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Endophytes from Ginkgo Biloba and Their Secondary Metabolites Zhihui Yuan1,3, Yun Tian1, Fulin He2,3* and Haiyan Zhou1*

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Endophytes from Ginkgo Biloba and Their Secondary Metabolites Zhihui Yuan1,3, Yun Tian1, Fulin He2,3* and Haiyan Zhou1* Yuan et al. Chin Med (2019) 14:51 https://doi.org/10.1186/s13020-019-0271-8 Chinese Medicine REVIEW Open Access Endophytes from Ginkgo biloba and their secondary metabolites Zhihui Yuan1,3, Yun Tian1, Fulin He2,3* and Haiyan Zhou1* Abstract Ginkgo biloba is a medicinal plant which contains abundant endophytes and various secondary metabolites. Accord- ing to the literary about the information of endophytics from Ginkgo biloba, Chaetomium, Aspergillus, Alternaria, Penicillium and Charobacter were isolated from the root, stem, leaf, seed and bark of G. biloba. The endophytics could produce lots of phytochemicals like favonoids, terpenoids, and other compounds. These compounds have antibac- teria, antioxidation, anticardiovascular, anticancer, antimicrobial and some novel functions. This paper set forth the development of active extracts isolated from endophytes of Ginkgo biloba and will help to improve the resources of Ginkgo biloba to be used in a broader feld. Keywords: Ginkgo biloba, Chinese medical plant, Endophytes, Secondary metabolites Background have been recognized as important sources of a variety of Ginkgo biloba (G. biloba) is a deciduous tree belonging novel secondary metabolites with anticancer, antimicro- to the ginkgo genus, which is also known as Gongsun- bial and other biological activities [4, 5]. shu, etc. G. biloba is one of the most ancient plants on Secondary metabolites are the chemical bank which earth dating back more than 200 million years. Com- provides a huge quantity of diverse commercial products monly Ginkgo biloba has been used for a medicinal plant for human medicines. First report about endophytics and its seeds, leaves and fruits can be used for medicines is that Stierle et al. isolated Taxomyces andreanae from with biological activities involving antibacteria, antioxi- phloem of Taxus brevifolia, which can produce taxol and dation, anticardiovascular and others. However, Ginkgo related chemicals at the concentration of 24–50 ng/L [6]. trees grow slowly and under natural conditions they need From then on, more and more endophytics from phar- more than 20 years from planting to fruiting, which is a maceutical plants, such as Camptotheca acuminata [7], restricting point for its development; while its endophyt- pine [8] and Taxus plants [9–11] were isolated. As to ics provide physiological metabolic pathways to pro- G. biloba, various endophytics including Chaetomium, duce numerous novel medicinal compounds which have Aspergillus, Alternaria, Penicillium and Charobacter become a hotspot [1]. were isolated from the root, stem, leaf, seed and bark of Te endophytics play important roles in the process of G. biloba. Tey produce lots of phytochemicals like fa- host plant growth and systematic evolution [1, 2]. During vonoids, terpenoids, and other compounds [12, 13]. 50% the whole life, endophytics protect their host from infec- of these isolates showed antimicrobial activities against tious diseases and also help to survive in adverse environ- various pathogens. Some secondary metabolites such ment [3]. Since the unique relationships between the host as 2-hexenal have been involved in the plant’s defense plant and associated endophytes, endophytes in G. biloba against pests. Tese bioactive metabolites are attractive to developing the commercial prodrugs and agricultural/ *Correspondence: [email protected]; [email protected] industrial production. Most importantly, as a therapeutic 1 College of Bioscience and Biotechnology, Hunan Agricultural University, drug, G. biloba has no side efects even after long periods Changsha 410128, China 3 College of Chemistry and Bioengineering, Hunan University of Science of use and its phytopharmaceuticals are readily accessible and Engineering, Yongzhou 425199, China throughout the world. For better using endophytic and Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Yuan et al. Chin Med (2019) 14:51 Page 2 of 40 secondary metabolites from ginkgo trees, we summarize Most are aerobic chemoheterotrophs and a few can the data previously reported. grow anaerobically by denitrifcation or mixed-acid fermentation. Endophytes in Ginkgo biloba Te Methylobacteriaceae comprises a large family of Te whole plant of G. biloba can be used as medicine. In Alphaproteobacteria and contains three genera including its root, stem, leaf, seed and bark of Ginkgo biloba, vari- Methylobacterium, Microvirga, and Meganema. Methylo- ous endophytes have been isolated and their biological bacterium species are ubiquitous in the natural environ- function was investigated. Te conventional procedure ment. Some species induce plant leaf and root nodule of endophytes isolation is to wash the roots, stems or formation, and can promote plant growth by production leaves of ginkgo frstly with 75% alcohol for 3 min, rinse of auxins [15]. Most of Methylobacterium are methylo- with sterile water 3–5 times, 0.1% mercury sterilized trophs and they can use methanol or other one-carbon for 2 min, rinsed with sterile water 3–5 times, cut into compounds as energy sources to produce proteins [16]. 0.5 cm × 0.5 cm pieces. Te cutting pieces were inocu- Otherwise, in Methylobacterium, common fatty acids lated in PDA medium at 28 °C for 4 days. After purifca- were contained especially ubiquinone Q-10, a popular tion, ginkgo endophytes were isolated. dietary supplement. For the endophytic procaryotes, on the total DNA Family Enterobacteriaceae contains a large number of as the template, 27F(AGA GTT TGATC-CTG GGT genera that are biochemically and genetically related to CAG)/1492R(GGT TAC CTT GTT ACG ACT T) as a one another. Many of them are pathogens, such as Sal- primer, 16S rDNA was amplifed. For the endophytic monella, Shigella or Yersinia, because they produce endo- eukarya, ITS5 (GAAG TAA AAG TCG TAA CAAGG)/ toxins. Endotoxins reside in the cell wall and when the ITS4 (TCC TCC GC TTA TTGA TATGC) as a primer, cell dies and the cell wall disintegrates, endotoxins are ITS rDNA was amplifed. According to the culturing and released [9]. molecular analysis between diferent species, the endo- Family Burkholderiaceae belongs to the order Bur- phytics residing in G. biloba belong to Chaetomium, kholderiales within the class Betaproteobacteria. Tis Aspergillus, Alternaria, Penicillium, Charobacter, etc. family is characterized by the presence of ecologically extremely diverse organisms and contains truly environ- Endophytic procaryotes in Ginkgo biloba mental saprophytic organisms, phytopathogens, oppor- From the previous reports, around 50 species of endo- tunistic pathogens, as well as primary pathogens for phytic procaryotes were found including Bacillus subtilis, humans and animals. Lactobacillus sp., Fusobacterium sp., Gemella sp., Neisse- Family Neisseriaceae and Micrococcaceae are wide- ria sp., Pseudomonas sp., Rothia sp., Veillonella sp., etc. spread in soil, subterranean cave silts, sea, glacier silts, Basing on 16S RNA sequence of endophytic procaryotes sewage, water sludge, aerial surfaces of plants, vegetables, from previous literatures, the phylogenetic tree was con- and various animal species and are even more distantly structed in Fig. 1. Amongst these procaryotes, the com- related to the human pathogens. munity structure or compositional diferences at diferent taxonomic levels was presented in Fig. 2. Endophytic eukarya in Ginkgo biloba Sphingomonadaceae are a family of the Alphaproteo- Te phylogenetic tree of endophytic eukarya (Fig. 3) bacteria and most abundant in G. biloba. An impor- was constructed basing on ITS sequence of roots and tant feature is the presence of sphingolipids in the outer leaves of Ginkgo biloba from previous literatures. membrane of the cell wall [14]. In this family, some spe- Amongst these endophytic eukarya, the community cies are phototrophic which may have high nutritional structure at diferent taxonomic levels was presented in value. Te phototrophic bacteria are rich in amino acids, Fig. 4. folic acid and vitamins, especially vitamin B12, biotin and Amongst eukarya, family Pleosporaceae belongs to sac coenzyme Q. Some other species are known as the abil- fungi. Te taxonomic relationship of this family to associ- ity to degrade some aromatic compounds which has the ated genera is still not determined. Te classifcation of interests for environmental remediation [11]. Pleosporaceae has been a challenge because of the lack Other abundant species are family Hyphomicrobiaceae, of the importance of morphological characters and ref- Burkholderiaceae, Methylobacteriaceae, Enterobacte- erence strains. From the present knowledge, the family riaceae, Neisseriaceae and Micrococcaceae. Te family Pleosporaceae includes numerous saprobic, opportunistic Hyphomicrobiaceae is afliated with Alphaproteobacteria human and plant pathogenic taxa [17]. and members of this family are distributed everywhere Phaeosphaeriaceae is a large and important family in soils, freshwater,
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