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Can dark septate endophytic fungi (DSE) mobilize selectively inorganic soil phosphorus thereby promoting sorghum growth? A preliminary study
¿Los hongos endófitos septados oscuros (DSE) pueden movilizar selectivamente el fósforo inorgánico y promover así el crecimiento del sorgo? Un estudio preliminar
Osvaldo Barresi, Raúl S. Lavado, Viviana M. Chiocchio
Corresponding author
chiocchi@agro.uba.ar

Corresponding author.
Facultad de Agronomía, Universidad de Buenos Aires & INBA (CONICET/UBA), Av. San Martín 4453, C1417DSE Buenos Aires, Argentina
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0020" class="elsevierStylePara elsevierViewall">Inorganic soil phosphates are mainly a mix of amorphous and crystalline forms of calcium &#40;Ca&#41;&#44; aluminum &#40;Al&#41; and iron &#40;Fe&#41; phosphates&#44; including adsorbed and surface-precipitated phosphates&#46; They are insoluble and the concentration of soluble phosphorus &#40;P&#41; forms is low&#44; therefore fertilization is needed to supply P to crops&#46; However&#44; some negative environmental effects have been detected in recent decades&#44; due to the use of phosphate fertilizers<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a>&#46; Soluble phosphate fertilizers tend to precipitate with soil components and sometimes move outside the application site&#44; following the slope and causing economic and environmental problems&#44; i&#46;e&#46; the eutrophication of water bodies<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">For this reason&#44; an objective of agriculture is to maintain an optimal P level in the rhizosphere&#44; maximizing the efficiency of root absorption and reducing environmental risks&#46; To deal with these issues&#44; different strategies have been developed&#46; One of them is the use of microorganisms that participate in soil P transformation processes&#46; Phosphorous solubilization can be carried out by bacteria or fungi&#44; mainly mycorrhizal and filamentous fungi<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a>&#46; To this purpose&#44; these organisms release organic acids&#44; such as citric&#44; oxalic&#44; malic and gluconic acids&#44; produce siderophores&#44; generate enzymes and chelating substances which act as complexing agents dissolving minerals and inorganic precipitates and releasing nutrients by chelation<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">3&#44;4</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Dark Septate Endophytes &#40;DSE&#41; are another group of fungi&#44; which can grow in biotrophic and saprophytic forms&#46; Given their great heterogeneity&#44; they are capable of producing different effects on their host&#44; including a wide range of symbiotic relationships<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">6</span></a>&#46; DSE fungi can function as substitutes or complements for mycorrhizae in environments under different stresses<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a>&#46; The ability of these fungi to dissolve soil phosphates is poorly understood&#44; although there are examples referring to the effect of DSE fungi on the absorption of P by plants<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a>&#46; Spagnoletti et al&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a>&#44; studied <span class="elsevierStyleItalic">in-vitro</span> the ability of several DSE fungal species to dissolve reagent grade calcium&#44; aluminum and iron phosphates and found different solubilizing capacities among the fungi studied&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Among other crops&#44; DSE fungi could form a mutualistic association with sorghum &#40;<span class="elsevierStyleItalic">Sorghum bicolor</span> L&#46; Moench&#41;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a>&#44; an important cereal grain in the world&#46; It is cultivated in the Pampas &#40;Argentina&#41; where Mollisols are predominant&#44; and among them&#44; Hapludolls are widespread<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">11</span></a>&#46; We studied the phosphate solubilizing activity of previously known DSE fungi in a Typic Hapludoll&#44; determining the solubilizing effect of these fungi on inorganic soil P fractions&#44; and their effect on the growth of sorghum by means of the production of sorghum biomass and its P concentration&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Soils and DSE fungi</span><p id="par0040" class="elsevierStylePara elsevierViewall">The soil was sampled near the city of Jun&#237;n&#44; Province of Buenos Aires&#44; Argentina &#40;&#8722;34&#44;585&#59; &#8722;60&#46;9589&#41;&#44; in accordance with the US Soil Taxonomy&#44; a silty Typic Hapludoll<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">11</span></a>&#46; The soil was chemically analyzed using standard techniques &#40;Sparks et al&#46;&#44; 1996&#41;&#44; showing the following characteristics&#58; 1&#46;21&#37; organic carbon &#40;Walkley and Black&#41;&#44; 0&#46;24&#37; total nitrogen &#40;Kjeldahl&#41;&#44; 5&#46;5 pH &#40;soil&#58;water 1&#58;2&#46;5&#41;&#44; 0&#46;42 dS&#47;m electrical conductivity &#40;soil&#58;water 1&#58;2&#46;5&#41;&#44; and 32&#46;71<span class="elsevierStyleHsp" style=""></span>mg&#47;kg extractable P &#40;Bray and Kurtz&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Three fungi that presented good phosphate solubilizing activity in our previous study<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a> were selected from the Fungi Bank of the Microbiology Department&#44; Faculty of Agronomy&#44; University of Buenos Aires&#46; DSE fungi were <span class="elsevierStyleItalic">Alternaria alternata</span> &#40;GenBank accession no KT274695&#41;&#44; isolated from wheat&#59; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; &#40;GenBank accession no KU323668&#41;&#44; isolated from <span class="elsevierStyleItalic">Chloris gayana</span> forage and <span class="elsevierStyleItalic">Ophiosphaerella</span> sp&#46; &#40;GenBank accession no KT274702&#41; isolated from wheat<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a>&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Microcosm experiments</span><p id="par0050" class="elsevierStylePara elsevierViewall">The three DSE fungi were tested to determine their effect on inorganic soil phosphorous fractions&#46; The fungal inocula used in this test were obtained from cultures in petri dishes containing malt extract agar &#40;MEA&#41; for 7 days&#44; at 25<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; One hundred g of dry sieved soil were placed in glass jars with a hermetic lid&#44; moistened to 60&#37; of the value of the field capacity and tyndalized &#40;3 consecutive days for 1<span class="elsevierStyleHsp" style=""></span>h at 100<span class="elsevierStyleHsp" style=""></span>&#176;C in an autoclave&#41;&#46; To each microcosm&#44; 1&#37; chloramphenicol and 5 inoculum 0&#46;5<span class="elsevierStyleHsp" style=""></span>cm diameter discs taken from a fungal colony grown in MEA were added&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">A randomized experiment was developed with four treatments &#40;3 fungi and a control&#41; and five replications&#46; All treatments were under controlled conditions of light and temperature&#44; ensuring that the mycelia contacted the total soil mass&#46; Soil aggregation was observed&#44; which could be attributed to mycelial growth&#46; After 20 days of growth&#44; a composite sample &#40;30&#47;g subsamples&#41; was extracted from each microcosm&#46; Inorganic P fractions were quantified using the Chang and Jackson sequential extraction technique&#44; as modified by Williams et al<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a>&#46; Thus&#44; Soluble P &#40;NH<span class="elsevierStyleInf">4</span>Cl 1<span class="elsevierStyleHsp" style=""></span>M&#44; soil&#47;extractant ratio 1&#58;50&#41;&#44; P linked to Al &#40;NH<span class="elsevierStyleInf">4</span>F 0&#46;5<span class="elsevierStyleHsp" style=""></span>M&#44; pH 8&#46;2&#44; soil&#47;extractant ratio 1&#58;12&#46;5&#41;&#44; P linked to Fe &#40;NaOH 0&#46;1<span class="elsevierStyleHsp" style=""></span>M&#44; soil&#47;extractant ratio 1&#58;12&#46;5&#41; P linked to Ca &#40;H<span class="elsevierStyleInf">2</span>SO<span class="elsevierStyleInf">4</span> 0&#46;25<span class="elsevierStyleHsp" style=""></span>M&#44; soil&#47;extractant ratio 1&#58;7&#46;1&#41;&#44; and P residual &#40;sodium citrate 0&#46;3<span class="elsevierStyleHsp" style=""></span>M&#44; NaHCO<span class="elsevierStyleInf">3</span> 1<span class="elsevierStyleHsp" style=""></span>M and Na<span class="elsevierStyleInf">2</span>S<span class="elsevierStyleInf">2</span>O<span class="elsevierStyleInf">4</span>&#44; soil&#47;extractant ratio 1&#58;12&#46;5&#41; were extracted&#46; Phosphorus concentrations were determined using the Murphy and Riley colorimetric ascorbic acid blue color method<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a>&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Pot experiments</span><p id="par0060" class="elsevierStylePara elsevierViewall">A substrate was prepared from a mix of soil&#44; vermiculite and sand &#40;7&#58;2&#58;1&#41; and tyndalized as previously indicated&#46; Ten discs&#44; each of 0&#46;5<span class="elsevierStyleHsp" style=""></span>cm diameter&#44; of each active mycelium of the three fungi were placed in 400<span class="elsevierStyleHsp" style=""></span>g of tyndalized substrate&#46; A final volume of 50<span class="elsevierStyleHsp" style=""></span>ml of water-malt was added to each inoculated substrate and then stored in the dark at 25<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2<span class="elsevierStyleHsp" style=""></span>&#176;C for 10 days&#44; adding sterile water when necessary&#44; and maintaining the mycelium in contact with the substrate mass&#46; Seedling germination trays&#44; previously disinfected with 3&#37; sodium hypochlorite&#44; were prepared and the inoculated substrates with each DSE fungi were added&#46; Sorghum seeds &#40;cultivar Min&#250; II&#41; were disinfected with 70&#37; ethanol&#44; then treated with 3&#37; sodium hypochlorite and finally rinsed with sterile distilled water&#46; The seeds were pregerminated for a period of 8 days&#44; and then two plants were transplanted to 2-L volume pots&#46; The experiment was conducted in a greenhouse under controlled conditions&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Each pot was maintained at values close to the field capacity&#46; To favor plant growth&#44; urea and KNO<span class="elsevierStyleInf">3</span> were alternately applied at a rate of 10<span class="elsevierStyleHsp" style=""></span>ml of a 1<span class="elsevierStyleHsp" style=""></span>mg&#47;l solution&#44; every 2 days&#44; in all treatments&#46; After 60 days the aerial part was cut&#44; dried at 60<span class="elsevierStyleHsp" style=""></span>&#176;C until constant weight and then&#44; weighed&#46; Half of the radicle biomass was mixed&#44; the composite sample stained and the roots were observed<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">9</span></a> and the other half was dried and weighed&#46; Phosphorus in aerial and root biomass was extracted by calcination and dissolution of the ashes&#44; and determined by the Murphy and Riley colorimetric methodology<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a>&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">The data of soil P fractions&#44; aerial and radicle biomass&#44; P content in the aerial and radicle biomass&#44; and radicle length were statistically analyzed using the RStudio software &#40;version 1&#46;1&#46;453 for Windows RStudio Team 2015&#41; for an ANOVA analysis&#44; after testing the variables for normality and homogeneity of variance&#46; Tukey&#39;s multiple range test &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; was used to assess the differences between the treatment means&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The test results to determine the effect of the fungi on inorganic soil P fractions are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; The three studied DSE fungi showed capacity to dissolve soil P fractions compared with the control&#46; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; significantly reduced residual P and P linked to Ca&#44; <span class="elsevierStyleItalic">Alternaria alternata</span> significantly decreased P linked to Al and to Ca fractions and <span class="elsevierStyleItalic">Ophiosphaerella</span> sp&#46; affected P linked to Ca and to Fe&#46; Compared with the control&#44; <span class="elsevierStyleItalic">A&#46; alternata</span> showed a decrease and <span class="elsevierStyleItalic">Curvularia</span> sp&#46; an increase in soluble P&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">In the pot experiment no melanized septate hyphae or microsclerotia were observed inside the roots of any of the treatments&#46; However&#44; septate pigmented conidia were detected in the rhizosphere area for all inoculated treatments&#44; indicating the presence of DSE fungi as soil saprobes&#46; No structure of DSE fungi was observed in the control treatment&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> shows the results for aerial and radicle biomass&#44; radicle length&#44; and P in aerial and radicle biomass&#44; respectively&#46; The <span class="elsevierStyleItalic">Curvularia</span> sp&#46; treatment showed the significantly highest aerial biomass&#44; while the other two fungi neither differed from the control nor even showed lower aerial biomass&#46; The highest radicle biomass was recorded in the control treatment&#44; which agreed with the lowest aerial biomass&#47;root biomass ratio&#58; 3&#46;2&#44; against ratios varying from 4&#46;2 to 7&#46;8 in the fungi treatments&#46; Furthermore&#44; the largest root length was observed in the <span class="elsevierStyleItalic">Curvularia</span> sp&#46; treatment&#46; The control&#44; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; and <span class="elsevierStyleItalic">Ophiosphaerella</span> sp&#46; treatments did not show any significant differences in P concentration&#44; and in aerial and root biomasses&#46; <span class="elsevierStyleItalic">A&#46; alternata</span> showed the lowest P concentration&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0090" class="elsevierStylePara elsevierViewall">A meta-analysis<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a> reported that DSE inoculation had positive effects on total aerial and root biomass in several host species&#46; In this study&#44; only one DSE fungus was related to increases in the sorghum aerial biomass&#46; Moreover&#44; the differences found in root length could be related to differences in root diameters<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a>&#44; although this was not verified in this study&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">The fungal species did not colonize the cortical parenchyma of sorghum roots because the interaction between the root and the fungi did not find proper conditions for the fungi infection<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a>&#46; However&#44; it could be presumed that the effects of DSE fungi on sorghum took place in their saprophytic form&#46; There are indications that DSE fungi are capable of promoting plant growth by improving plant nutrition&#44; releasing nutrients from minerals or organic compounds&#44; or generating secondary metabolites like precursors of plant hormones that stimulate the growth of plants&#46; Additionally&#44; DSE fungi have positive effects controlling pathogens and increasing the abiotic stress tolerance of plants<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">3&#44;6</span></a>&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">DSE fungi affect the proportion of P insoluble fractions of the soil dissolving each fungi different P compounds&#44; as previously found in reagent grade phosphates<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a>&#46; In this experiment&#44; the solubilized P from some fractions did not precipitate in others&#44; as found in other conditions<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">1</span></a>&#46; The extraction of the P-sol&#46; is similar to that used to determine the soil bioavailable P&#44; which in the Pampas region is a mixture of 0&#46;03<span class="elsevierStyleHsp" style=""></span>N NH<span class="elsevierStyleInf">4</span>F and 0&#46;025<span class="elsevierStyleHsp" style=""></span>N HCl &#40;Bray &#38; Kurtz method&#41;&#46; Anyway&#44; there is a clear relationship between P-sol and the sorghum reaction&#46; The released P from the soil inorganic insoluble forms was only partially accumulated in the sorghum biomass&#44; as indicated by the higher quantity of P &#40;concentration<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>biomass&#41; taken from the soils by sorghum plants in the <span class="elsevierStyleItalic">Curvularia</span> sp&#46; treatment &#40;0&#46;0085<span class="elsevierStyleHsp" style=""></span>mg&#47;biomass vs 0&#46;0073<span class="elsevierStyleHsp" style=""></span>mg&#47;biomass in the control&#41;&#46; It is possible that part of the solubilized inorganic fractions could be integrated into the organic P fraction<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a> or&#44; also&#44; incorporated into the biomass of the fungi<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a>&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">The capacity of three DSE fungi &#40;<span class="elsevierStyleItalic">A&#46; alternata</span>&#44; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; and <span class="elsevierStyleItalic">Ophiosphaerella</span> sp&#46;&#41; to dissolve selectively P from reagent grade phosphates is reiterated on the insoluble phosphates of the soil&#46; No endophytic structures in sorghum roots were observed&#44; as the inoculated fungi remained in the saprophytic forms&#46; However&#44; there was a positive effect of <span class="elsevierStyleItalic">Curvularia</span> sp&#46; on the sorghum aerial biomass and radicle length&#46; The potential capacity of DSE fungi to solubilize the insoluble P soil fractions was not clearly related to the root absorption of the released P&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Results are far for conclusive but are a step forward to the utilization of DSE fungi as a potential solubilizer to deal with P crop nutrition&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Funding</span><p id="par0115" class="elsevierStylePara elsevierViewall">This work was financially supported by <span class="elsevierStyleGrantSponsor" id="gs1">Universidad de Buenos Aires &#40;UBACyT&#41;</span> project 20020170100707BA&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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    "highlights" => array:2 [
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      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">DSE fungi selectively mobilize insoluble phosphates from soils&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">There was a positive effect of <span class="elsevierStyleItalic">Curvularia</span> sp&#46; on sorghum growth&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">The absorption of P was not clearly related to the capacity of DSE fungi to solubilize it&#46;</p></li></ul></p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Phosphate fertilizers tend to precipitate with soil components&#44; affecting fertilization efficiency and causing negative environmental effects&#46; Soil microorganisms have been used to solve this problem&#46; However&#44; the ability of dark septate endophytic fungi &#40;DSE&#41; to dissolve phosphates and increase crop yield are not well known&#46; The activity of DSE fungi capable of solubilizing reagent grade phosphates was studied in a Typic Hapludoll &#40;<span class="elsevierStyleItalic">Hapludol t&#237;pico</span>&#41;&#46; The effect of the fungi on the inorganic phosphorus fractions was evaluated and an experiment was conducted in pots with sorghum as a crop&#46; No fungal structures were found in the roots&#46; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; aerial biomass and root length increased&#59; however&#44; P concentration was not affected&#46; Although the results are not conclusive&#44; they represent an advance in the potential use of DSE fungi as P solubilizers to treat crop nutrition&#46;</p></span>"
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        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Los fertilizantes fosfatados tienden a precipitar con componentes del suelo&#44; lo que afecta la eficiencia de la fertilizaci&#243;n y causa efectos negativos&#46; Para resolver este problema se han utilizado microorganismos del suelo&#46; Sin embargo&#44; no se conoce bien la capacidad de los hongos end&#243;fitos septados oscuros &#40;ESO&#41; para disolver fosfatos y aumentar el rendimiento de los cultivos&#46; Se estudi&#243; en un hapludol t&#237;pico <span class="elsevierStyleItalic">&#40;typic hapludoll&#41;</span> la actividad de hongos ESO capaces de solubilizar fosfatos de grado reactivo&#46; Se evalu&#243; el efecto de los hongos sobre las fracciones de f&#243;sforo inorg&#225;nico y se realiz&#243; un experimento en macetas con sorgo como cultivo&#46; No se encontraron estructuras f&#250;ngicas en las ra&#237;ces&#46; <span class="elsevierStyleItalic">Curvularia</span> sp&#46; aument&#243; la biomasa a&#233;rea y la longitud radical&#44; pero la concentraci&#243;n de f&#243;sforo no se vio afectada&#46; Aunque los resultados no son concluyentes&#44; representan un avance en el uso potencial de hongos ESO como solubilizadores de f&#243;sforo para tratar la nutrici&#243;n de cultivos&#46;</p></span>"
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          "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Different letters mean significant differences according to Tukey&#39;s test &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p>"
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                  \t\t\t\t" scope="col">Fraction&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">P&#8211; sol&#46;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">37&#46;98<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;59 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">40&#46;16<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;06 a&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">37&#46;88<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;17 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">196&#46;32<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;68 a&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">163&#46;12<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>9&#46;32 a&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">120&#46;94<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>7&#46;36 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;23<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02 d&nbsp;\t\t\t\t\t\t\n
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    ]
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      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
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            0 => array:3 [
              "identificador" => "bib0080"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Changes in soil phosphorous fractions caused by cropping without nutrient reposition&#46; A case study"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "O&#46; Barresi"
                            1 => "V&#46;M&#46; Chiocchio"
                            2 => "R&#46;S&#46; Lavado"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Python"
                        "fecha" => "2018"
                        "volumen" => "87"
                        "paginaInicial" => "14"
                        "paginaFinal" => "17"
                      ]
                    ]
                  ]
                ]
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              "identificador" => "bib0085"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush&#44; <span class="elsevierStyleItalic">Atriplex canescens</span>"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "J&#46;R&#46; Barrow"
                            1 => "P&#46; Osuna"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J Arid Environ 2002"
                        "fecha" => "2002"
                        "volumen" => "51"
                        "paginaInicial" => "449"
                        "paginaFinal" => "459"
                      ]
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