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Bioactive Secondary Metabolites with Multiple Activities from a Fungal Endophyte

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Bioactive Secondary Metabolites with Multiple Activities from a Fungal Endophyte bs_bs_banner Bioactive secondary metabolites with multiple activities from a fungal endophyte Catherine W. Bogner,1 Ramsay S.T. Kamdem,2 triggering plant resistance, thus suggesting a dual Gisela Sichtermann,1 Christian Matthaus,€ 3,4 activity, either directly, by killing or compromising Dirk Holscher,€ 5† Jurgen€ Popp,3,4 Peter Proksch,2 nematodes, or indirectly, by inducing defence mecha- Florian M.W. Grundler1 and Alexander Schouten1*‡ nisms against pathogens (nematodes) in plants. Such 1Institute of Crop Science and Resource Conservation compounds may serve as important leads in the devel- (INRES), Department of Molecular Phytomedicine, opment of novel, environmental friendly, nematocides. University of Bonn, Karlrobert-Kreiten Str. 13, 53115, Bonn, Germany. 2Institute of Pharmaceutical Biology and Biotechnology, Introduction € € Heinrich-Heine-University Dusseldorf, Universitats Str. 1. Plant-parasitic nematodes pose a problem in agriculture € Building. 26.23, 40225, Dusseldorf, Germany. by significantly affecting plant growth and crop yield at a 3 Institute of Photonic Technology, Workgroup global scale (Jones et al., 2013). The availability of resis- Spectroscopy/Imaging, Albert-Einstein-Str. 9, 07745, tant plant varieties is limited (Onkendi et al., 2014), and Jena, Germany. the most effective nematocides are unfortunately also the 4 Institute of Physical Chemistry and Abbe Center of most hazardous from an environmental and human health Photonics, Friedrich Schiller University, Helmholtzweg 4, perspective (Fuller et al., 2008). Evidently, there is cur- 07743, Jena, Germany. rently strong pressure in driving these toxic nematocides 5 Research Group Biosynthesis/NMR, Max Planck from the market, leaving the grower with only moderately € Institute for Chemical Ecology, Hans-Knoll-Str. 8, 07745, effective chemicals, which generally have nematostatic Jena, Germany. rather than nematocidal activity. Unless alternative meth- ods or chemicals to contain nematode proliferation in the field become available, crop losses caused by nematodes Summary may be further aggravated in future. In order to replace particularly biohazardous nemato- A potential opportunity to control nematode damages in cides, there is a strong drive to finding natural product- crops is the use of endophytes and their secondary based alternatives with the aim of containing nema- metabolites. Endophytes are generally defined as faculta- tode pests in agriculture. The metabolites produced by tive plant-colonizing microorganisms that do not cause the fungal endophyte Fusarium oxysporum 162 when disease symptoms in the plant (Hyde and Soytong, 2008). cultivated on rice media were isolated and their struc- Their ability to provide quantitative resistance towards tures elucidated. Eleven compounds were obtained, of nematodes is still not well understood. There is evidence which six were isolated from a Fusarium spp. for the that endophytes may affect nematodes either directly, by first time. The three most potent nematode-antagonis- synthesizing nematocidal compounds that kill or paralyse tic compounds, 4-hydroxybenzoic acid, indole-3-acetic nematodes, or indirectly by triggering plant defence acid (IAA) and gibepyrone D had LC50 values of 104, responses that are aimed at the nematode (Schouten, À 117 and 134 lgml 1, respectively, after 72 h. IAA is a 2016). This knowledge gap is obstructing further develop- well-known phytohormone that plays a role in ment of endophytes or their metabolites towards an effec- tive means of controlling nematodes in the field. Received 2 September, 2016; revised 31 October, 2016; accepted One of the endophytes that have been intensively 3 November, 2016. *For correspondence. E-mail sander.schouten@ † studied with respect to nematode control is Fo162. This wur.nl; Tel. +31-627500757; Fax +31-317418094. Present address: is a strain of the Fusarium oxysporum species complex Organic Plant Production and Agroecosystems Research in the Tropics and Subtropics (OPATS), University of Kassel, Steinstr. 19, (FOSC) that has been shown to reduce nematode infec- 37213, Witzenhausen, Germany. ‡ tion, development and fecundity (Martinuz et al., 2013). Present address:Laboratory of Nematology, Wageningen University, This effect is mostly attributed to systemic induced resis- Droevendaalsesteeg 1, 6708 PD, Wageningen, The Netherlands. Microbial Biotechnology (2017) 10(1), 175–188 tance mechanisms inside the plant (Martinuz et al., doi:10.1111/1751-7915.12467 2012), although it was also demonstrated that Fo162 Funding Information was capable of producing nematocidal compounds (Hall- This study was funded by the BMZ (Federal Ministry for Economic Cooperation and Development), Germany (Project number 102 701 24). mann and Sikora, 1996). However, the responsible ª 2016 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 176 C. W. Bogner et al. metabolites were never identified. In this study, we fully isolated from F. oxysporum. The secondary metabolites characterized a number of compounds that can be syn- produced in rice media by Fo162 [originally isolated from thesized by Fo162, some of which do have nematocidal the cortical tissue of surface-sterilized tomato roots cv. activity against the economically important root-knot Moneymaker in Kenya by Hallmann and Sikora (1994)] nematode, Meloidogyne incognita (Hu et al., 2013). were studied and eleven known compounds were iso- Remarkably, one of the best performing nematocidal lated. The compounds were isolated according to various compounds is in fact a known phytohormone, indicating procedures as illustrated in Fig. 1. The chemical struc- the multiple roles that natural products from endophytes tures of the compounds are shown in Fig. 2. A summary can play in defence against nematodes. This finding of the detailed NMR descriptions of all the pure com- forces us to reconsider the role of particular compounds pounds is given in Figs S1–S10. Literature comparison of in host–pathogen interactions and further emphasizes all compounds was in agreement with the obtained NMR that endophytes can serve as a valuable reservoir for data. The compounds were identified as: gibepyrone D finding effective natural compounds with both a direct (1), gibepyrone G (2), indole-3-acetic acid (3), indole-3- and an indirect activity towards nematodes. acetic acid methyl ester (4), 4-hydroxybenzoic acid (5), methyl 4-hydroxybenzoate (6), methyl 2-(4-hydroxyphe- Results nyl)acetate (7), uridine (8), fusarinolic acid (9), 5-(but-3- en-1-yl)picolinic acid (10) and beauvericin (11). Our study Identification of compounds from Fo162 of Fo162 metabolites led to the isolation of at least seven Fungal metabolites have primarily served as lead struc- bioactive compounds, six of which were purified from this tures for the development of nematocidal compounds, but fungal species for the first time. These were compounds so far only few reports have mentioned such compounds 3, 4, 5, 6, 7 and 8. Liquid–Liquid Filtration and Large-scale fractionation Solid rice extraction Evaporate Crude Extract 90% Methanolic fermentation EtOAc Extract 90% MeOH Fusarium oxysporum 162 culture (3.939 g) fraction Accession: KT357581 47.4 g (3) (1) (2) + n-Hexane (4) 90% Methanolic fraction (1242.85 mg) Sephadex LH 20 with 100% MeOH as mobile phase 101 fractions after Sephadex, TLC and pooling of samples 8 fractions Fraction 2 Fraction 3 Fraction 4 Fraction 5 Fraction 6 (209.73 mg) (469.51 mg) (180.25 mg) (112.35 mg) Semi- (48.85 mg) VLC Sephadex LH 20 preparative Sephadex LH 20 Step gradient with 100% Acetone HPLC; with 100% MeOH 0-100% MeOH as mobile phase 3 fractions as mobile phase 6 fractions 6 fractions 3 fractions FoSeph2-N2 FO-4-RP3 (3) FO-4-RP4 Fraction 2 Fraction 5 (4) (27.15 mg) Eluted with 50% Indol-3-acetic Eluted with 65% (55.22 mg) (11.02 mg) Indol-3-acetic MeOH acid (3.08 mg) Semi- MeOH acid methyl preparative Semi- Semi- Semi- Semi- ester (2.03 mg) HPLC; preparative preparative preparative preparative 7 fractions HPLC HPLC HPLC; 3 fractions HPLC; 1 fraction (8) (11) (1) (2) Uridine Beauvericin Gibepyrone D Gibepyrone G (1.86 mg) (1.95 mg) Z config. E config. (1.62 mg) (4.52 mg) VLC (7) Step gradient TLC Methyl 2-(4-hydroxyphenyl)acetate 0-100% MeOH EtOAc:MeOH:H20 (2.55 mg) 6 fractions 30:6:6 FO-RP-18-3 FO-RP-18-4 Eluted with 25% Eluted with 35% MeOH MeOH (5) (6) TLC 4-hydroxybenzoic Methyl-4-hydroxybenzoate EtOAc:MeOH:H20 acid (2.42 mg) acid (1.75 mg) 30:12:6 (9) (10) Fusarinolic acid 5-(but-3-en-1-yl) (12.59 mg) picolinic acid (17.89 mg) Fig. 1. Flow chart illustrating the process of extraction and fractionation of bioactive compounds produced by endophytic Fusarium oxysporum 162 on solid rice media. All compounds (1-11) are highlighted in grey. Numbers in parentheses are dry weights (mg) of fractions. ª 2016 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology, Microbial Biotechnology, 10, 175–188 Endophytic metabolites with dual function 177 OH O O O O O O O E Z HO OH N N H H H H O O Indole-3-acetic acid Indole-3-acetic acid (3) Gibepyrone D (1) Gibepyrone G (2) methyl ester (4) OH OH HO O O HO O O O Methyl 2-(4- Methyl 4-hydroxybenzoate (6) (7) 4-Hydroxybenzoic acid (5) hydroxyphenyl)acetate OH HO O N O HO HO N HO NH N OH O O O Uridine (8) Fusarinolic acid (9) 5-(but-3-en-1-yl)picolinic acid (10) O O N O O O Beauvericin (11) N N O O O O Fig. 2. Structures of compounds 1-11 isolated from endophytic Fusarium oxysporum 162, grown on solid rice media. The negative control (1% methanol) was tolerated by Nematocidal activities of isolated metabolites against the M. incognita J2 larvae and did not lead to significant M.
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