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Original article
Fungal endophytes isolated from Protium heptaphyllum and Trattinnickia rhoifolia as antagonists of Fusarium oxysporum
Endófitos fúngicos aislados de Protium heptaphyllum y Trattinnickia rhoifolia como antagonistas de Fusarium oxysporum
Juan E. Fierro-Cruz, Pedro Jiménez, Ericsson Coy-Barrera
Corresponding author
inquibio@unimilitar.edu.co

Corresponding author.
Universidad Militar Nueva Granada, Km 2 Cajicá – Zipaquirá, Cajicá, Colombia
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Using chemically synthesized fungicides has been the first line strategy to control phytopathogenic fungi<a class="elsevierStyleCrossRef" href="#bib0405"><span class="elsevierStyleSup">31</span></a>&#46; However&#44; secondary effects&#44; such as environmental pollution and resistance development due to the use of these products&#44; has led to a growing reluctance to use hazardous fungicides in agriculture&#46; Thus&#44; an enhanced trend in searching new control strategies involving environment-friendly alternatives in the management of plant pathogens has arisen<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">20</span></a>&#46; In the search for such control strategies&#44; naturally-occurring chemical entities have become potential alternatives for the industry to replace synthetic products<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">23</span></a>&#46; In this context&#44; microorganisms constitute a rich source of compounds with useful properties<a class="elsevierStyleCrossRef" href="#bib0490"><span class="elsevierStyleSup">48</span></a> for several applications in the agrochemical and pharmaceutical industries<a class="elsevierStyleCrossRefs" href="#bib0305"><span class="elsevierStyleSup">11&#44;23</span></a>&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">For several decades&#44; the interaction between fungal endophytes and their hosts has attracted the researchers&#8217; attention&#44; mainly because of the advantageous characteristics they confer to their host&#46; Among these characteristics we can mention enhanced stress tolerance&#44; plant growth factor production&#44; herbivore repellency and protection against pathogens<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">18</span></a>&#46; The latter characteristic is partly due to the fact that endophytes compete with other microorganisms for a specific niche&#44; which could be achieved by the production of antibiotic-like secondary metabolites&#44; along with other strategies<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">4</span></a>&#46; As a consequence of their repellent properties&#44; endophytes have been proposed as biocontrollers and as a promising source of antifungal metabolites against phytopathogens of agronomic importance<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">18</span></a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Based on our ongoing search for biologically active secondary metabolites from endophytic fungi&#44; the objective of this work was to explore the diversity of endophytes isolated from <span class="elsevierStyleItalic">Protium heptaphyllum</span> and <span class="elsevierStyleItalic">Trattinnickia rhoifolia</span> &#40;Burseraceae&#41; form Casanare&#44; Colombia&#46; These tree species&#44; have been traditionally used by indigenous communities to treat several ailments<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">12</span></a>&#44; and their complex chemical repertory has provided useful compounds having industrial&#44; pharmaceutical and agronomic potential<a class="elsevierStyleCrossRefs" href="#bib0440"><span class="elsevierStyleSup">38&#44;43</span></a>&#46; Furthermore&#44; endophytes have been isolated from a species of the Burseraceae family&#44; such as <span class="elsevierStyleItalic">Muscodor yucatensis</span><a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">25</span></a>&#44; with potential for controlling phytopathogens&#46; Therefore&#44; the aim of this work was to test <span class="elsevierStyleItalic">in vitro</span> the abilities of endophytes to inhibit the mycelial growth of <span class="elsevierStyleItalic">Fusarium oxysporum</span>&#44; by metabolite production&#46; <span class="elsevierStyleItalic">F&#46; oxysporum</span> is a pathogen of many plant species that represent a major threat for the production of several agriculturally important crops&#44; such as banana&#44; carnation&#44; chickpeas&#44; dates&#44; lentils&#44; tomato&#44; and others<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">27</span></a>&#46; The active component or components&#44; responsible for the antifungal activity were partially characterized following a bioassay-guided fractionation test of the liquid culture-derived crude extract from the most antagonistic endophyte&#44; to be incorporated in the future to control management programs for plant pathogen <span class="elsevierStyleItalic">F&#46; oxysporum&#46;</span></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Recovery of endophytes and isolation</span><p id="par0020" class="elsevierStylePara elsevierViewall">A total of two individuals from <span class="elsevierStyleItalic">P&#46; heptaphyllum</span> and two from <span class="elsevierStyleItalic">T&#46; rhoifolia</span> were collected in the foothill of the west Colombian Andes mountains in Aguazul&#44; Casanare&#44; Colombia &#40;N 05&#176;13&#8242;47&#46;89&#8243;&#44; W 072&#176;30&#8242;31&#46;38&#8243;&#41;&#44; a transition ecosystem between the savanna and the high Andean ecosystems&#46; Botanical specimens of <span class="elsevierStyleItalic">P&#46; heptaphyllum</span> &#40;Aubl&#46;&#41; Marchand &#40;COL573961&#41; and <span class="elsevierStyleItalic">T&#46; rhoifolia</span> &#40;Aubl&#46;&#41; Marchand &#40;COL573962&#41; were deposited in the Colombian National Herbarium&#46; From each tree&#44; the plant material &#40;from higher&#44; medium and lower strata&#41; was sampled in order to collect representative isolates from all the plants&#46; Five leaves per level were collected in a total of 60 leaflets that were bagged in sealed bags and stored in dark conditions for 24<span class="elsevierStyleHsp" style=""></span>h at room temperature &#40;<span class="elsevierStyleItalic">ca</span>&#46; 26<span class="elsevierStyleHsp" style=""></span>&#176;C&#41;&#46; Petioles were then removed and the complete leaves were vigorously washed with distilled sterile water and Tween 20 &#40;0&#46;01&#37;&#41;&#44; then submerged in 70&#37; aqueous ethanol &#40;1<span class="elsevierStyleHsp" style=""></span>min&#41;&#44; then in 1&#37; sodium hypochlorite &#40;3<span class="elsevierStyleHsp" style=""></span>min&#41;&#44; and then rinsed three times with sterilized distilled water&#46; Leaves were then imprinted on Potato Dextrose Agar &#40;PDA&#44; Oxoid&#44; UK&#41; for verifying the disinfection of all epiphytic microorganisms&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Each leaf was sectioned into 2<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleSup">2</span> pieces&#44; and 5 randomly-chosen pieces from each leaf were seeded in Petri dishes &#40;90<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>15<span class="elsevierStyleHsp" style=""></span>mm&#41; containing water agar &#40;agar 1&#46;5&#37;&#41; &#40;WA&#41;&#44; 1&#47;10 PDA &#40;PDA at a 10th of the recommended concentration&#41; or PDA&#44; and then incubated at 26<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Hyphae tips emerging from the leaf pieces were collected for three weeks&#44; and sub-cultured on PDA at 26<span class="elsevierStyleHsp" style=""></span>&#176;C in the dark&#46; Axenic cultures were established and&#44; when a specific fungus sporulated&#44; a monosporic culture was established&#46; Those fungi that never sporulated were kept for a hyphal tip culture&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Identification of endophytes</span><p id="par0030" class="elsevierStylePara elsevierViewall">Fungal populations were identified on the basis of cultural characteristics and morphology of fruiting bodies and spores<a class="elsevierStyleCrossRefs" href="#bib0265"><span class="elsevierStyleSup">3&#44;14&#44;21</span></a>&#46; Fungi were identified up to the genus level by observing the presence of conidial mycelium&#44; spore mass color&#44; distinctive reverse colony color&#44; production of diffusible pigments&#44; and spore morphology<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">3</span></a>&#46; Cultures that repetitively failed to sporulate on different media were recorded as <span class="elsevierStyleItalic">mycelia sterilia</span>&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Additionally&#44; those endophytes that inhibited <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth above 40&#37; were identified by amplification of the nuclear ribosomal internal transcribed spacer &#40;ITS&#41; region&#44; using the primers ITS1 &#40;5&#8242;-TCC GTA GGT GAA CCT GCG G-3&#8242;&#41; and ITS 4&#40;5&#8242;-TCC TCC GCT TAT TGA TAT GC-3&#8242;&#41;<a class="elsevierStyleCrossRef" href="#bib0480"><span class="elsevierStyleSup">46</span></a>&#46; Amplicons were sequenced with the same primers bidirectionally a single time in Macrogen Inc&#46; &#40;Korea&#41;&#44; and the resulting sequences were aligned and edited in BioEdit v7&#46;2&#46;5<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">13</span></a>&#46; The sequences were confronted with those in GeneBank database &#40;<a href="http://www.ncbi.nlm.nih.gov/">http&#58;&#47;&#47;www&#46;ncbi&#46;nlm&#46;nih&#46;gov</a>&#41;&#44; using BLASTN 2&#46;2&#46;28<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">28</span></a>&#46; The closest match was selected and aligned using ClustalW<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">26</span></a>&#46; For the phylogenetic analysis&#44; tree constructions were done with the MEGA 6&#46;0 program package<a class="elsevierStyleCrossRef" href="#bib0455"><span class="elsevierStyleSup">41</span></a> using the neighbor-joining method<a class="elsevierStyleCrossRef" href="#bib0435"><span class="elsevierStyleSup">37</span></a>&#46; Bootstrap analysis was done using 1000-times resampled data&#46; The resulting sequences were deposited in the GenBank&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Ethyl acetate &#40;EtOAc&#41; extraction</span><p id="par0040" class="elsevierStylePara elsevierViewall">Fungi selected for their inhibitory activity at <span class="elsevierStyleItalic">in vitro</span> conditions against <span class="elsevierStyleItalic">F&#46; oxysporum</span> were reactivated in 500<span class="elsevierStyleHsp" style=""></span>ml of Potato Dextrose Broth &#40;PDB&#44; Oxoid&#44; UK&#41;&#44; Sabouraud Broth &#40;SAB&#44; Oxoid&#44; UK&#41; and yeast extract sucrose media &#40;YES&#41;<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">19</span></a>&#44; and cultured in an orbital shaker under constant agitation &#40;100<span class="elsevierStyleHsp" style=""></span>rpm&#41; at 21<span class="elsevierStyleHsp" style=""></span>&#176;C for 7 days&#46; After that period the culture was filtered using Whatman No&#46; 1 qualitative filter paper&#44; and mycelia were lyophilized&#46; Separately&#44; both mycelia and filtered media were mixed with EtOAc in a 1&#58;3 proportion and incubated in an orbital shaker in constant agitation &#40;100<span class="elsevierStyleHsp" style=""></span>rpm&#41; for 48<span class="elsevierStyleHsp" style=""></span>h&#46; The organic phase &#40;EtOAc&#41; was separated from the mycelia by vacuum filtration using Whatman No&#46; 1 qualitative filter paper&#44; and from filtered liquid media using a decantation funnel&#46; The resulting extracts were concentrated by lyophilization&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Antifungal assays</span><p id="par0045" class="elsevierStylePara elsevierViewall">Fungal endophytes and a phytopathogenic isolate &#40;<span class="elsevierStyleItalic">F&#46; oxysporum</span> G1 isolated from <span class="elsevierStyleItalic">Physalis peruviana</span> &#40;Cape gooseberry&#41; available in the collection of the phytopathology laboratory at Universidad Militar Nueva Granada&#41; were cultured on PDA at 26<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 days at 26<span class="elsevierStyleHsp" style=""></span>&#176;C in the dark&#46; In order to evaluate the possible effect of each endophyte on phytopathogen growth&#44; dual cultures were settled and each isolate was challenged with <span class="elsevierStyleItalic">F&#46; oxysporum</span> G1&#46; Thus&#44; a plug &#40;3<span class="elsevierStyleHsp" style=""></span>mm diameter&#41;&#44; which was obtained from the colonial actively growing edge of the endophyte to be tested&#44; was seeded on PDA&#44; 10<span class="elsevierStyleHsp" style=""></span>mm away from the edge of a Petri dish &#40;90<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleHsp" style=""></span>mm&#41;&#46; At a spot distance &#40;10<span class="elsevierStyleHsp" style=""></span>mm&#41; from the diametrally-opposed edge&#44; a similar plug of <span class="elsevierStyleItalic">F&#46; oxysporum</span> was seeded&#46; Six days later&#44; the effect of each endophyte on <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth was observed and <span class="elsevierStyleItalic">F&#46; oxysporum</span> colony radial measurement and distance between colonies were recorded&#46; As control&#44; a plug of each organism was cultured alone&#46; These experiments were replicated three times&#46; Results were compared by the Tukey&#39;s HSD &#40;honest significant difference&#41; test&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The antifungal activity of the extracts was tested by direct TLC bioautographic detection<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">9</span></a>&#46; Extracts and fractions from the selected endophytes &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41; were diluted in ethanol &#40;HPLC grade&#41; and 30<span class="elsevierStyleHsp" style=""></span>&#956;g were seeded in a single spot on a TLC Aluminum silica gel 60 Sheet 20<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>20<span class="elsevierStyleHsp" style=""></span>cm &#40;Sigma&#8211;Aldrich&#41;&#46; Then the silica sheet was sprayed with a 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">6</span><span class="elsevierStyleHsp" style=""></span>conidia&#47;ml conidial suspension of <span class="elsevierStyleItalic">F&#46; oxysporum</span> until the whole sheet was covered&#46; The assays were incubated in a humid chamber for 3 days&#44; and then <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth over the sheet was evaluated under UV-light&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Fractionation of the most active extract</span><p id="par0055" class="elsevierStylePara elsevierViewall">The most active extract was fractionated by preparative HPLC &#40;Shimadzu prominence LC20AD&#41;&#44; in gradient elution&#44; using a Shimadzu Premier column C-18 &#40;4&#46;6<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>150<span class="elsevierStyleHsp" style=""></span>mm&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;m&#41; at a flow rate of 2<span class="elsevierStyleHsp" style=""></span>ml&#47;min&#46; The injection volume was 50<span class="elsevierStyleHsp" style=""></span>&#956;l&#46; The mobile phases consisted in methanol &#40;HPLC grade&#41; &#40;Phase A&#41; and trifluoroacetic acid 0&#46;005&#37; &#40;HPLC grade&#41; &#40;Phase B&#41;&#46; Separation was carried out for 25<span class="elsevierStyleHsp" style=""></span>min&#44; in a FRC 10A Shimadzu fraction collector&#46; A diode array detector &#40;DAD&#41; performed signal detection at 270<span class="elsevierStyleHsp" style=""></span>nm&#46; A total of 20 fractions were recovered and then concentrated by lyophilization&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">LC-MS-based chemical analysis</span><p id="par0060" class="elsevierStylePara elsevierViewall">Extracts and fractions were characterized by Reverse Phase Liquid Chromatography with multi-wavelength UV-VIS detection &#40;by a DAD&#41; and coupled by electrospray to a mass spectrometry detector &#40;RP-HPLC-DAD-ESI-MS&#41; &#40;Shimadzu Prominence LC&#47;MS 8030&#41;&#46; Analyses were performed on a Shimadzu prominence instrument&#44; in gradient elution&#44; using a Shimadzu Premier column C-18 &#40;4&#46;6<span class="elsevierStyleHsp" style=""></span>mm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>150<span class="elsevierStyleHsp" style=""></span>mm&#44; 5<span class="elsevierStyleHsp" style=""></span>&#956;m&#41;&#46; Simultaneous monitoring was carried out at 270<span class="elsevierStyleHsp" style=""></span>nm&#44; at a flow rate of 0&#46;6<span class="elsevierStyleHsp" style=""></span>ml&#47;min&#46; The operating temperature was 30<span class="elsevierStyleHsp" style=""></span>&#176;C and the injection volume was 20<span class="elsevierStyleHsp" style=""></span>&#956;l&#46; As mobile phase A 1&#37; formic acid in distilled water &#40;HPLC grade&#41; was used&#44; and acetonitrile &#40;ACN&#41; &#40;HPLC grade&#41; as mobile phase B&#59; separation was performed for 33<span class="elsevierStyleHsp" style=""></span>min&#46; The mass spectrometry detector &#40;MSD&#41; consisted of an electrospray ionization &#40;ESI&#41; source and a triple quadrupole analyzer&#46; The mass spectrometry method consisted of a scan in simultaneous positive and negative ionization with an acquisition time of 2&#8211;33<span class="elsevierStyleHsp" style=""></span>min&#44; a mass range of 50&#8211;2000<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">m&#47;z</span>&#44; a scan speed of 1667<span class="elsevierStyleHsp" style=""></span>&#956;&#47;s&#44; an event time of 0&#46;5<span class="elsevierStyleHsp" style=""></span>s&#44; nebulizer gas flow of 1&#46;5<span class="elsevierStyleHsp" style=""></span>l&#47;min&#44; 350<span class="elsevierStyleHsp" style=""></span>&#176;C interface temperature and DL&#44; and 450<span class="elsevierStyleHsp" style=""></span>&#176;C block temperature&#46; The drying gas flow rate was 9<span class="elsevierStyleHsp" style=""></span>l&#47;s&#46; The analysis was monitored at wavelengths between 270 and 330<span class="elsevierStyleHsp" style=""></span>nm&#46; Annotation and identification of the major and minor metabolites in the extract was performed by mass spectrometry- based analysis&#44; complemented with the analysis of reported metabolites&#46;</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Results</span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Recovery of endophytes</span><p id="par0065" class="elsevierStylePara elsevierViewall">A total of 577 endophytes were isolated from 900 cultured pieces of leaflets&#46; A subtotal of 355 endophytes were selected after the elimination of redundant morphotypes derived from the same leaflet&#46; The highest number of endophytes &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>236&#41; was recovered from the lowest collection level for both species&#46; The ITS region of the isolates was amplified and sequenced to determine the phylogenetic relationships among them &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; A phylogenetic tree was constructed based on a 570<span class="elsevierStyleHsp" style=""></span>bp sequences and isolates clustered as follows&#58; endophyte F92&#95;UMNG clustered with <span class="elsevierStyleItalic">Talaromyces amestolkiae</span>&#44; F18&#95;UMNG with <span class="elsevierStyleItalic">Phyllosticta</span> sp&#46;&#44; F211&#95;UMNG with <span class="elsevierStyleItalic">Chaetomium globosum</span>&#44; F299&#95;UMNG with <span class="elsevierStyleItalic">Xylaria grammica</span>&#44; and F281&#95;UMNG with <span class="elsevierStyleItalic">Meyerozyma</span> sp&#46; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Antifungal test</span><p id="par0070" class="elsevierStylePara elsevierViewall">The antifungal ability of 355 fungal endophytes against <span class="elsevierStyleItalic">F&#46; oxysporum</span> G1 was evaluated by the dual culture method&#46; Five endophytes reduced the area of <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth by at least 40&#37;&#44; without colony contact &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#44; which were grouped in a single group by the Tukey&#39;s HSD test&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">EtOAc-soluble extracts obtained from two isolates&#44; F211&#95;UMNG and F281&#95;UMNG&#44; cultured in YES&#44; exerted inhibitory effect on <span class="elsevierStyleItalic">F&#46; oxysporum</span> by direct bioautography &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A&#41;&#46; On comparing the inhibitory effect produced by these two isolates on <span class="elsevierStyleItalic">F&#46; oxysporum</span> radial growth&#44; it was found that isolate F211&#95;UMNG &#40;<span class="elsevierStyleItalic">C&#46; globosum&#41;</span> exerted a 64&#37; <span class="elsevierStyleItalic">in vitro</span> inhibition of <span class="elsevierStyleItalic">F&#46; oxysporum</span> colony growth arresting its growth producing with a distance between colonies of 12&#46;5<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;6<span class="elsevierStyleHsp" style=""></span>mm while F281&#95;UMNG caused 45&#37; inhibition showing 5&#46;7<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;9<span class="elsevierStyleHsp" style=""></span>mm between colonies &#40;<a class="elsevierStyleCrossRefs" href="#fig0010">Figs&#46; 2 and 3</a>A&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">Since the extract from F211&#95;UMNG isolate showed greater inhibitory activity against <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#44; it was fractionated in order to determine the most active fractions&#46; A total of 20 fractions were recovered &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>A&#41; and were additionally tested by bioautography against a conidial suspension of <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#46; Only fraction &#35;14 &#40;30<span class="elsevierStyleHsp" style=""></span>&#956;g&#41; exerted inhibition of the fungus &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>B&#41;&#46; Fraction &#35;14 was analyzed by LC-MS&#44; rendering a chromatogram that included two defined signals between min 12 and min 17 &#40;peaks <span class="elsevierStyleBold">1</span> and <span class="elsevierStyleBold">3</span>&#44; <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>B&#41;&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0085" class="elsevierStylePara elsevierViewall">From the recovered isolates&#44; fungi like <span class="elsevierStyleItalic">Alternaria</span> sp&#46;&#44; <span class="elsevierStyleItalic">Aspergillus</span> sp&#46;&#44; <span class="elsevierStyleItalic">Chaetomium</span> sp&#46;&#44; <span class="elsevierStyleItalic">Epicoccum</span> sp&#46;&#44; <span class="elsevierStyleItalic">Fusarium</span> sp&#46;&#44; <span class="elsevierStyleItalic">Pestalotiopsis</span> sp&#46;&#44; <span class="elsevierStyleItalic">Phomopsis</span> sp&#46;&#44; <span class="elsevierStyleItalic">Xylaria</span> sp&#46;&#44; among others&#44; were identified by their morphological traits and have been previously reported as common endophytes in other plants<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">6&#8211;8&#44;22&#44;24&#44;29&#44;47&#44;49</span></a>&#46; A high diversity of fungal species were also found in leaves and stems of <span class="elsevierStyleItalic">Boswellia sacra</span> &#40;Burseraceae&#41;&#44; being <span class="elsevierStyleItalic">Alternaria</span> and <span class="elsevierStyleItalic">Aspergillus</span> the most dominant genera&#44; which were both also isolated in this work&#46; However&#44; <span class="elsevierStyleItalic">Chaetomium</span> was also found in a relative high proportion &#40;26&#46;3&#37;&#41; represented by two species&#44; <span class="elsevierStyleItalic">C&#46; globosum</span> and <span class="elsevierStyleItalic">C&#46; spirale</span><a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">10</span></a>&#46; Screening works in <span class="elsevierStyleItalic">Boswellia serrata</span> exhibited <span class="elsevierStyleItalic">Myrothecium verrucaria</span> and <span class="elsevierStyleItalic">Phoma</span> sp&#46;<a class="elsevierStyleCrossRef" href="#bib0450"><span class="elsevierStyleSup">40</span></a> as dominant endophytes&#44; which were also isolated in our samples&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">The 355 endophytes isolated in this work were evaluated by the dual culture method against <span class="elsevierStyleItalic">F&#46; oxysporum</span> and only five endophytes showed inhibition against <span class="elsevierStyleItalic">F&#46; oxysporum</span> presumably by metabolite production because they inhibited the extension on the colony without mycelial contact and reduced the area of the phytopathogen by at least 40&#37; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#44; <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Antagonistic endophytes were identified by amplification of a 570<span class="elsevierStyleHsp" style=""></span>bp &#40;ITS&#41; region as <span class="elsevierStyleItalic">C&#46; globosum</span>&#44; <span class="elsevierStyleItalic">Meyerozyma</span> spp&#46;&#44; <span class="elsevierStyleItalic">Phyllosticta</span> spp&#46;&#44; <span class="elsevierStyleItalic">T&#46; amestolkiae</span>&#44; and <span class="elsevierStyleItalic">X&#46; grammic&#59;</span> such species have been reported as being endophytes and having antibiotic activity<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">1&#44;2&#44;17&#44;33&#44;35&#44;39&#44;49</span></a>&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">The extract from isolate <span class="elsevierStyleItalic">C&#46; globosum</span> F211&#95;UMNG&#44; at 30<span class="elsevierStyleHsp" style=""></span>&#956;g&#44; caused inhibit they inhibited the extension on the colony ion of <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A&#41;&#46; Based on the available literature&#44; in the <span class="elsevierStyleItalic">Chaetomium</span> genus&#44; mostly in <span class="elsevierStyleItalic">C&#46; globosum</span>&#44; seven signals defined by mass spectrum analysis were found to have the same <span class="elsevierStyleItalic">m&#47;z</span> value to that reported &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; Nevertheless&#44; five isomers previously reported in the <span class="elsevierStyleItalic">Chaetomium</span> genus matched the <span class="elsevierStyleItalic">m&#47;z</span> value detected at 38<span class="elsevierStyleHsp" style=""></span>min &#40;peak <span class="elsevierStyleBold">5</span>&#44; <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>B&#41; and&#44; therefore they cannot be differentiated in accordance with the known MS limitations&#46; Previous studies found that <span class="elsevierStyleItalic">C&#46; globosum</span> synthetized several molecules such as chaetoglobosins&#44; epipolythiodioxopiperazines&#44; azaphilones&#44; xanthones&#44; anthraquinones&#44; chromones&#44; depsidones&#44; terpenoids&#44; and steroids&#44; among others&#46; These types of compounds have shown antitumor&#44; cytotoxic&#44; antimalarial&#44; enzyme inhibitory&#44; antibiotic&#44; and other activities<a class="elsevierStyleCrossRef" href="#bib0500"><span class="elsevierStyleSup">50</span></a>&#46; In the present study cladosporin&#44; chaetoatrosin A and chaetoviridin A &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>C&#41; were identified to be active against <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#44; in the EtOAc extract of <span class="elsevierStyleItalic">C&#46; globosum</span> F211&#95;UMNG&#46; These compounds were previously reported as having antifungal activity<a class="elsevierStyleCrossRefs" href="#bib0330"><span class="elsevierStyleSup">16&#44;34&#44;45</span></a>&#46; Chaetoatrosin A acts as an inhibitor of chitin synthase II&#44; while chaetoviridin A inhibits the cholesteryl ester transfer protein &#40;CETP&#41;<a class="elsevierStyleCrossRef" href="#bib0460"><span class="elsevierStyleSup">42</span></a>&#46; The action of cladosporin is no fully understood but it has been reported that it exhibited lysyl-tRNA synthetase inhibition in <span class="elsevierStyleItalic">P&#46; falciparum</span><a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">15</span></a> and that its mode of action is different to that affecting <span class="elsevierStyleItalic">&#223;</span>-tubuline assembly in mitosis<a class="elsevierStyleCrossRef" href="#bib0475"><span class="elsevierStyleSup">45</span></a>&#46; The combination of the modes of action of the identified molecules might rationalize the observed growth inhibition of <span class="elsevierStyleItalic">F&#46; oxysporum</span> in the <span class="elsevierStyleItalic">in vitro</span> and bioautography test&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0100" class="elsevierStylePara elsevierViewall">In conclusion&#44; five endophytes acting as antagonists of <span class="elsevierStyleItalic">F&#46; oxysporum</span> under <span class="elsevierStyleItalic">in vitro</span> conditions were isolated and identified in the present study&#46; Isolate <span class="elsevierStyleItalic">C&#46; globosum</span> F211&#95;UMNG-derived extract inhibits the growth of <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#44; possibly by at least three molecules having different modes of action&#44; implying its possible application in control schemes of <span class="elsevierStyleItalic">F&#46; oxysporum</span><a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">27</span></a>&#46; A confirmation of the results through <span class="elsevierStyleItalic">in vivo</span> testing is required&#44; involving endophyte <span class="elsevierStyleItalic">C&#46; globosum</span> and purifying the identified compounds for evaluating their ability in the control of the disease caused by <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Ethical responsibilities</span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Protection of human and animal subjects</span><p id="par0105" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Confidentiality of data</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors declare that they have followed the protocols of their work center on the publication of patient data&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Right to privacy and informed consent</span><p id="par0115" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Funding</span><p id="par0120" class="elsevierStylePara elsevierViewall">The present work was financed by Vicerrector&#237;a de Investigaciones at UMNG through the project INV-CIAS-1472&#46;</p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflict of interest</span><p id="par0125" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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          "identificador" => "xres883271"
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              "identificador" => "abst0005"
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          "titulo" => "Keywords"
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          "titulo" => "Resumen"
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          "titulo" => "Palabras clave"
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          "identificador" => "sec0005"
          "titulo" => "Introduction"
        ]
        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Methods"
          "secciones" => array:6 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Recovery of endophytes and isolation"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Identification of endophytes"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Ethyl acetate &#40;EtOAc&#41; extraction"
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            3 => array:2 [
              "identificador" => "sec0030"
              "titulo" => "Antifungal assays"
            ]
            4 => array:2 [
              "identificador" => "sec0035"
              "titulo" => "Fractionation of the most active extract"
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            5 => array:2 [
              "identificador" => "sec0040"
              "titulo" => "LC-MS-based chemical analysis"
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          "titulo" => "Results"
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              "identificador" => "sec0050"
              "titulo" => "Recovery of endophytes"
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              "titulo" => "Antifungal test"
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          "titulo" => "Discussion"
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          "titulo" => "Ethical responsibilities"
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              "titulo" => "Protection of human and animal subjects"
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              "identificador" => "sec0075"
              "titulo" => "Confidentiality of data"
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            2 => array:2 [
              "identificador" => "sec0080"
              "titulo" => "Right to privacy and informed consent"
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          "identificador" => "sec0085"
          "titulo" => "Funding"
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        10 => array:2 [
          "identificador" => "sec0090"
          "titulo" => "Conflict of interest"
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        11 => array:2 [
          "identificador" => "xack295015"
          "titulo" => "Acknowledgements"
        ]
        12 => array:1 [
          "titulo" => "References"
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      ]
    ]
    "pdfFichero" => "main.pdf"
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    "fechaRecibido" => "2016-02-08"
    "fechaAceptado" => "2016-12-28"
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          "clase" => "keyword"
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          "palabras" => array:4 [
            0 => "Endophytes"
            1 => "Burseraceae"
            2 => "<span class="elsevierStyleItalic">Chaetomium</span>"
            3 => "Metabolites"
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          "palabras" => array:4 [
            0 => "End&#243;fitos"
            1 => "Burseraceae"
            2 => "<span class="elsevierStyleItalic">Chaetomium</span>"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Control of fungal pathogens is mainly addressed by the use of chemically synthesized fungicides which result in environmental pollution&#44; developing resistance after prolonged use&#46; In this context&#44; endophytes have been recognized as potential biocontrollers&#44; and also as a promising source of antifungal metabolites&#46; Therefore&#44; as part of our research on phytopathogen controllers&#44; 355 fungal endophytes were isolated from <span class="elsevierStyleItalic">Protium heptaphyllum</span> and <span class="elsevierStyleItalic">Trattinnickia rhoifolia</span> &#40;Burseraceae&#41;&#44; both ethnobotanically important tree species that produce secondary metabolites of agronomic and industrial interest&#46; Endophytes were tested by <span class="elsevierStyleItalic">in vitro</span> dual culture against <span class="elsevierStyleItalic">Fusarium oxysporum</span>&#44; a phytopathogen of agronomic importance&#46; Five endophytes exerted at least 40&#37; inhibition on <span class="elsevierStyleItalic">F&#46; oxysporum</span> growth&#46; Ethyl acetate &#40;EtOAc&#41; extracts were obtained from the most active antagonistic fungi&#44; after growing them in three different liquid media&#46; The extracts were tested against a conidial suspension of <span class="elsevierStyleItalic">F&#46; oxysporum</span> by direct bioautography&#46; Two extracts derived from fungi identified as <span class="elsevierStyleItalic">Chaetomium globosum</span>&#44; F211&#95;UMNG and <span class="elsevierStyleItalic">Meyerozima</span> sp&#46; F281&#95;UMNG showed inhibition of pathogen growth&#46; Isolate <span class="elsevierStyleItalic">C&#46; globosum</span>&#44; F211&#95;UMNG was selected for a chemical analysis by RP-HPLC-DAD-ESI-MS and antifungal molecules such as cladosporin&#44; chaetoatrosin A and chaetoviridin A were annotated and identified based on their MS data&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">El control de pat&#243;genos f&#250;ngicos se basa principalmente en el uso de fungicidas de s&#237;ntesis qu&#237;mica&#44; los que pueden dar lugar a la contaminaci&#243;n del medio ambiente y el desarrollo de resistencia despu&#233;s de un uso prolongado&#46; En este contexto&#44; los end&#243;fitos han sido reconocidos como potenciales biocontroladores y tambi&#233;n como fuentes prometedoras de metabolitos secundarios antif&#250;ngicos&#46; En el marco de nuestra investigaci&#243;n sobre controladores de fitopat&#243;genos&#44; se aislaron 355 hongos end&#243;fitos de <span class="elsevierStyleItalic">Protium heptaphyllum</span> y <span class="elsevierStyleItalic">Trattinnickia rhoifolia</span> &#40;Burseraceae&#41;&#44; especies arb&#243;reas de valor etnobot&#225;nico que producen metabolitos secundarios de inter&#233;s agron&#243;mico e industrial&#46; Los end&#243;fitos fueron evaluados <span class="elsevierStyleItalic">in vitro</span> en cultivos duales frente a <span class="elsevierStyleItalic">Fusarium oxysporum</span>&#44; un fitopat&#243;geno de importancia agron&#243;mica&#46; Cinco end&#243;fitos mostraron al menos un 40&#37; de inhibici&#243;n en el crecimiento de <span class="elsevierStyleItalic">F&#46; oxysporum</span>&#46; Una vez determinados los hongos m&#225;s activos&#44; estos se cultivaron en 3 medios l&#237;quidos diferentes y a partir de ellos se prepar&#243; una serie de extractos solubles en acetato de etilo&#46; Los extractos fueron probados contra una suspensi&#243;n de conidios de <span class="elsevierStyleItalic">F&#46; oxysporum</span> por bioautograf&#237;a directa&#46; Dos extractos derivados de los hongos identificados como <span class="elsevierStyleItalic">Chaetomium globosum</span> &#40;F211&#95;UMNG&#41; y <span class="elsevierStyleItalic">Meyerozima</span> sp&#46; &#40;F281&#95;UMNG&#41; mostraron inhibici&#243;n del crecimiento del pat&#243;geno&#46; En el extracto derivado del hongo <span class="elsevierStyleItalic">C&#46; globosum</span> se anotaron e identificaron los compuestos antif&#250;ngicos cladosporina&#44; chaetoatrosina A y chaetoviridina A mediante el an&#225;lisis por RP-HPLC-DAD-ESI-MS&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Dendrogram showing the phylogenetic relationship of fungal endophytes based on the ITS region&#46; Phylogenies were inferred using the neighbor-joining analysis and trees generated in MEGA 6&#46;0 software&#46; Numbers at branch points indicate bootstrap values&#46; The scale bars represent the estimated difference in nucleotide sequence&#46; Red rectangles indicate the endophytes isolated in this work&#46;</p>"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Inhibition of <span class="elsevierStyleItalic">F&#46; oxysporum</span> G1 &#40;Fox&#41; caused by <span class="elsevierStyleItalic">C&#46; globosum</span> F211&#95;UMNG &#40;Cg&#41; and <span class="elsevierStyleItalic">Meyerozima</span> sp&#46; &#40;Mg&#41; in PDA media in dual cultures at 6 days post inoculation&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">&#40;A&#41; Direct bioautography of endophyte-derived EtOAc extracts against <span class="elsevierStyleItalic">F&#46; oxysporum</span> conidia&#46; Solid lines&#58; Procloraz 40<span class="elsevierStyleHsp" style=""></span>ng &#40;control&#41;&#46; Medium dashed line&#58; Supernatant medium of EtOAc extract from <span class="elsevierStyleItalic">C&#46; globosum</span> F211&#95;UMNG&#46; Highly dashed line&#58; Supernatant medium of EtOAc extract from <span class="elsevierStyleItalic">M&#46; guilliermondii</span> F281&#95;UMNG&#46; &#40;B&#41; Bioautography of F211&#95;UMNG extract and most active fraction against <span class="elsevierStyleItalic">F&#46; oxysporum</span> conidia&#46; A&#58; Fraction &#35;14&#44; B&#58; Extract 211 INI&#44; C&#58; Sportak 40<span class="elsevierStyleHsp" style=""></span>ng&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">&#40;A&#41; Chromatographic profile of EtOAc extract from F211&#95;UMNG in YES medium&#46; F14&#43; arrow indicates fraction &#35;14&#46; &#40;B&#41; RP-HPLC-DAD chromatogram of fraction &#35;14&#46; Numbers indicate the annotated compounds by MS data &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; &#40;C&#41; Structures of the identified compounds in the most active fraction from EtOAc-soluble extract of <span class="elsevierStyleItalic">C&#46; globosum</span> F 211&#95;UMNG&#46;</p>"
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          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Species were defined when the node was supported with &#8804;90 &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " colspan="4" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Endophyte isolation conditions</th><th class="td" title="table-head  " align="center" valign="top" scope="col">Closest match&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col">NCBI accession&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Code&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Plant&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Level&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Recovered from&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">92&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">T&#46; rhoifolia</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Low&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PDA 1&#47;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Talaromyces amestolkiae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KU184613&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">211&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">P&#46; heptaphyllum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Low&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">WA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Chaetomium globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KU184610&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">219&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">P&#46; heptaphyllum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Low&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">PDA 1&#47;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Phyllosticta</span> sp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KU184614&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">281&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">P&#46; heptaphyllum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">High&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">WA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Meyerozyma</span> sp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KU184611&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">299&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">P&#46; heptaphyllum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Low&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">WA&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Xylaria grammica</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KU184612&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Isolation media and closest match in phylogenetic analysis by the neighbor joining method form the most active endophytes against <span class="elsevierStyleItalic">F&#46; oxysporum</span></p>"
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                  <table border="0" frame="\n
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Peak<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">t</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">R</span></span> &#40;min&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Isolated from&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">292&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">14&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Unknown&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15&#46;5&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">339&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">31&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Chaetoatrosin A<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">16</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; atrobrunneum</span> F449&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">262&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">38&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Chaetomugilin C<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">30</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">433&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Chaetomugilin N<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">30</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">433&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">433&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">433&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">4&#8242;-<span class="elsevierStyleItalic">epi</span>-chaetoviridin A<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">5</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">433&#46;9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">38&#46;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Differanisole&#47;differanisole A<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">32</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46;</span> spp&#46; strain RB-001&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">278&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">39&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Unidentified &#40;Reaxys RN 19364999&#41;<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">36</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; globosum</span> ZY-22&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">460&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Identified compounds isolated from other <span class="elsevierStyleItalic">Chaetomium</span> strains as constituents of fraction &#35;14</p>"
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                  "host" => array:1 [
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                      "titulo" => "Endophytic <span class="elsevierStyleItalic">Xylaria</span> &#40;Xylariaceae&#41; among liverworts and angiosperms&#58; phylogenetics&#44; distribution&#44; and symbiosis"
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                      "doi" => "10.1371/journal.pone.0036826"
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ISSN: 03257541
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