The decrease in the population of Gluconacetobacter diazotrophicus in sugarcane after nitrogen fertilization is related to plant physiology in split root experiments

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2 => array:2 [ "nombre" => "Antonio" "apellidos" => "Sorlózano" ] 3 => array:2 [ "nombre" => "Blanca" "apellidos" => "Gutiérrez-Soto" ] 4 => array:2 [ "nombre" => "José María" "apellidos" => "Navarro-Marí" ] 5 => array:2 [ "nombre" => "José" "apellidos" => "Gutiérrez-Fernández" ] ] ] ] ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754115001121?idApp=UINPBA00004N" "url" => "/03257541/0000004700000004/v2_201602050024/S0325754115001121/v2_201602050024/es/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "The decrease in the population of Gluconacetobacter diazotrophicus in sugarcane after nitrogen fertilization is related to plant physiology in split root experiments" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "335" "paginaFinal" => "343" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Osvaldo Rodríguez-Andrade, Luis E. Fuentes-Ramírez, Yolanda E. Morales-García, Dalia Molina-Romero, María R. Bustillos-Cristales, Rebeca D. Martínez-Contreras, Jesús Muñoz-Rojas" "autores" => array:7 [ 0 => array:2 [ "nombre" => "Osvaldo" "apellidos" => "Rodríguez-Andrade" ] 1 => array:2 [ "nombre" => "Luis E." "apellidos" => "Fuentes-Ramírez" ] 2 => array:2 [ "nombre" => "Yolanda E." "apellidos" => "Morales-García" ] 3 => array:2 [ "nombre" => "Dalia" "apellidos" => "Molina-Romero" ] 4 => array:2 [ "nombre" => "María R." "apellidos" => "Bustillos-Cristales" ] 5 => array:2 [ "nombre" => "Rebeca D." "apellidos" => "Martínez-Contreras" ] 6 => array:4 [ "nombre" => "Jesús" "apellidos" => "Muñoz-Rojas" "email" => array:1 [ 0 => "joymerre@yahoo.com.mx" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Laboratorio Ecología Molecular Microbiana, Centro de Investigaciones en Ciencias Microbiológicas (CICM)-Instituto de Ciencias (IC), Benemérita Universidad Autónoma de Puebla (BUAP), Puebla, México" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "La disminución de la población de Gluconacetobacter diazotrophicus en caña de azúcar, después de la fertilización nitrogenada, está relacionada con la fisiología de las plantas en experimentos de raíz dividida" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 3411 "Ancho" => 2383 "Tamanyo" => 255487 ] ] "descripcion" => array:1 [ "en" => "Bacterial population inside roots in split root experiments. Each value represents the media of data for five independent plants (Log of cell number/g root) with the respective standard deviation. Mean values with equal letters are not statistically different at p≤0.05, using the t-Student test. dpi: days post inoculation; dpf: days post fertilization; ND: not detected; N+: addition of 180mg of nitrogen/plant." ] ] ] "textoCompleto" => "IntroductionGluconacetobacter diazotrophicus is a gram-negative bacterium, initially isolated as endophyte from Brazilian sugarcane plants<a class="elsevierStyleCrossRef" href="#bib0250">8</a> and subsequently from sugarcane plants in other countries<a class="elsevierStyleCrossRefs" href="#bib0240">6,34</a>. In addition, G. diazotrophicus has also been isolated from the inner tissue of diverse hosts<a class="elsevierStyleCrossRef" href="#bib0275">13</a>, such as Ipomoea batatas, Pennisetum purpureum<a class="elsevierStyleCrossRef" href="#bib0270">12</a>, Saccharococcus sachari<a class="elsevierStyleCrossRefs" href="#bib0225">3,31</a>, Eleusine coracana<a class="elsevierStyleCrossRef" href="#bib0300">18</a>, pineapple<a class="elsevierStyleCrossRef" href="#bib0395">37</a>, and also from the rhizosphere of Coffea arabica<a class="elsevierStyleCrossRef" href="#bib0295">17</a>. More recently this bacterium was isolated from wetland rice<a class="elsevierStyleCrossRef" href="#bib0345">27</a>, carrot, raddish and beetroot<a class="elsevierStyleCrossRef" href="#bib0305">19</a> and was related to a dominant phylotype detected as endophyte from needles of Pinus flexilis and Picea engelmannii using 16S rRNA pyrosequencing<a class="elsevierStyleCrossRef" href="#bib0255">9</a>.G. diazotrophicus is a nitrogen fixing bacterium that produces phytohormones, such as indol acetic acid<a class="elsevierStyleCrossRefs" href="#bib0285">15,32,33</a> and gibberellins<a class="elsevierStyleCrossRef" href="#bib0230">4</a>. This bacterial species is able to stimulate the growth of sugarcane after its inoculation<a class="elsevierStyleCrossRefs" href="#bib0335">25,35,36,40</a>. The principal mechanism for stimulating plant growth occurs through the auxinic via<a class="elsevierStyleCrossRefs" href="#bib0370">32,35</a> and depends on the sugarcane variety and the genotype of G. diazotrophicus<a class="elsevierStyleCrossRef" href="#bib0335">25</a>.Isolation of G. diazotrophicus from sugarcane plants depends on the amount of nitrogen fertilization applied to the crops: the higher the level of nitrogen applied to the crops, the lower the probability to isolate G. diazotrophicus<a class="elsevierStyleCrossRefs" href="#bib0280">14,28,31</a>. In addition, seven genotypes of G. diazotrophicus associated with sugarcane plants fertilized with low levels of nitrogen were identified in Brazilian fields and the diversity between them seemed to be affected by the high levels of nitrogen applied to sugarcane crops<a class="elsevierStyleCrossRef" href="#bib0245">7</a> while only one genotype was detected in sugarcane plants fertilized with high levels of nitrogen in Mexican fields. Moreover, G. diazotrophicus colonization is reduced in plants fertilized with high doses of nitrogen<a class="elsevierStyleCrossRefs" href="#bib0280">14,22,25</a>.The decrease in the population of G. diazotrophicus associated with sugarcane plants could be due to pleomorphic changes that occur while culturing bacteria in the presence of high nitrogen concentrations<a class="elsevierStyleCrossRef" href="#bib0355">29</a>. Additionally, it has been proposed that the decrease in the population of G. diazotrophicus associated with sugarcane could be due to physiological changes that the plant suffers in the presence of high nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0245">7,14</a>.Split root experiments have been developed to evaluate the systemic effect of a specific substance on plants, when this substance is supplied only on one end of the plant, while the other end could be used as control<a class="elsevierStyleCrossRef" href="#bib0420">42</a>, but also to evaluate the systemic effect on plant pathogens due to the action of the induced systemic resistance produced by rhizobacteria<a class="elsevierStyleCrossRef" href="#bib0215">1</a>.In this work we show a statistical analysis of the behavior of the population of G. diazotrophicus present inside the roots and in the rhizosphere using split root experiments, both at high or low nitrogen levels in the form of NH4NO3. In accordance with our results, the negative effect of nitrogen on the population of G. diazotrophicus is influenced by the plant.Materials and methodsBacterial strains used for in vitro studies were G. diazotrophicus PAl 5T, PAl 3 and UAP 5560, each one corresponding to a different genotype. PAl 5T represents the predominant genotype isolated from different Brazilian sugarcane varieties (ET 3), PAl 3 corresponds to a rare genotype not frequently isolated (ET 5) and UAP 5560 is the predominant genotype isolated from different Mexican sugarcane varieties (ET1)<a class="elsevierStyleCrossRef" href="#bib0245">7</a>.Experiment 1. In vitro assaysThe ability of G. diazotrophicus strains to grow at different nitrogen concentrations was explored in two in vitro conditions: one using LGI solid Plates<a class="elsevierStyleCrossRef" href="#bib0250">8</a> supplemented with different concentrations of NH4NO3 and the other using semisolid LGI medium<a class="elsevierStyleCrossRef" href="#bib0250">8</a> supplemented with different concentrations of NH4NO3 (Sigma–Aldrich A3795). In the first case, bacteria were grown until stationary phase (five independent growth tubes by strain) in MESMA liquid medium<a class="elsevierStyleCrossRef" href="#bib0280">14</a> for 48h at 30°C and 200rpm. Cells were washed twice by centrifugation and resuspended in MgSO4 10mM (Sigma–Aldrich M7506). Each bacterial suspension was serially diluted (factor 1:10) and dilutions were placed in plates at different NH4NO3 concentrations. Bacterial population was quantified by the DPSM method<a class="elsevierStyleCrossRef" href="#bib0260">10</a>. For the second condition, bacterial strains were grown until stationary phase (five independent growth tubes by strain), in 150ml of MESMA liquid medium, for 48h at 30°C and 200rpm. Each washed bacterial suspension was serially diluted (factor 1:10) and 100μl of each dilution were placed in series of semisolid LGI tubes in triplicate<a class="elsevierStyleCrossRef" href="#bib0335">25</a> containing the amount of NH4NO3 assessed (data observed in <a class="elsevierStyleCrossRefs" href="#tbl0005">Tables 1 and 2</a>). Quantification was carried out by the most probable number method (MPN) using a McCrady table with three replicate vials for each dilution.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Experiment 2. Plant assaysThe effect of NH4NO3 on bacterial association with sugarcane was assessed with the use of split root experiments. For this purpose, sugarcane plantlets variety MEX 57-473 were obtained by micropropagation as described previously<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. Micropropagated plantlets were free from bacteria. Forty plantlets were inoculated with G. diazotrophicus PAl 5T strain by immersion of roots for 1h in the bacterial suspension (5×108UFC/ml). Forty plantlets were used as non-inoculated controls and were only immersed in distilled sterile water. To obtain the bacterial suspension, G. diazotrophicus PAl 5T was grown in 10 flasks containing 35ml of TESMA medium until stationary phase, cells were washed by centrifugation twice; after, the pellet was resuspended in 35ml of MgSO4 (10mM) and mixed to obtain 350ml of bacterial suspension. Ten milliliters of this suspension were dispensed in tubes of 25cm×2.5cm and a single tube was used to inoculate each sugarcane plantlet.After inoculation, both inoculated and non-inoculated plantlets were placed in sterile split root systems (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>), each consisting of two pots joined by the upper part. Each pot had 500ml capacity and contained sterile vermiculite. For each plant, half of the roots were placed in pot 1 and the other half in pot 2, approximately 3 roots in each pot. The split root systems were watered in both pots with enough water and low doses of NH4NO3 (10mgN/plant equivalent to 0.35mM) and mineral salts, according to Muñoz-Rojas and Caballero-Mellado<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. The pots were covered with aluminum foil, and the zone where the plants emerged was protected with sterile cotton. The plantlets were maintained under greenhouse conditions with controlled temperature (26–30°C) with a light/dark photoperiod of 16/8h. Twenty days after inoculation (dpi) the bacterial number was determined for five plants both in their rhizospheres and inside the roots. At 20dpi, 15 plants of each treatment (inoculated and non-inoculated) were supplemented with a high dose of NH4NO3 in one of the pots (180mg of N/plant equivalent to 6.3mM) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>) under sterile conditions. Plants were again maintained under greenhouse conditions and watered periodically with distilled sterile water. Rhizospheric and endophytic bacteria were recovered from the two pots for each plant system and the population was determined at 35, 55 and 100dpi, equivalent to 15, 35 and 80 days post fertilization (dpf). Bacterial number was determined as described previously by the most probable number method using a McCrady table with three replicate vials for each dilution<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. For this purpose, five independent plants or systems for each treatment (inoculated and non-inoculated) and treatments at different nitrogen levels were analyzed in each time. The plants were carefully removed from the vermiculite, each side of the root system was placed in an independent sterile container, and the root was shaken to discard vermiculite that was not adhered. The resultant root-vermiculite was submerged in enough sterile water (covering the root) and vortexed to maximal velocity for 40s: the suspension was used to perform rhizospheric bacterial quantification. Vermiculite weight was obtained by drying samples without the roots. Furthermore, for endophytic bacteria quantification, each root was placed in a sterile bottle, washed to discard vermiculite and disinfected with 70% ethanol for 30s. Then the roots were rinsed with distilled water and the surface was sterilized with a 1.5% sodium hypochlorite solution (Sigma–Aldrich 425044) for 20min. Later, the roots were rinsed six times with sterile distilled water under sterile conditions. Fresh roots were macerated in water in 1:10 (w/v) proportion. Each sample used for bacterial quantification was diluted (factor 1:10) until dilution 1:1,000,000 and after, 100μl of each dilution were placed in a tube containing semisolid LGI medium (without nitrogen for the growth of diazotrophic bacteria), three tubes were dispensed. After bacterial growth, positive and negative tubes were registered; the presence of a yellow pellicle at the top of the LGI semisolid medium, was recorded as a positive tube<a class="elsevierStyleCrossRefs" href="#bib0250">8,25,27</a>. In addition, acidification of the media was observed with color changes from green to yellow, which is characteristic of G. diazotrophic growth; furthermore, after 7 days the yellow color was absorbed by bacteria<a class="elsevierStyleCrossRef" href="#bib0250">8</a>. The estimation of the bacterial number of each sample was carried out by the most probable number method using a McCrady table with three replicate vials for each dilution (with a confidence limit of 95%). For rhizospheric bacteria quantification, the value obtained from the McCrady table was multiplied per 10 and the dilution factor was considered in order to obtain the number of bacterial cells/ml of liquid suspension (sample). This value was multiplied per the initial water volume where the root was vortexed and divided by the amount in grams (g) of vermiculite (V) present in the suspension (considered as the adhered soil to the roots)<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. The final quantified values obtained were stated as the number of cells/gV. To assess endophytic bacteria quantification, the value obtained from the McCrady table, was multiplied by 10 and the dilution factor was considered in order to obtain the number of bacterial cells/ml of liquid suspension (sample); later this value was multiplied by 10 due to initial dilution (w/v) of fresh roots for each side of the root systems. Each bacterial number value obtained was transformed to logarithmic form for statistical purposes. All treatments explored in the present work had five bacterial number values which were used to calculate the standard deviation and the statistical analysis. To ensure that quantified bacteria corresponded to G. diazotrophicus PAl 5T, its ability to inhibit a sensitive strain (PAl 3) was checked and electrophoretic mobility patterns of 12 metabolic enzymes were compared with a reference strain<a class="elsevierStyleCrossRefs" href="#bib0240">6,7,17</a>. To achieve this goal, some positive tubes of semisolid LGI media with characteristic growth of G. diazortrophicus, were used to streak the bacteria pellicle on solid plates of LGI media and selected colonies were assessed for their ability to inhibit a sensitive strain by the double agar layer method<a class="elsevierStyleCrossRefs" href="#bib0310">20,26</a>. All selected isolates were able to inhibit the growth of G. diazotrophicus PAl 3 (an antagonistic characteristic of strain PAl 5T), and they also had the same pattern of electrophoretic mobility of the metabolic enzymes explored, as the reference strain G. diazotrophicus PAl 5T (data not shown).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>Statistical analysisData corresponding to each treatment for the different experiments were statistically compared in pairs with the t-Student test, using Sigma Plot of the Jandel Scientific Software. Results of comparison were used to generate a matrix of differences and similarities between treatments for assignment of letters (data not shown).ResultsEffect of NH4NO3 on G. diazotrophicus strains in vitroThe three strains of G. diazotrophicus explored (PAl 5T, PAl 3 and UAP 5560) were able to grow in solid media until 22.4mM of NH4NO3 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>), which is a high nitrogen level and corresponds to 640mg of N/plant. The statistical analysis showed no differences between bacteria grown in the presence of 22.4mM of NH4NO3 in comparison with normal LGI. G. diazotrophicus UAP 5560 tolerated a concentration of 89.6mM in solid LGI, but the bacterial number was reduced from 108 to 105CFU/ml (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). In semisolid LGI medium it was also observed that the three strains of G. diazotrophicus explored were able to grow until 22.4mM of NH4NO3 (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>); the growth of the strains was affected at 44.8mM in the order of 102cells/ml and the growth of UAP 5560 also tolerated better than others the presence of high levels of NH4NO3 (89.6mM); however, under this condition bacterial numbers diminished in the order of 101cells/ml.Effect of NH4NO3 on the colonization of sugarcane testing G. diazotrophicus PAl 5T in split root experimentsThe analysis of the population of G. diazotrophicus strain PAl 5T was carried out using the sugarcane variety MEX-57473 with split root experiments both in rhizospheres as endophytically. Bacteria were not detected in non-inoculated control plants. Rhizospheric population was similar in both sides of the root systems at 20dpi, about 1×107cells/g vermiculite (V) when basal levels of NH4NO3 were present. No statistical differences were observed at 35dpi (15dpf) in the rhizospheric population between both sides of the system, neither between treatments fertilized with high levels of NH4NO3 in comparison to those fertilized with basal levels. Furthermore, there were no differences when comparing the same treatments 20dpi (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). In accordance with our data, bacterial rhizospheric population decreased at 55dpi (35dpf) in plants fertilized with high levels of NH4NO3 when compared to the initial population observed in plants at 20dpi. However, no differences were observed between the bacterial numbers recovered from each side of the split root systems neither for the plants fertilized with high levels of NH4NO3 nor for the plants treated with basal levels. Interestingly, at 100dpi (80dpf), fertilized plants with high levels of nitrogen had differences in rhizospheric population, detecting low bacterial numbers (around 1×104cells/gV) in the pot fertilized with basal nitrogen in comparison with the bacterial numbers detected in the other pot of the system and also when compared to the bacterial numbers of both pots from plants fertilized with low levels of nitrogen, in the order of 105cells/gV (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>The effect of nitrogen on the endophytic population of G. diazotrophicus PAl 5T was more evident (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Inside the roots, the population of G. diazotrophicus was detected in the order of 103cells/g of root at 20dpi. After the addition of high levels of NH4NO3 in one pot of the split root systems corresponding to the treated plants containing high levels of nitrogen, no changes were observed in the bacterial population measured 35dpi (15dpf) when comparing pots of the same system or systems with basal nitrogen. However, 55dpi (35dpf), the bacterial population of roots from pots with basal nitrogen showed a decrease (around 50cells/g of root) in comparison with the bacterial population of roots from pots added with high level of NH4NO3 (around 6×102cells/g of root) of the same plant system, and also when compared to the bacterial numbers observed in roots from plants fertilized with low levels of nitrogen (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Similar results were observed 100dpi (80dpf) in plants fertilized with high levels of nitrogen. In this case, the population of G. diazotrophicus was not detected inside the roots from pots fertilized with basal levels of NH4NO3, but bacteria were detected in roots from pots fertilized with high levels of nitrogen (around 10cells/g of root) of the same split root system. These fertilized pots are statistically similar to the bacterial numbers detected in pots from plants fertilized with basal levels of nitrogen (around 40cells/g of root) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).<elsevierMultimedia ident="fig0015"></elsevierMultimedia>DiscussionPlants require nitrogen for their development. The addition of this component produces key molecules that increase plant growth or the accumulation of metabolic compounds<a class="elsevierStyleCrossRefs" href="#bib0220">2,5,11</a>. Rhizospheric bacteria population could be modified in response to nitrogen fertilization. It has been shown that ammonium nutrition increased root colonization by Pseudomonas fluorescens 2-79RLI at the root tip and in the lateral root zone when the pH of the nutrient solution was allowed to change according to the nitrogen form provided<a class="elsevierStyleCrossRef" href="#bib0315">21</a>. In contrast, the population of G. diazotrophicus associated with sugar cane diminishes after nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0280">14,25</a>, regardless of the form of nitrogen supplemented<a class="elsevierStyleCrossRef" href="#bib0320">22</a>. This decrease could be explained by pleomorphic changes observed in G. diazotrophic cells when they grow in the presence of high levels of NH4NO3 (25mM)<a class="elsevierStyleCrossRef" href="#bib0355">29</a>. However, in accordance with this study, bacterial cells survive under this nitrogen concentration in culture media. On the other hand, it has also been suggested that the reduction in the number of bacterial cells associated with sugarcane occurs by stimulating changes in plant physiology after nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0280">14,31</a>; however, this hypothesis has not been confirmed yet. In this work, the survival of G. diazotrophicus was influenced by 44.8mM of NH4NO3 (equivalent to 640mgN/plant) irrespective of the genotype of G. diazotrophicus used (in vitro experiments). However, strain UAP5560 was more tolerant to nitrogen concentrations, showing survival with a decreased number of cells. Nitrogen concentration affecting bacterial survival (44.8mM) was higher than the level of nitrogen that affects the population associated with sugarcane (6.3mM equivalents to 180mgN/plant). Based on the results presented in this work and data previously published<a class="elsevierStyleCrossRef" href="#bib0335">25</a>, it was reasonable to propose that nitrogen fertilization induces changes in the physiology of plants that prevent G. diazotrophicus colonization. To verify this hypothesis, we carried out split root experiments to evaluate the effect of high levels of NH4NO3 when applied on one side of system, while the population of G. diazotrophicus was measured on the other side. For this experiment, strain UAP5560 was applied to the sugarcane variety MEX 57-473, given that this interaction is very stable according to previous data<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. As we had expected, G. diazotrophicus population diminished in the plants fertilized with high levels of NH4NO3. This decrease was more evident inside the roots exposed to basal levels of nitrogen, in comparison with the roots fertilized with high nitrogen levels, both in the same plant system. Moreover, this decrease in bacterial population was also evident in plant systems fertilized with low levels in both pots. These observations suggest that the effect of NH4NO3 on the population of G. diazotrophicus occurs through systemic changes in the plant, affecting the establishment of G. diazotrophicus in the roots on the other side. This observation was more evident 100dpi or 80dpf, when a decrease in the population of G. diazotrophicus was observed, due to the age of the plant<a class="elsevierStyleCrossRef" href="#bib0335">25</a>. Supplementing high levels of NH4NO3 to sugarcane plants induce a decrease in the sucrose content in stalks in early growth<a class="elsevierStyleCrossRef" href="#bib0330">24</a> and sucrose has been proposed as the principal carbon source to G. diazotrophicus<a class="elsevierStyleCrossRef" href="#bib0270">12</a>. Furthermore, NH4NO3 produces changes in the components of the apoplastic sap of sugarcane plants, including aminoacids, proteins, and sugars<a class="elsevierStyleCrossRef" href="#bib0400">38</a>. Those changes could increase during plant growth and could be related to bacterial diminution. Moreover, exopolysaccharide production is required for biofilm formation and plant colonization by G. diazotrophicus<a class="elsevierStyleCrossRef" href="#bib0325">23</a>, and the changes occurring in the plant could inhibit biofilm formation and bacteria establishment. Finally, some chemical compounds are responsible for inducing a resistance to disease in plants<a class="elsevierStyleCrossRef" href="#bib0360">30</a>, but could also induce a systemic resistance (ISR) similar to that produced by rhizobacteria<a class="elsevierStyleCrossRefs" href="#bib0405">39,41</a>, making it conceivable that NH4NO3 could elicit ISR and prevent the colonization of G. diazotrophicus in sugarcane<a class="elsevierStyleCrossRef" href="#bib0290">16</a>. The nitrogen effect over the population of G. diazotrophicus is more evident inside the plant than in the rhizosphere (<a class="elsevierStyleCrossRefs" href="#fig0010">Figs. 2 and 3</a>). This could be due to physiological changes occurring inside the plant and directly affecting the bacterial population; however, in the rhizosphere, firstly the metabolites have to be exported to provoke changes in the environment.Taken together, the results in this study show that the decrease of G. diazotrophicus associated with sugarcane occurs due to changes in the physiology of the plant rather than by the direct effect that NH4NO3 could exert on bacterial cells.Ethical disclosuresProtection of human and animal subjectsThe authors declare that no experiments were performed on humans or animals for this study.Confidentiality of dataThe authors declare that no patient data appear in this article.Right to privacy and informed consentThe authors declare that no patient data appear in this article.Conflict of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres602693" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec616747" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres602692" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec616748" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Experiment 1. In vitro assays" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Experiment 2. Plant assays" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Statistical analysis" ] ] ] 6 => array:3 [ "identificador" => "sec0030" "titulo" => "Results" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Effect of NHNO on G. diazotrophicus strains in vitro" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "Effect of NHNO on the colonization of sugarcane testing G. diazotrophicus PAl 5 in split root experiments" ] ] ] 7 => array:2 [ "identificador" => "sec0045" "titulo" => "Discussion" ] 8 => array:3 [ "identificador" => "sec0050" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0055" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0060" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0065" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0070" "titulo" => "Conflict of interest" ] 10 => array:2 [ "identificador" => "xack202831" "titulo" => "Acknowledgments" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2014-10-16" "fechaAceptado" => "2015-09-29" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec616747" "palabras" => array:5 [ 0 => "Nitrogen fertilization" 1 => "Bacterial population" 2 => "G. diazotrophicus" 3 => "Sugarcane" 4 => "Plant growth promoting bacteria" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec616748" "palabras" => array:5 [ 0 => "Fertilización nitrogenada" 1 => "Población bacteriana" 2 => "G. diazotrophicus" 3 => "Caña de azúcar" 4 => "Bacterias promotoras del crecimiento de plantas" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "It has been established that a decrease in the population of Gluconacetobacter diazotrophicus associated with sugarcane occurs after nitrogen fertilization. This fact could be due to a direct influence of NH4NO3 on bacterial cells or to changes in plant physiology after fertilizer addition, affecting bacterial establishment. In this work, we observed that survival of G. diazotrophicus was directly influenced when 44.8mM of NH4NO3 (640mgN/plant) was used for in vitro experiments. Furthermore, micropropagated sugarcane plantlets were inoculated with G. diazotrophicus and used for split root experiments, in which both ends of the system were fertilized with a basal level of NH4NO3 (0.35mM; 10mgN/plant). Twenty days post inoculation (dpi) one half of the plants were fertilized with a high dose of NH4NO3 (6.3mM; 180mgN/plant) on one end of the system. This nitrogen level was lower than that directly affecting G. diazotrophicus cells; however, it caused a decrease in the bacterial population in comparison with control plants fertilized with basal nitrogen levels. The decrease in the population of G. diazotrophicus was higher in pots fertilized with a basal nitrogen level when compared with the corresponding end supplied with high levels of NH4NO3 (100dpi; 80 days post fertilization) of the same plant system. These observations suggest that the high nitrogen level added to the plants induce systemic physiological changes that affect the establishment of G. diazotrophicus." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La población de Gluconacetobacter diazotrophicus asociada a la caña de azúcar disminuye después de la fertilización nitrogenada, lo cual podría ocurrir por la influencia directa del NH4NO3 sobre la supervivencia bacteriana, o por cambios en la fisiología de las plantas, que impiden el establecimiento bacteriano. En el presente trabajo se observó que en experimentos in vitro la supervivencia de G. diazotrophicus fue influenciada por 44,8mM de NH4NO3 (640mgN/plant). Además, G. diazotrophicus fue inoculado en plántulas micropropagadas de caña de azúcar, que fueron usadas para realizar experimentos de raíz dividida, en las que ambos extremos de los sistemas se fertilizaron con un nivel basal de NH4NO3 (0,35mM; 10mgN/planta). A los 20 días posteriores a la inoculación (dpi), la mitad de plantas fueron fertilizadas en uno de sus extremos con una dosis elevada de NH4NO3 (6,3mM; 180mg of N/plant). Este nivel fue menor al que afectó directamente a las células de G. diazotrophicus; sin embargo, provocó una disminución de la población bacteriana en comparación con plantas testigo fertilizadas con niveles basales de nitrógeno. La disminución de la población fue mayor para raíces fertilizadas con un nivel basal de nitrógeno en comparación con las raíces fertilizadas con altos niveles del mismo sistema de plantas (100dpi; 80días posfertilización). Estas observaciones indican que el alto nivel de nitrógeno añadido a las plantas inducen cambios fisiológicos sistémicos que afectan el establecimiento de G. diazotrophicus." ] ] "multimedia" => array:5 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 870 "Ancho" => 1817 "Tamanyo" => 250023 ] ] "descripcion" => array:1 [ "en" => "Scheme representing the system used for the split root experiments (A). After G. diazotrophicus inoculation, the root of each plant was divided and placed in 2 pots. At 20dpi half of the plants were supplemented with high doses of NH4NO3 on one side of the system. Images from plants in the split root experiment (B), in the greenhouse (C) and one plant at 35dpi before the bacterial count (D)." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 3357 "Ancho" => 2389 "Tamanyo" => 262364 ] ] "descripcion" => array:1 [ "en" => "Rhizospheric bacterial populations in split root experiments. Each value represents the media of data for five independent plants (Log of cell number/gV) with the respective standard deviation. Mean values with equal letters are not statistically different at p≤0.05, using the t-Student test. dpi: days post inoculation; dpf: days post fertilization; N+: addition of 180mg of nitrogen/plant." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 3411 "Ancho" => 2383 "Tamanyo" => 255487 ] ] "descripcion" => array:1 [ "en" => "Bacterial population inside roots in split root experiments. Each value represents the media of data for five independent plants (Log of cell number/g root) with the respective standard deviation. Mean values with equal letters are not statistically different at p≤0.05, using the t-Student test. dpi: days post inoculation; dpf: days post fertilization; ND: not detected; N+: addition of 180mg of nitrogen/plant." ] ] 3 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "Values correspond to the media of five independent samples determined by the DPSM method. Mean values with equal letters are not statistically different at p≤0.05, using the t-Student test. SD: standard deviation." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">[NH4NO3] mM \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Log CFU/ml (SD)</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 5T \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 3 \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">UAP 5560 \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">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.43 (±0.63)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.00 (±0.62)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.09 (±0.30)A \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">0.35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.79 (±0.17)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.09 (±0.35)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.16 (±0.15)A \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">0.7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.05 (±0.31)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.09 (±0.36)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.79 (±0.17)A \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">1.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.31 (±0.15)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.44 (±0.08)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.89 (±0.17)A \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">2.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.01 (±0.27)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.20 (±0.17)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.16 (±0.27)A \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">5.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.95 (±0.24)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.31 (±0.28)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.95 (±0.24)A \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">11.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.29 (±0.35)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.33 (±0.05)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.05 (±0.35)A \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">22.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.72 (±0.30)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">9.41 (±0.12)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.85 (±0.11)A \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">44.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5.02 (±0.25)B \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">89.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">5.07 (±0.05)B \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">179.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 C \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab986775.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Bacterial number of three strains of G. diazotrophicus grown in solid LGI media supplemented with different NH4NO3 concentrations" ] ] 4 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:2 [ "leyenda" => "Values correspond to the media of five independent samples determined by the MPN method using a McCrady table with three replicate vials for all dilutions of each sample. Mean values with equal letters are not statistically different at p≤0.05, using the t-Student test. SD: standard deviation." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">[NH4NO3] mM \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Log of cell number/ml (SD)</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 5T \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 3 \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">UAP 5560 \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">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.57 (±0.43)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.51 (±0.43)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.49 (±0.30)A \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">0.35 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.43 (±0.37)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.47 (±0.35)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.27 (±0.13)A \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">0.7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.43 (±0.31)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.44 (±0.41)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.43 (±0.31)A \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">1.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.46 (±0.35)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.29 (±0.36)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.28 (±0.32)A \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">2.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.40 (±0.27)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.33 (±0.38)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.21 (±0.42)A \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">5.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.38 (±0.34)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.26 (±0.37)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.25 (±0.33)A \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">11.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.32 (±0.35)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.13 (±0.25)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.13 (±0.38)A \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">22.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.32 (±0.44)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.17 (±0.32)A \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8.15 (±0.40)A \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">44.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2.56 (±0.32)B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2.62 (±0.44)B \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">2.57 (±0.35)B \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">89.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">1.03 (±0.45)C \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">179.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 D \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">0 D \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab986776.png" ] ] ] ] "descripcion" => array:1 [ 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La disminución de la población de Gluconacetobacter diazotrophicus en caña de azúcar, después de la fertilización nitrogenada, está relacionada con la fisiología de las plantas en experimentos de raíz dividida

Osvaldo Rodríguez-Andrade, Luis E. Fuentes-Ramírez, Yolanda E. Morales-García, Dalia Molina-Romero, María R. Bustillos-Cristales, Rebeca D. Martínez-Contreras, Jesús Muñoz-Rojas

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joymerre@yahoo.com.mx

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Laboratorio Ecología Molecular Microbiana, Centro de Investigaciones en Ciencias Microbiológicas (CICM)-Instituto de Ciencias (IC), Benemérita Universidad Autónoma de Puebla (BUAP), Puebla, México

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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Bacterial population inside roots in split root experiments&#46; Each value represents the media of data for five independent plants &#40;Log of cell number&#47;g root&#41; with the respective standard deviation&#46; Mean values with equal letters are not statistically different at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; using the <span class="elsevierStyleItalic">t</span>-Student test&#46; dpi&#58; days post inoculation&#59; dpf&#58; days post fertilization&#59; ND&#58; not detected&#59; N&#43;&#58; addition of 180<span class="elsevierStyleHsp" style=""></span>mg of nitrogen&#47;plant&#46;</p>"
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<span class="elsevierStyleItalic">Saccharococcus sachari</span><a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">3&#44;31</span></a>&#44; <span class="elsevierStyleItalic">Eleusine coracana</span><a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">18</span></a>&#44; pineapple<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">37</span></a>&#44; and also from the rhizosphere of <span class="elsevierStyleItalic">Coffea arabica</span><a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">17</span></a>&#46; More recently this bacterium was isolated from wetland rice<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">27</span></a>&#44; carrot&#44; raddish and beetroot<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">19</span></a> and was related to a dominant phylotype detected as endophyte from needles of <span class="elsevierStyleItalic">Pinus flexilis</span> and <span class="elsevierStyleItalic">Picea engelmannii</span> using 16S rRNA pyrosequencing<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">9</span></a>&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">G&#46; diazotrophicus</span> is a nitrogen fixing bacterium that produces phytohormones&#44; such as indol acetic acid<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">15&#44;32&#44;33</span></a> and gibberellins<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">4</span></a>&#46; This bacterial species is able to stimulate the growth of sugarcane after its inoculation<a class="elsevierStyleCrossRefs" href="#bib0335"><span class="elsevierStyleSup">25&#44;35&#44;36&#44;40</span></a>&#46; The principal mechanism for stimulating plant growth occurs through the auxinic via<a class="elsevierStyleCrossRefs" href="#bib0370"><span class="elsevierStyleSup">32&#44;35</span></a> and depends on the sugarcane variety and the genotype of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span><a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Isolation of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> from sugarcane plants depends on the amount of nitrogen fertilization applied to the crops&#58; the higher the level of nitrogen applied to the crops&#44; the lower the probability to isolate <span class="elsevierStyleItalic">G&#46; diazotrophicus</span><a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">14&#44;28&#44;31</span></a>&#46; In addition&#44; seven genotypes of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> associated with sugarcane plants fertilized with low levels of nitrogen were identified in Brazilian fields and the diversity between them seemed to be affected by the high levels of nitrogen applied to sugarcane crops<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">7</span></a> while only one genotype was detected in sugarcane plants fertilized with high levels of nitrogen in Mexican fields&#46; Moreover&#44; <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> colonization is reduced in plants fertilized with high doses of nitrogen<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">14&#44;22&#44;25</span></a>&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The decrease in the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> associated with sugarcane plants could be due to pleomorphic changes that occur while culturing bacteria in the presence of high nitrogen concentrations<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">29</span></a>&#46; Additionally&#44; it has been proposed that the decrease in the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> associated with sugarcane could be due to physiological changes that the plant suffers in the presence of high nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">7&#44;14</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Split root experiments have been developed to evaluate the systemic effect of a specific substance on plants&#44; when this substance is supplied only on one end of the plant&#44; while the other end could be used as control<a class="elsevierStyleCrossRef" href="#bib0420"><span class="elsevierStyleSup">42</span></a>&#44; but also to evaluate the systemic effect on plant pathogens due to the action of the induced systemic resistance produced by rhizobacteria<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">1</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">In this work we show a statistical analysis of the behavior of the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> present inside the roots and in the rhizosphere using split root experiments&#44; both at high or low nitrogen levels in the form of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span>&#46; In accordance with our results&#44; the negative effect of nitrogen on the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> is influenced by the plant&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><p id="par0035" class="elsevierStylePara elsevierViewall">Bacterial strains used for <span class="elsevierStyleItalic">in vitro</span> studies were <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span>&#44; PAl 3 and UAP 5560&#44; each one corresponding to a different genotype&#46; PAl 5<span class="elsevierStyleSup">T</span> represents the predominant genotype isolated from different Brazilian sugarcane varieties &#40;ET 3&#41;&#44; PAl 3 corresponds to a rare genotype not frequently isolated &#40;ET 5&#41; and UAP 5560 is the predominant genotype isolated from different Mexican sugarcane varieties &#40;ET1&#41;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">7</span></a>&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Experiment 1&#46; <span class="elsevierStyleItalic">In vitro</span> assays</span><p id="par0040" class="elsevierStylePara elsevierViewall">The ability of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> strains to grow at different nitrogen concentrations was explored in two <span class="elsevierStyleItalic">in vitro</span> conditions&#58; one using LGI solid Plates<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">8</span></a> supplemented with different concentrations of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> and the other using semisolid LGI medium<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">8</span></a> supplemented with different concentrations of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;Sigma&#8211;Aldrich A3795&#41;&#46; In the first case&#44; bacteria were grown until stationary phase &#40;five independent growth tubes by strain&#41; in MESMA liquid medium<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">14</span></a> for 48<span class="elsevierStyleHsp" style=""></span>h at 30<span class="elsevierStyleHsp" style=""></span>&#176;C and 200<span class="elsevierStyleHsp" style=""></span>rpm&#46; Cells were washed twice by centrifugation and resuspended in MgSO<span class="elsevierStyleInf">4</span> 10<span class="elsevierStyleHsp" style=""></span>mM &#40;Sigma&#8211;Aldrich M7506&#41;&#46; Each bacterial suspension was serially diluted &#40;factor 1&#58;10&#41; and dilutions were placed in plates at different NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> concentrations&#46; Bacterial population was quantified by the DPSM method<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">10</span></a>&#46; For the second condition&#44; bacterial strains were grown until stationary phase &#40;five independent growth tubes by strain&#41;&#44; in 150<span class="elsevierStyleHsp" style=""></span>ml of MESMA liquid medium&#44; for 48<span class="elsevierStyleHsp" style=""></span>h at 30<span class="elsevierStyleHsp" style=""></span>&#176;C and 200<span class="elsevierStyleHsp" style=""></span>rpm&#46; Each washed bacterial suspension was serially diluted &#40;factor 1&#58;10&#41; and 100<span class="elsevierStyleHsp" style=""></span>&#956;l of each dilution were placed in series of semisolid LGI tubes in triplicate<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a> containing the amount of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> assessed &#40;data observed in <a class="elsevierStyleCrossRefs" href="#tbl0005">Tables 1 and 2</a>&#41;&#46; Quantification was carried out by the most probable number method &#40;MPN&#41; using a McCrady table with three replicate vials for each dilution&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Experiment 2&#46; Plant assays</span><p id="par0045" class="elsevierStylePara elsevierViewall">The effect of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on bacterial association with sugarcane was assessed with the use of split root experiments&#46; For this purpose&#44; sugarcane plantlets variety MEX 57-473 were obtained by micropropagation as described previously<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; Micropropagated plantlets were free from bacteria&#46; Forty plantlets were inoculated with <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span> strain by immersion of roots for 1<span class="elsevierStyleHsp" style=""></span>h in the bacterial suspension &#40;5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">8</span><span class="elsevierStyleHsp" style=""></span>UFC&#47;ml&#41;&#46; Forty plantlets were used as non-inoculated controls and were only immersed in distilled sterile water&#46; To obtain the bacterial suspension&#44; <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span> was grown in 10 flasks containing 35<span class="elsevierStyleHsp" style=""></span>ml of TESMA medium until stationary phase&#44; cells were washed by centrifugation twice&#59; after&#44; the pellet was resuspended in 35<span class="elsevierStyleHsp" style=""></span>ml of MgSO<span class="elsevierStyleInf">4</span> &#40;10<span class="elsevierStyleHsp" style=""></span>mM&#41; and mixed to obtain 350<span class="elsevierStyleHsp" style=""></span>ml of bacterial suspension&#46; Ten milliliters of this suspension were dispensed in tubes of 25<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>2&#46;5<span class="elsevierStyleHsp" style=""></span>cm and a single tube was used to inoculate each sugarcane plantlet&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">After inoculation&#44; both inoculated and non-inoculated plantlets were placed in sterile split root systems &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#44; each consisting of two pots joined by the upper part&#46; Each pot had 500<span class="elsevierStyleHsp" style=""></span>ml capacity and contained sterile vermiculite&#46; For each plant&#44; half of the roots were placed in pot 1 and the other half in pot 2&#44; approximately 3 roots in each pot&#46; The split root systems were watered in both pots with enough water and low doses of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;10<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant equivalent to 0&#46;35<span class="elsevierStyleHsp" style=""></span>mM&#41; and mineral salts&#44; according to Mu&#241;oz-Rojas and Caballero-Mellado<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; The pots were covered with aluminum foil&#44; and the zone where the plants emerged was protected with sterile cotton&#46; The plantlets were maintained under greenhouse conditions with controlled temperature &#40;26&#8211;30<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; with a light&#47;dark photoperiod of 16&#47;8<span class="elsevierStyleHsp" style=""></span>h&#46; Twenty days after inoculation &#40;dpi&#41; the bacterial number was determined for five plants both in their rhizospheres and inside the roots&#46; At 20<span class="elsevierStyleHsp" style=""></span>dpi&#44; 15 plants of each treatment &#40;inoculated and non-inoculated&#41; were supplemented with a high dose of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> in one of the pots &#40;180<span class="elsevierStyleHsp" style=""></span>mg of N&#47;plant equivalent to 6&#46;3<span class="elsevierStyleHsp" style=""></span>mM&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41; under sterile conditions&#46; Plants were again maintained under greenhouse conditions and watered periodically with distilled sterile water&#46; Rhizospheric and endophytic bacteria were recovered from the two pots for each plant system and the population was determined at 35&#44; 55 and 100<span class="elsevierStyleHsp" style=""></span>dpi&#44; equivalent to 15&#44; 35 and 80 days post fertilization &#40;dpf&#41;&#46; Bacterial number was determined as described previously by the most probable number method using a McCrady table with three replicate vials for each dilution<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; For this purpose&#44; five independent plants or systems for each treatment &#40;inoculated and non-inoculated&#41; and treatments at different nitrogen levels were analyzed in each time&#46; The plants were carefully removed from the vermiculite&#44; each side of the root system was placed in an independent sterile container&#44; and the root was shaken to discard vermiculite that was not adhered&#46; The resultant root-vermiculite was submerged in enough sterile water &#40;covering the root&#41; and vortexed to maximal velocity for 40<span class="elsevierStyleHsp" style=""></span>s&#58; the suspension was used to perform rhizospheric bacterial quantification&#46; Vermiculite weight was obtained by drying samples without the roots&#46; Furthermore&#44; for endophytic bacteria quantification&#44; each root was placed in a sterile bottle&#44; washed to discard vermiculite and disinfected with 70&#37; ethanol for 30<span class="elsevierStyleHsp" style=""></span>s&#46; Then the roots were rinsed with distilled water and the surface was sterilized with a 1&#46;5<span class="elsevierStyleHsp" style=""></span>&#37; sodium hypochlorite solution &#40;Sigma&#8211;Aldrich 425044&#41; for 20<span class="elsevierStyleHsp" style=""></span>min&#46; Later&#44; the roots were rinsed six times with sterile distilled water under sterile conditions&#46; Fresh roots were macerated in water in 1&#58;10 &#40;w&#47;v&#41; proportion&#46; Each sample used for bacterial quantification was diluted &#40;factor 1&#58;10&#41; until dilution 1&#58;1&#44;000&#44;000 and after&#44; 100<span class="elsevierStyleHsp" style=""></span>&#956;l of each dilution were placed in a tube containing semisolid LGI medium &#40;without nitrogen for the growth of diazotrophic bacteria&#41;&#44; three tubes were dispensed&#46; After bacterial growth&#44; positive and negative tubes were registered&#59; the presence of a yellow pellicle at the top of the LGI semisolid medium&#44; was recorded as a positive tube<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">8&#44;25&#44;27</span></a>&#46; In addition&#44; acidification of the media was observed with color changes from green to yellow&#44; which is characteristic of <span class="elsevierStyleItalic">G&#46; diazotrophic</span> growth&#59; furthermore&#44; after 7 days the yellow color was absorbed by bacteria<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">8</span></a>&#46; The estimation of the bacterial number of each sample was carried out by the most probable number method using a McCrady table with three replicate vials for each dilution &#40;with a confidence limit of 95<span class="elsevierStyleHsp" style=""></span>&#37;&#41;&#46; For rhizospheric bacteria quantification&#44; the value obtained from the McCrady table was multiplied per 10 and the dilution factor was considered in order to obtain the number of bacterial cells&#47;ml of liquid suspension &#40;sample&#41;&#46; This value was multiplied per the initial water volume where the root was vortexed and divided by the amount in grams &#40;g&#41; of vermiculite &#40;V&#41; present in the suspension &#40;considered as the adhered soil to the roots&#41;<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; The final quantified values obtained were stated as the number of cells&#47;g<span class="elsevierStyleHsp" style=""></span>V&#46; To assess endophytic bacteria quantification&#44; the value obtained from the McCrady table&#44; was multiplied by 10 and the dilution factor was considered in order to obtain the number of bacterial cells&#47;ml of liquid suspension &#40;sample&#41;&#59; later this value was multiplied by 10 due to initial dilution &#40;w&#47;v&#41; of fresh roots for each side of the root systems&#46; Each bacterial number value obtained was transformed to logarithmic form for statistical purposes&#46; All treatments explored in the present work had five bacterial number values which were used to calculate the standard deviation and the statistical analysis&#46; To ensure that quantified bacteria corresponded to <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span>&#44; its ability to inhibit a sensitive strain &#40;PAl 3&#41; was checked and electrophoretic mobility patterns of 12 metabolic enzymes were compared with a reference strain<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">6&#44;7&#44;17</span></a>&#46; To achieve this goal&#44; some positive tubes of semisolid LGI media with characteristic growth of <span class="elsevierStyleItalic">G&#46; diazortrophicus</span>&#44; were used to streak the bacteria pellicle on solid plates of LGI media and selected colonies were assessed for their ability to inhibit a sensitive strain by the double agar layer method<a class="elsevierStyleCrossRefs" href="#bib0310"><span class="elsevierStyleSup">20&#44;26</span></a>&#46; All selected isolates were able to inhibit the growth of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 3 &#40;an antagonistic characteristic of strain PAl 5<span class="elsevierStyleSup">T</span>&#41;&#44; and they also had the same pattern of electrophoretic mobility of the metabolic enzymes explored&#44; as the reference strain <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span> &#40;data not shown&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Statistical analysis</span><p id="par0055" class="elsevierStylePara elsevierViewall">Data corresponding to each treatment for the different experiments were statistically compared in pairs with the <span class="elsevierStyleItalic">t</span>-Student test&#44; using Sigma Plot of the Jandel Scientific Software&#46; Results of comparison were used to generate a matrix of differences and similarities between treatments for assignment of letters &#40;data not shown&#41;&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Results</span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Effect of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> strains <span class="elsevierStyleItalic">in vitro</span></span><p id="par0060" class="elsevierStylePara elsevierViewall">The three strains of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> explored &#40;PAl 5<span class="elsevierStyleSup">T</span>&#44; PAl 3 and UAP 5560&#41; were able to grow in solid media until 22&#46;4<span class="elsevierStyleHsp" style=""></span>mM of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#44; which is a high nitrogen level and corresponds to 640<span class="elsevierStyleHsp" style=""></span>mg of N&#47;plant&#46; The statistical analysis showed no differences between bacteria grown in the presence of 22&#46;4<span class="elsevierStyleHsp" style=""></span>mM of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> in comparison with normal LGI&#46; <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> UAP 5560 tolerated a concentration of 89&#46;6<span class="elsevierStyleHsp" style=""></span>mM in solid LGI&#44; but the bacterial number was reduced from 10<span class="elsevierStyleSup">8</span> to 10<span class="elsevierStyleSup">5</span><span class="elsevierStyleHsp" style=""></span>CFU&#47;ml &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; In semisolid LGI medium it was also observed that the three strains of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> explored were able to grow until 22&#46;4<span class="elsevierStyleHsp" style=""></span>mM of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#59; the growth of the strains was affected at 44&#46;8<span class="elsevierStyleHsp" style=""></span>mM in the order of 10<span class="elsevierStyleSup">2</span><span class="elsevierStyleHsp" style=""></span>cells&#47;ml and the growth of UAP 5560 also tolerated better than others the presence of high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;89&#46;6<span class="elsevierStyleHsp" style=""></span>mM&#41;&#59; however&#44; under this condition bacterial numbers diminished in the order of 10<span class="elsevierStyleSup">1</span><span class="elsevierStyleHsp" style=""></span>cells&#47;ml&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Effect of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on the colonization of sugarcane testing <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span> in split root experiments</span><p id="par0065" class="elsevierStylePara elsevierViewall">The analysis of the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> strain PAl 5<span class="elsevierStyleSup">T</span> was carried out using the sugarcane variety MEX-57473 with split root experiments both in rhizospheres as endophytically&#46; Bacteria were not detected in non-inoculated control plants&#46; Rhizospheric population was similar in both sides of the root systems at 20<span class="elsevierStyleHsp" style=""></span>dpi&#44; about 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span><span class="elsevierStyleHsp" style=""></span>cells&#47;g vermiculite &#40;V&#41; when basal levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> were present&#46; No statistical differences were observed at 35<span class="elsevierStyleHsp" style=""></span>dpi &#40;15<span class="elsevierStyleHsp" style=""></span>dpf&#41; in the rhizospheric population between both sides of the system&#44; neither between treatments fertilized with high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> in comparison to those fertilized with basal levels&#46; Furthermore&#44; there were no differences when comparing the same treatments 20<span class="elsevierStyleHsp" style=""></span>dpi &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; In accordance with our data&#44; bacterial rhizospheric population decreased at 55<span class="elsevierStyleHsp" style=""></span>dpi &#40;35<span class="elsevierStyleHsp" style=""></span>dpf&#41; in plants fertilized with high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> when compared to the initial population observed in plants at 20<span class="elsevierStyleHsp" style=""></span>dpi&#46; However&#44; no differences were observed between the bacterial numbers recovered from each side of the split root systems neither for the plants fertilized with high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> nor for the plants treated with basal levels&#46; Interestingly&#44; at 100<span class="elsevierStyleHsp" style=""></span>dpi &#40;80<span class="elsevierStyleHsp" style=""></span>dpf&#41;&#44; fertilized plants with high levels of nitrogen had differences in rhizospheric population&#44; detecting low bacterial numbers &#40;around 1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">4</span><span class="elsevierStyleHsp" style=""></span>cells&#47;g<span class="elsevierStyleHsp" style=""></span>V&#41; in the pot fertilized with basal nitrogen in comparison with the bacterial numbers detected in the other pot of the system and also when compared to the bacterial numbers of both pots from plants fertilized with low levels of nitrogen&#44; in the order of 10<span class="elsevierStyleSup">5</span><span class="elsevierStyleHsp" style=""></span>cells&#47;g<span class="elsevierStyleHsp" style=""></span>V &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">The effect of nitrogen on the endophytic population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> PAl 5<span class="elsevierStyleSup">T</span> was more evident &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; Inside the roots&#44; the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was detected in the order of 10<span class="elsevierStyleSup">3</span><span class="elsevierStyleHsp" style=""></span>cells&#47;g of root at 20<span class="elsevierStyleHsp" style=""></span>dpi&#46; After the addition of high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> in one pot of the split root systems corresponding to the treated plants containing high levels of nitrogen&#44; no changes were observed in the bacterial population measured 35<span class="elsevierStyleHsp" style=""></span>dpi &#40;15<span class="elsevierStyleHsp" style=""></span>dpf&#41; when comparing pots of the same system or systems with basal nitrogen&#46; However&#44; 55<span class="elsevierStyleHsp" style=""></span>dpi &#40;35<span class="elsevierStyleHsp" style=""></span>dpf&#41;&#44; the bacterial population of roots from pots with basal nitrogen showed a decrease &#40;around 50<span class="elsevierStyleHsp" style=""></span>cells&#47;g of root&#41; in comparison with the bacterial population of roots from pots added with high level of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;around 6<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">2</span><span class="elsevierStyleHsp" style=""></span>cells&#47;g of root&#41; of the same plant system&#44; and also when compared to the bacterial numbers observed in roots from plants fertilized with low levels of nitrogen &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; Similar results were observed 100<span class="elsevierStyleHsp" style=""></span>dpi &#40;80<span class="elsevierStyleHsp" style=""></span>dpf&#41; in plants fertilized with high levels of nitrogen&#46; In this case&#44; the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was not detected inside the roots from pots fertilized with basal levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span>&#44; but bacteria were detected in roots from pots fertilized with high levels of nitrogen &#40;around 10<span class="elsevierStyleHsp" style=""></span>cells&#47;g of root&#41; of the same split root system&#46; These fertilized pots are statistically similar to the bacterial numbers detected in pots from plants fertilized with basal levels of nitrogen &#40;around 40<span class="elsevierStyleHsp" style=""></span>cells&#47;g of root&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Discussion</span><p id="par0075" class="elsevierStylePara elsevierViewall">Plants require nitrogen for their development&#46; The addition of this component produces key molecules that increase plant growth or the accumulation of metabolic compounds<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">2&#44;5&#44;11</span></a>&#46; Rhizospheric bacteria population could be modified in response to nitrogen fertilization&#46; It has been shown that ammonium nutrition increased root colonization by <span class="elsevierStyleItalic">Pseudomonas fluorescens</span> 2-79RLI at the root tip and in the lateral root zone when the pH of the nutrient solution was allowed to change according to the nitrogen form provided<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">21</span></a>&#46; In contrast&#44; the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> associated with sugar cane diminishes after nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">14&#44;25</span></a>&#44; regardless of the form of nitrogen supplemented<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">22</span></a>&#46; This decrease could be explained by pleomorphic changes observed in <span class="elsevierStyleItalic">G&#46; diazotrophic</span> cells when they grow in the presence of high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;25<span class="elsevierStyleHsp" style=""></span>mM&#41;<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">29</span></a>&#46; However&#44; in accordance with this study&#44; bacterial cells survive under this nitrogen concentration in culture media&#46; On the other hand&#44; it has also been suggested that the reduction in the number of bacterial cells associated with sugarcane occurs by stimulating changes in plant physiology after nitrogen fertilization<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">14&#44;31</span></a>&#59; however&#44; this hypothesis has not been confirmed yet&#46; In this work&#44; the survival of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was influenced by 44&#46;8<span class="elsevierStyleHsp" style=""></span>mM of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;equivalent to 640<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41; irrespective of the genotype of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> used &#40;<span class="elsevierStyleItalic">in vitro</span> experiments&#41;&#46; However&#44; strain UAP5560 was more tolerant to nitrogen concentrations&#44; showing survival with a decreased number of cells&#46; Nitrogen concentration affecting bacterial survival &#40;44&#46;8<span class="elsevierStyleHsp" style=""></span>mM&#41; was higher than the level of nitrogen that affects the population associated with sugarcane &#40;6&#46;3<span class="elsevierStyleHsp" style=""></span>mM equivalents to 180<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41;&#46; Based on the results presented in this work and data previously published<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#44; it was reasonable to propose that nitrogen fertilization induces changes in the physiology of plants that prevent <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> colonization&#46; To verify this hypothesis&#44; we carried out split root experiments to evaluate the effect of high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> when applied on one side of system&#44; while the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was measured on the other side&#46; For this experiment&#44; strain UAP5560 was applied to the sugarcane variety MEX 57-473&#44; given that this interaction is very stable according to previous data<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; As we had expected&#44; <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> population diminished in the plants fertilized with high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span>&#46; This decrease was more evident inside the roots exposed to basal levels of nitrogen&#44; in comparison with the roots fertilized with high nitrogen levels&#44; both in the same plant system&#46; Moreover&#44; this decrease in bacterial population was also evident in plant systems fertilized with low levels in both pots&#46; These observations suggest that the effect of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> occurs through systemic changes in the plant&#44; affecting the establishment of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> in the roots on the other side&#46; This observation was more evident 100<span class="elsevierStyleHsp" style=""></span>dpi or 80<span class="elsevierStyleHsp" style=""></span>dpf&#44; when a decrease in the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was observed&#44; due to the age of the plant<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">25</span></a>&#46; Supplementing high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> to sugarcane plants induce a decrease in the sucrose content in stalks in early growth<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">24</span></a> and sucrose has been proposed as the principal carbon source to <span class="elsevierStyleItalic">G&#46; diazotrophicus</span><a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">12</span></a>&#46; Furthermore&#44; NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> produces changes in the components of the apoplastic sap of sugarcane plants&#44; including aminoacids&#44; proteins&#44; and sugars<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">38</span></a>&#46; Those changes could increase during plant growth and could be related to bacterial diminution&#46; Moreover&#44; exopolysaccharide production is required for biofilm formation and plant colonization by <span class="elsevierStyleItalic">G&#46; diazotrophicus</span><a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">23</span></a>&#44; and the changes occurring in the plant could inhibit biofilm formation and bacteria establishment&#46; Finally&#44; some chemical compounds are responsible for inducing a resistance to disease in plants<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">30</span></a>&#44; but could also induce a systemic resistance &#40;ISR&#41; similar to that produced by rhizobacteria<a class="elsevierStyleCrossRefs" href="#bib0405"><span class="elsevierStyleSup">39&#44;41</span></a>&#44; making it conceivable that NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> could elicit ISR and prevent the colonization of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> in sugarcane<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">16</span></a>&#46; The nitrogen effect over the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> is more evident inside the plant than in the rhizosphere &#40;<a class="elsevierStyleCrossRefs" href="#fig0010">Figs&#46; 2 and 3</a>&#41;&#46; This could be due to physiological changes occurring inside the plant and directly affecting the bacterial population&#59; however&#44; in the rhizosphere&#44; firstly the metabolites have to be exported to provoke changes in the environment&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Taken together&#44; the results in this study show that the decrease of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> associated with sugarcane occurs due to changes in the physiology of the plant rather than by the direct effect that NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> could exert on bacterial cells&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Ethical disclosures</span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Protection of human and animal subjects</span><p id="par0085" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Confidentiality of data</span><p id="par0090" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Right to privacy and informed consent</span><p id="par0095" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conflict of interest</span><p id="par0100" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
      "secciones" => array:12 [
        0 => array:3 [
          "identificador" => "xres602693"
          "titulo" => "Abstract"
          "secciones" => array:1 [
            0 => array:1 [
              "identificador" => "abst0005"
            ]
          ]
        ]
        1 => array:2 [
          "identificador" => "xpalclavsec616747"
          "titulo" => "Keywords"
        ]
        2 => array:3 [
          "identificador" => "xres602692"
          "titulo" => "Resumen"
          "secciones" => array:1 [
            0 => array:1 [
              "identificador" => "abst0010"
            ]
          ]
        ]
        3 => array:2 [
          "identificador" => "xpalclavsec616748"
          "titulo" => "Palabras clave"
        ]
        4 => array:2 [
          "identificador" => "sec0005"
          "titulo" => "Introduction"
        ]
        5 => array:3 [
          "identificador" => "sec0010"
          "titulo" => "Materials and methods"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Experiment 1&#46; In vitro assays"
            ]
            1 => array:2 [
              "identificador" => "sec0020"
              "titulo" => "Experiment 2&#46; Plant assays"
            ]
            2 => array:2 [
              "identificador" => "sec0025"
              "titulo" => "Statistical analysis"
            ]
          ]
        ]
        6 => array:3 [
          "identificador" => "sec0030"
          "titulo" => "Results"
          "secciones" => array:2 [
            0 => array:2 [
              "identificador" => "sec0035"
              "titulo" => "Effect of NHNO on G&#46; diazotrophicus strains in vitro"
            ]
            1 => array:2 [
              "identificador" => "sec0040"
              "titulo" => "Effect of NHNO on the colonization of sugarcane testing G&#46; diazotrophicus PAl 5 in split root experiments"
            ]
          ]
        ]
        7 => array:2 [
          "identificador" => "sec0045"
          "titulo" => "Discussion"
        ]
        8 => array:3 [
          "identificador" => "sec0050"
          "titulo" => "Ethical disclosures"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "sec0055"
              "titulo" => "Protection of human and animal subjects"
            ]
            1 => array:2 [
              "identificador" => "sec0060"
              "titulo" => "Confidentiality of data"
            ]
            2 => array:2 [
              "identificador" => "sec0065"
              "titulo" => "Right to privacy and informed consent"
            ]
          ]
        ]
        9 => array:2 [
          "identificador" => "sec0070"
          "titulo" => "Conflict of interest"
        ]
        10 => array:2 [
          "identificador" => "xack202831"
          "titulo" => "Acknowledgments"
        ]
        11 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2014-10-16"
    "fechaAceptado" => "2015-09-29"
    "PalabrasClave" => array:2 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec616747"
          "palabras" => array:5 [
            0 => "Nitrogen fertilization"
            1 => "Bacterial population"
            2 => "<span class="elsevierStyleItalic">G&#46; diazotrophicus</span>"
            3 => "Sugarcane"
            4 => "Plant growth promoting bacteria"
          ]
        ]
      ]
      "es" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec616748"
          "palabras" => array:5 [
            0 => "Fertilizaci&#243;n nitrogenada"
            1 => "Poblaci&#243;n bacteriana"
            2 => "<span class="elsevierStyleItalic">G&#46; diazotrophicus</span>"
            3 => "Ca&#241;a de az&#250;car"
            4 => "Bacterias promotoras del crecimiento de plantas"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "resumen" => array:2 [
      "en" => array:2 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">It has been established that a decrease in the population of <span class="elsevierStyleItalic">Gluconacetobacter diazotrophicus</span> associated with sugarcane occurs after nitrogen fertilization&#46; This fact could be due to a direct influence of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on bacterial cells or to changes in plant physiology after fertilizer addition&#44; affecting bacterial establishment&#46; In this work&#44; we observed that survival of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was directly influenced when 44&#46;8<span class="elsevierStyleHsp" style=""></span>mM of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;640<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41; was used for <span class="elsevierStyleItalic">in vitro</span> experiments&#46; Furthermore&#44; micropropagated sugarcane plantlets were inoculated with <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> and used for split root experiments&#44; in which both ends of the system were fertilized with a basal level of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;0&#46;35<span class="elsevierStyleHsp" style=""></span>mM&#59; 10<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41;&#46; Twenty days post inoculation &#40;dpi&#41; one half of the plants were fertilized with a high dose of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;6&#46;3<span class="elsevierStyleHsp" style=""></span>mM&#59; 180<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41; on one end of the system&#46; This nitrogen level was lower than that directly affecting <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> cells&#59; however&#44; it caused a decrease in the bacterial population in comparison with control plants fertilized with basal nitrogen levels&#46; The decrease in the population of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> was higher in pots fertilized with a basal nitrogen level when compared with the corresponding end supplied with high levels of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;100<span class="elsevierStyleHsp" style=""></span>dpi&#59; 80 days post fertilization&#41; of the same plant system&#46; These observations suggest that the high nitrogen level added to the plants induce systemic physiological changes that affect the establishment of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span>&#46;</p></span>"
      ]
      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">La poblaci&#243;n de <span class="elsevierStyleItalic">Gluconacetobacter diazotrophicus</span> asociada a la ca&#241;a de az&#250;car disminuye despu&#233;s de la fertilizaci&#243;n nitrogenada&#44; lo cual podr&#237;a ocurrir por la influencia directa del NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> sobre la supervivencia bacteriana&#44; o por cambios en la fisiolog&#237;a de las plantas&#44; que impiden el establecimiento bacteriano&#46; En el presente trabajo se observ&#243; que en experimentos <span class="elsevierStyleItalic">in vitro</span> la supervivencia de <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> fue influenciada por 44&#44;8<span class="elsevierStyleHsp" style=""></span>mM de NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;640<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;plant&#41;&#46; Adem&#225;s&#44; <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> fue inoculado en pl&#225;ntulas micropropagadas de ca&#241;a de az&#250;car&#44; que fueron usadas para realizar experimentos de ra&#237;z dividida&#44; en las que ambos extremos de los sistemas se fertilizaron con un nivel basal de NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;0&#44;35<span class="elsevierStyleHsp" style=""></span>mM&#59; 10<span class="elsevierStyleHsp" style=""></span>mg<span class="elsevierStyleHsp" style=""></span>N&#47;planta&#41;&#46; A los 20 d&#237;as posteriores a la inoculaci&#243;n &#40;dpi&#41;&#44; la mitad de plantas fueron fertilizadas en uno de sus extremos con una dosis elevada de NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> &#40;6&#44;3<span class="elsevierStyleHsp" style=""></span>mM&#59; 180<span class="elsevierStyleHsp" style=""></span>mg of N&#47;plant&#41;&#46; Este nivel fue menor al que afect&#243; directamente a las c&#233;lulas de <span class="elsevierStyleItalic">G&#46; diazotrophicus</span>&#59; sin embargo&#44; provoc&#243; una disminuci&#243;n de la poblaci&#243;n bacteriana en comparaci&#243;n con plantas testigo fertilizadas con niveles basales de nitr&#243;geno&#46; La disminuci&#243;n de la poblaci&#243;n fue mayor para ra&#237;ces fertilizadas con un nivel basal de nitr&#243;geno en comparaci&#243;n con las ra&#237;ces fertilizadas con altos niveles del mismo sistema de plantas &#40;100<span class="elsevierStyleHsp" style=""></span>dpi&#59; 80<span class="elsevierStyleHsp" style=""></span>d&#237;as posfertilizaci&#243;n&#41;&#46; Estas observaciones indican que el alto nivel de nitr&#243;geno a&#241;adido a las plantas inducen cambios fisiol&#243;gicos sist&#233;micos que afectan el establecimiento de <span class="elsevierStyleItalic">G&#46; diazotrophicus</span>&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Scheme representing the system used for the split root experiments &#40;A&#41;&#46; After <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> inoculation&#44; the root of each plant was divided and placed in 2 pots&#46; At 20<span class="elsevierStyleHsp" style=""></span>dpi half of the plants were supplemented with high doses of NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> on one side of the system&#46; Images from plants in the split root experiment &#40;B&#41;&#44; in the greenhouse &#40;C&#41; and one plant at 35<span class="elsevierStyleHsp" style=""></span>dpi before the bacterial count &#40;D&#41;&#46;</p>"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Rhizospheric bacterial populations in split root experiments&#46; Each value represents the media of data for five independent plants &#40;Log of cell number&#47;g<span class="elsevierStyleHsp" style=""></span>V&#41; with the respective standard deviation&#46; Mean values with equal letters are not statistically different at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; using the <span class="elsevierStyleItalic">t</span>-Student test&#46; dpi&#58; days post inoculation&#59; dpf&#58; days post fertilization&#59; N&#43;&#58; addition of 180<span class="elsevierStyleHsp" style=""></span>mg of nitrogen&#47;plant&#46;</p>"
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        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
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        "figura" => array:1 [
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Bacterial population inside roots in split root experiments&#46; Each value represents the media of data for five independent plants &#40;Log of cell number&#47;g root&#41; with the respective standard deviation&#46; Mean values with equal letters are not statistically different at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; using the <span class="elsevierStyleItalic">t</span>-Student test&#46; dpi&#58; days post inoculation&#59; dpf&#58; days post fertilization&#59; ND&#58; not detected&#59; N&#43;&#58; addition of 180<span class="elsevierStyleHsp" style=""></span>mg of nitrogen&#47;plant&#46;</p>"
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          "leyenda" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Values correspond to the media of five independent samples determined by the DPSM method&#46; Mean values with equal letters are not statistically different at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; using the <span class="elsevierStyleItalic">t</span>-Student test&#46; SD&#58; standard deviation&#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-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">&#91;NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span>&#93; mM&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " colspan="3" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Log CFU&#47;ml &#40;SD&#41;</th></tr><tr title="table-row"><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="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 5T&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PAl 3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">UAP 5560&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">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;43 &#40;&#177;0&#46;63&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;00 &#40;&#177;0&#46;62&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;09 &#40;&#177;0&#46;30&#41;<span class="elsevierStyleBold">A</span>&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">0&#46;35&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;79 &#40;&#177;0&#46;17&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;09 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;16 &#40;&#177;0&#46;15&#41;<span class="elsevierStyleBold">A</span>&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">0&#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">9&#46;05 &#40;&#177;0&#46;31&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;09 &#40;&#177;0&#46;36&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;79 &#40;&#177;0&#46;17&#41;<span class="elsevierStyleBold">A</span>&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">1&#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">9&#46;31 &#40;&#177;0&#46;15&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;44 &#40;&#177;0&#46;08&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;89 &#40;&#177;0&#46;17&#41;<span class="elsevierStyleBold">A</span>&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&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;01 &#40;&#177;0&#46;27&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;20 &#40;&#177;0&#46;17&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;16 &#40;&#177;0&#46;27&#41;<span class="elsevierStyleBold">A</span>&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&#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">8&#46;95 &#40;&#177;0&#46;24&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;31 &#40;&#177;0&#46;28&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;95 &#40;&#177;0&#46;24&#41;<span class="elsevierStyleBold">A</span>&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">11&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;29 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;33 &#40;&#177;0&#46;05&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;05 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&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">22&#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">8&#46;72 &#40;&#177;0&#46;30&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">9&#46;41 &#40;&#177;0&#46;12&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;85 &#40;&#177;0&#46;11&#41;<span class="elsevierStyleBold">A</span>&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">44&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">C</span>&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">5&#46;02 &#40;&#177;0&#46;25&#41;<span class="elsevierStyleBold">B</span>&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">89&#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">0 <span class="elsevierStyleBold">C</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">C</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">5&#46;07 &#40;&#177;0&#46;05&#41;<span class="elsevierStyleBold">B</span>&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">179&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">C</span>&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Bacterial number of three strains of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> grown in solid LGI media supplemented with different NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> concentrations</p>"
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          "leyenda" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Values correspond to the media of five independent samples determined by the MPN method using a McCrady table with three replicate vials for all dilutions of each sample&#46; Mean values with equal letters are not statistically different at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; using the <span class="elsevierStyleItalic">t</span>-Student test&#46; SD&#58; standard deviation&#46;</p>"
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;51 &#40;&#177;0&#46;43&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;49 &#40;&#177;0&#46;30&#41;<span class="elsevierStyleBold">A</span>&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">0&#46;35&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;43 &#40;&#177;0&#46;37&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;47 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;27 &#40;&#177;0&#46;13&#41;<span class="elsevierStyleBold">A</span>&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">0&#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">8&#46;43 &#40;&#177;0&#46;31&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;44 &#40;&#177;0&#46;41&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;43 &#40;&#177;0&#46;31&#41;<span class="elsevierStyleBold">A</span>&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">1&#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">8&#46;46 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;29 &#40;&#177;0&#46;36&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;28 &#40;&#177;0&#46;32&#41;<span class="elsevierStyleBold">A</span>&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&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;40 &#40;&#177;0&#46;27&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;33 &#40;&#177;0&#46;38&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;21 &#40;&#177;0&#46;42&#41;<span class="elsevierStyleBold">A</span>&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&#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">8&#46;38 &#40;&#177;0&#46;34&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;26 &#40;&#177;0&#46;37&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;25 &#40;&#177;0&#46;33&#41;<span class="elsevierStyleBold">A</span>&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">11&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;32 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;13 &#40;&#177;0&#46;25&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;13 &#40;&#177;0&#46;38&#41;<span class="elsevierStyleBold">A</span>&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">22&#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">8&#46;32 &#40;&#177;0&#46;44&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;17 &#40;&#177;0&#46;32&#41;<span class="elsevierStyleBold">A</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8&#46;15 &#40;&#177;0&#46;40&#41;<span class="elsevierStyleBold">A</span>&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">44&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;56 &#40;&#177;0&#46;32&#41;<span class="elsevierStyleBold">B</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;62 &#40;&#177;0&#46;44&#41;<span class="elsevierStyleBold">B</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">2&#46;57 &#40;&#177;0&#46;35&#41;<span class="elsevierStyleBold">B</span>&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">89&#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">0 <span class="elsevierStyleBold">D</span>&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">1&#46;03 &#40;&#177;0&#46;45&#41;<span class="elsevierStyleBold">C</span>&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">179&#46;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">D</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">D</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">0 <span class="elsevierStyleBold">D</span>&nbsp;\t\t\t\t\t\t\n
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                  """
              ]
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Bacterial number of three strains of <span class="elsevierStyleItalic">G&#46; diazotrophicus</span> grown in semisolid LGI media supplemented with different NH<span class="elsevierStyleInf">4</span>NO<span class="elsevierStyleInf">3</span> concentrations</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:42 [
            0 => array:3 [
              "identificador" => "bib0215"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Induced systemic resistance in cucumber and <span class="elsevierStyleItalic">Arabidopsis thaliana</span> by the combination of <span class="elsevierStyleItalic">Trichoderma harzianum</span> Tr6 and <span class="elsevierStyleItalic">Pseudomonas</span> sp&#46; Ps14"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:7 [
                            0 => "H&#46; Alizadeh"
                            1 => "K&#46; Behboudi"
                            2 => "M&#46; Ahmadzadeh"
                            3 => "M&#46; Javan-Nikkhah"
                            4 => "C&#46; Zamioudis"
                            5 => "C&#46;M&#46;J&#46; Pieterse"
                            6 => "P&#46;A&#46;H&#46;M&#46; Bakker"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Biol Control"
                        "fecha" => "2013"
                        "volumen" => "65"
                        "paginaInicial" => "14"
                        "paginaFinal" => "23"
                      ]
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                ]
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            ]
            1 => array:3 [
              "identificador" => "bib0220"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Influence of ammonium and nitrate on the growth and photosynthesis of sugarcane"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "R&#46; Armas"
                            1 => "M&#46;-H&#46; Valadier"
                            2 => "M&#46;L&#46; Champigny"
                            3 => "T&#46; Lamaze"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "J Plant Physiol"
                        "fecha" => "1992"
                        "volumen" => "140"
                        "paginaInicial" => "531"
                        "paginaFinal" => "535"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0225"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Acetic acid bacterial biota of the pink sugarcane mealybug&#44; <span class="elsevierStyleItalic">Saccharoccocus sacchari</span>&#44; and its environs"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "N&#46;J&#46; Ashbolt"
                            1 => "P&#46;E&#46; Inkerman"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Appl Environ Microbiol"
                        "fecha" => "1990"
                        "volumen" => "56"
                        "paginaInicial" => "707"
                        "paginaFinal" => "712"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/16348144"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib0230"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Production of indole-3-acetic acid and gibberellins A1 y A3 by <span class="elsevierStyleItalic">Acetobacter diazotrophicus</span> and <span class="elsevierStyleItalic">Herbaspirillum seropedicae</span> in chemically-defined culture media"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:6 [
                            0 => "F&#46; Bastian"
                            1 => "A&#46; Cohen"
                            2 => "P&#46; Piccoli"
                            3 => "V&#46; Luna"
                            4 => "R&#46; Baraldi"
                            5 => "R&#46; Bottini"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Plant Growth Regul"
                        "fecha" => "1998"
                        "volumen" => "24"
                        "paginaInicial" => "7"
                        "paginaFinal" => "11"
                        "itemHostRev" => array:3 [
                          "pii" => "S0735109708034347"
                          "estado" => "S300"
                          "issn" => "07351097"
                        ]
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                ]
              ]
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            4 => array:3 [
              "identificador" => "bib0235"
              "etiqueta" => "5"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Ecological significance and complexity of N-source preference in plants"
                      "autores" => array:1 [
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        "texto" => "<p id="par0105" class="elsevierStylePara elsevierViewall">We are grateful to <span class="elsevierStyleGrantSponsor" id="gs1">CONACYT</span> &#40;<span class="elsevierStyleGrantNumber" refid="gs1">000000000156576</span>&#41;&#44; <span class="elsevierStyleGrantSponsor" id="gs2">PRODEP</span> and <span class="elsevierStyleGrantSponsor" id="gs3">VIEP-BUAP-2014</span> for the support of this work&#46; Osvaldo Rodr&#237;guez-Andrade and Dalia Molina Romero were awarded a CONACYT fellowship&#46; This work is dedicated to the memory of Jes&#250;s Caballero-Mellado&#46;</p>"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2015.09.004

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Year/Month	Html	Pdf	Total

2024 November	1	0	1
2024 October	20	7	27
2024 September	38	8	46
2024 August	26	4	30
2024 July	23	12	35
2024 June	30	1	31
2024 May	20	9	29
2024 April	23	3	26
2024 March	25	7	32
2024 February	19	4	23
2024 January	24	5	29
2023 December	18	7	25
2023 November	27	7	34
2023 October	34	6	40
2023 September	17	8	25
2023 August	14	3	17
2023 July	10	7	17
2023 June	29	4	33
2023 May	13	2	15
2023 April	17	6	23
2023 March	7	7	14
2023 February	24	3	27
2023 January	22	11	33
2022 December	35	8	43
2022 November	43	10	53
2022 October	25	7	32
2022 September	24	25	49
2022 August	32	8	40
2022 July	29	7	36
2022 June	21	12	33
2022 May	20	24	44
2022 April	19	8	27
2022 March	40	10	50
2022 February	45	11	56
2022 January	56	18	74
2021 December	32	8	40
2021 November	49	17	66
2021 October	37	26	63
2021 September	39	17	56
2021 August	37	17	54
2021 July	12	8	20
2021 June	21	9	30
2021 May	22	10	32
2021 April	7	22	29
2021 March	13	9	22
2021 February	12	9	21
2021 January	18	12	30
2020 December	13	10	23
2020 November	14	8	22
2020 October	10	6	16
2020 September	16	16	32
2020 August	11	8	19
2020 July	6	5	11
2020 June	20	17	37
2020 May	15	12	27
2020 April	17	4	21
2020 March	16	6	22
2020 February	18	11	29
2020 January	17	10	27
2019 December	11	11	22
2019 November	11	17	28
2019 October	17	6	23
2019 September	15	19	34
2019 August	8	9	17
2019 July	13	18	31
2019 June	37	11	48
2019 May	86	9	95
2019 April	45	13	58
2019 March	12	4	16
2019 February	20	4	24
2019 January	25	4	29
2018 December	18	10	28
2018 November	26	5	31
2018 October	27	7	34
2018 September	23	5	28
2018 August	32	5	37
2018 July	13	2	15
2018 June	21	7	28
2018 May	12	7	19
2018 April	34	13	47
2018 March	108	2	110
2018 February	19	2	21
2018 January	102	5	107
2017 December	40	1	41
2017 November	12	5	17
2017 October	17	7	24
2017 September	13	15	28
2017 August	12	6	18
2017 July	12	2	14
2017 June	24	4	28
2017 May	21	4	25
2017 April	12	26	38
2017 March	22	74	96
2017 February	12	4	16
2017 January	10	1	11
2016 December	31	9	40
2016 November	27	7	34
2016 October	37	6	43
2016 September	38	9	47
2016 August	32	4	36
2016 July	30	7	37
2016 June	40	18	58
2016 May	23	14	37
2016 April	37	27	64
2016 March	61	28	89
2016 February	32	27	59
2016 January	26	34	60
2015 December	9	8	17

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