Zhou J, Lin Z, Hu Z. Study on fermentation condition for production of huperzine A from endophytic fungus 2F09P03B of Huperzia serrata. Chin Med Biotechnol. 2007;2(4):254–9.
Zhang ZB, Zeng QG, Yan RM, Wang Y, Zou ZR, Zhu D. Endophytic fungus Cladosporium cladosporioides LF70 from Huperzia serrata produces huperzine A. World J Microbiol Biotechnol. 2011;27(3):479–86.
Zhu D, Wang J, Zeng Q, Zhang Z, Yan R. A novel endophytic huperzine A–producing fungus, Shiraia sp. Slf14, isolated from Huperzia serrata. J Appl Microbiol. 2010;109(4):1469–78.
Dong LH, Fan SW, Ling QZ, Huang BB, Wei ZJ. Indentification of huperzine A-producing endophytic fungi isolated from Huperzia serrata. World J Microbiol Biotechnol. 2014;30(3):1011–7.
Shu S, Zhao X, Wang W, Zhang G, Cosoveanu A, Ahn Y, et al. Identification of a novel endophytic fungus from Huperzia serrata which produces huperzine A. World J Microbiol Biotechnol. 2014;30(12):3101–9.
Su JQ, Yang MH. Huperzine A production by Paecilomyces tenuis YS-13, an endophytic fungus isolated from Huperzia serrata. Nat Prod Res. 2015;29(11):1035–41.
Le TTM, Hoang ATH, Nguyen NP, Le TTB, Trinh HTT, Vo TTB, et al. A novel huperzine A-producing endophytic fungus Fusarium sp. Rsp5.2 isolated from Huperzia serrate. Biotechnol Lett. 2020;42(6):987–95.
Kang X, Liu C, Shen P, Hu L, Lin R, Ling J, et al. Genomic characterization provides new insights into the biosynthesis of the secondary metabolite huperzine A in the endophyte Colletotrichum gloeosporioides Cg01. Front Microbiol. 2019;9:3237.
Han WX, Han ZW, Jia M, Zhang H, Li WZ, Yang LB, et al. Five novel and highly efficient endophytic fungi isolated from Huperzia serrata expressing huperzine A for the treatment of Alzheimer’s disease. Appl Microbiol Biotechnol. 2020;104(21):9159–77.
Zaki AG, El-Shatoury EH, Ahmed AS, Al-Hagar OEA. Production and enhancement of the acetylcholinesterase inhibitor, huperzine A, from an endophytic Alternaria brassicae AGF041. Appl Microbiol Biotechnol. 2019;103(14):5867–78.
Wang Y, Yan RM, Zeng QG, Zhang ZB, Wang D, Zhu D. Producing huperzine A by an endophytic fungus from Huperzia serrata. Mycosystema. 2011;30(2):255–62.
Thi Minh Le T, Thi Hong Hoang A, ThiBich Le T, ThiBich Vo T, Van Quyen D, Hoang Chu H. Isolation of endophytic fungi and screening of Huperzine A-producing fungus from Huperzia serrata in Vietnam. Sci Rep. 2019;9(1):16152.
Wang Y. Isolation and Characterization of Endophytic Huperzine A-producing Fungi from Huperzia Serrata. Nanchang:Master's Thesis of Jiangxi Normal University; 2011.
Su JQ, Huang B, Qiu H, Yan LM, Zhang JC, Yang MH. Alkaloid and Huperzine A-producing endophytic fungi isolated from Huperzia serrata. Chin Pharm J. 2011;46(19):1477–81.
Li LF, Yang A, Zhao ZW. Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol Ecol. 2005;54(3):367–73.
Wu Z, Su Q, Cui Y, He H, Wang J, Zhang Y, et al. Temporal and spatial pattern of endophytic fungi diversity of Camellia sinensis (cv. Shu Cha Zao). BMC Microbiology. 2020;20(1):270.
Materatski P, Varanda C, Carvalho T, Dias AB, Campos MD, Rei F, et al. Spatial and temporal variation of fungal endophytic richness and diversity associated to the phyllosphere of olive cultivars. Fungal Biol. 2019;123(1):66–76.
Cui L, Noushahi HA, Zhang Y, Liu J, Cosoveanu A, Liu Y, et al. Endophytic Fungal community of Huperzia serrata: diversity and relevance to the production of huperzine A by the plant host. Molecules. 2021;26(4):892.
Fan SP, Miao LY, Li HD, Lin AH, Song FJ, Zhang P. Illumina-based analysis yields new insights into the diversity and composition of endophytic fungi in cultivated Huperzia serrata. PLoS ONE. 2020;15(11): e0242258.
Pang B, Yin DP, Zhai YF, He AG, Qiu LL, Liu Q, et al. Diversity of endophytic fungal community in Huperzia serrata from different ecological areas and their correlation with Hup A content. BMC Microbiol. 2022;22(1):191.
Xie HT, Feng XX, Wang MC, Wang YF, Kumar Awasthi M, Xu P. Implications of endophytic microbiota in Camellia sinensis: a review on current understanding and future insights. Bioengineered. 2020;11(1):1001–15.
Collado J, Platas G, González I, Peláez F. Geographical and seasonal influences on the distribution of fungal endophytes in Quercus ilex. New Phytol. 1999;144(3):525–32.
Naik BS, Shashikala J, Krishnamurthy YL. Diversity of fungal endophytes in shrubby medicinal plants of Malnad region, Western Ghats. Southern India Fungal Ecology. 2008;1(2–3):89–93.
Fang WP, Yang LC, Zhu XJ, Zeng L, Li XH. Seasonal and habitat dependent variations in culturable endophytes of Camellia sinensis. J Plant Pathology Microbiol. 2013;4(3):169.
Gupta S, Chaturvedi P, Kulkarni MG, Staden JV. A critical review on exploiting the pharmaceutical potential of plant endophytic fungi. Biotechnol Adv. 2020;39:107462.
Ma K, Xu YX, Ma N, Ma JJ, Tong YJ, He WX. Air Temperature Variation Trend in Shaanxi Hanzhong from 1951 to 2015. Henan Science. 2019;37(2):275–82.
Li G, Tang KH, Wei H, Yang WB, LI. Effects of Different Culture Condition on Biomass Accumulation and Total Alkaloid Content in Endophytic Fungi of Huperzia Serratum. Guizhou Agric Sci. 2010;38(12):138–41.
Joosten L, van Veen JA. Defensive properties of pyrrolizidine alkaloids against microorganisms. Phytochem Rev. 2011;10(1):127–36.
Paudel JR, Davidson C, Song J, Maxim I, Aharoni A, Tai HH. Pathogen and pest responses are altered due to RNAi-mediated knockdown of glycoalkaloid metabolism 4 in Solanum tuberosum. Mol Plant Microbe Interact. 2017;30(11):876–85.
Liu ZX, Wang MQ, Tian MX, Yuan LL, Yu BM, Qu B, et al. Pyrrole alkaloids from Solanum rostratum and their chemical defense function against Henosepilachna vigintioctomaculata. Fitoterapia. 2021;155: 105031.
Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, et al. Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol. 2010;185(4):1062–73.
Yuan J, Zhang W, Sun K, Tang MJ, Chen PX, Li X, et al. Comparative transcriptomics and proteomics of Atractylodes lancea in response to endophytic fungus Gilmaniella sp. AL12 reveals regulation in plant metabolism. Front Microbiol. 2019;10:1208.
Zhou JY, Liu ZL, Wang SF, Li J, Li YK, Chen WK, et al. Fungal endophytes promote the accumulation of Amaryllidaceae alkaloids in Lycoris radiata. Environ Microbiol. 2020;22(4):1421–34.
Jia M, Chen L, Xin HL, Zheng CJ, Rahman K, Han T, et al. A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol. 2016;7:906.
Barazani O, von Dahl CC, Baldwin IT. Sebacina vermifera promotes the growth and fitness of Nicotiana attenuata by inhibiting ethylene signaling. Plant Physiol. 2007;144(2):1223–32.
Gershenzon J, Dudareva N. The function of terpene natural products in the natural world. Nat Chem Biol. 2007;3(7):408–14.
Liu C, Tian J, An T, Lyu F, Jia P, Zhou M, et al. Secondary metabolites from solanum Rostratum and their Antifeedant defense mechanisms against Helicoverpa armigera. J Agric Food Chem. 2020;68(1):88–96.
Chen SS, Zhang MH, Wang JX, Zhang XC. Original plant and research progress of the medicinal plant Huperzia javanica. Guihaia. 2021;41(11):1794–809.
Zhang D, Yang Y, Castlebury LA, Cerniglia CE. A method for the large scale isolation of high transformation efficiency fungal genomic DNA. FEMS Microbiol Lett. 1996;145(2):261–5.
Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2(2):113–8.
White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide Methods Appl. 1990;8:315–22.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6.
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22(21):5271–7.
Heck KL Jr, van Belle G, Simberloff D. Explicit Calculation of the Rarefaction Diversity Measurement and the Determination of Sufficient Sample Size. Ecology. 1975;56(6):1459–61.
Kemp PF, Aller JY. Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol. 2004;2:161–77.
Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a Web browser. BMC Bioinformatics. 2011;12(1):385.
Chao A. Nonparametric estimation of the number of classes in a population. Scand J Statist. 1984;11:265–70.
Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1948;27(4):379–423.
Simpson EH. Measurement of diversity. Nature. 1949;163(4148):688.
Faith DP. Conservation evaluation and phylogenetic diversity. Biol Cons. 1992;61(1):1–10.
Pielou ECJ. The measurement of diversity in different types of biological collections. J Theor Biol. 1966;13:131–44.
Good IJ. The population frequency of species and the estimation of the population parameters. Biometrika. 1953;3–4:237–64.
Legendre P, Legendre L. Numerical Ecology, Volume 20, Second Edition (Developments in Environmental Modelling). 1998.
Zeng HY, Zhang XC. Determination of the content of huperzine A in Huperzia serrata from three different populations of Huaihua Region. Hunan Province Journal of Huaihua University. 2009;28(11):26–8.