Brief report
The drop plate method as an alternative for Azospirillum spp. viable cell enumeration within the consensus protocol of the REDCAI network
La técnica de la microgota como alternativa para el recuento de Azospirillum spp. dentro del protocolo de la Red de Control de Calidad de Inoculantes (REDCAI)
Luciana P. Di Salvoa,b,1, Julia E. Garcíac,1, Mariana L. Puentec,1,
, Josefina Amigod, Analía Anríqueze, Claudia Barloccof, Silvia Benintendeg, Tatiana Bochatayh, Marta Bortolatoi, Fabricio Cassánj, Carolina Castañok, Melina Catafestal, Anahí Coniglioj, Marisa Díazm, Liliana R. Galiánn, Eugenia Gallaceo, Patricia Garcíak, Inés E. García de Salamonea, Marianela Landap, Germán Liernurq..., María Laura Maneirom, Rosana Massar, Julieta Malinvernip, Nicolás Marchessin, Emilia Monteleones, Silvina Oviedom, Lucrecia Poblitit, Gabriela Portelau, Débora Radovancichv, Silvia Righesw, Rosina Rochax, Enrique Rodríguez Cáceresq, Alejandro Rossim, Gisela Santellay, María Laura Tortoraz, Nora Trejon, José A. Valenzuelaaa, Daniela VallejocVer más
Corresponding author
a Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Biología Aplicada y Alimentos, Cátedra de Microbiología Agrícola, Buenos Aires, Argentina
b CONICET, Buenos Aires, Argentina
c Instituto Nacional de Tecnología Agropecuaria (INTA), Instituto de Microbiología y Zoología Agrícola, Argentina
d Laboratorio de Control de Inoculantes (LABOCOIN)-Cátedra de Microbiología Agrícola-Facultad de Agronomía y Zootecnia-Universidad Nacional de Tucumán, Argentina
e Universidad Nacional de Santiago del Estero, Facultad de Agronomía y Agroindustrias, Cátedra de Microbiología Agrícola, Santiago del Estero, Argentina
f Instituto Nacional de Investigación Agropecuaria (INIA), Programa de Producción y Sustentabilidad Ambiental, Plataforma Bioinsumos, Laboratorio de Microbiología de Suelos, Estación Experimental INIA Las Brujas, Ruta 48 km 10, 90200 Canelones, Uruguay
g Facultad de Ciencias Agropecuarias UNER, Cátedra Microbiología Agrícola, Argentina
h BASF Agricultural Specialities S.A., Santo Tomé, Santa Fé, Argentina
i Universidad Nacional de Rosario, Facultad de Ciencias Agrarias, Departamento de Ciencias de la Tierra y Tecnología, Cátedra de Microbiología Agrícola, Santa Fe, Argentina
j Laboratorio de Fisiología Vegetal e Interacción Planta-Microorganismo, Instituto de Investigaciones Agrobiotecnológicas (INIAB-CONICET), Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina
k Laboratorio de Microbiología Agrícola, Facultad de Ciencias Exactas y Naturales, Universidad Nacional La Pampa, Argentina
l Bio Nova - Nova S.A., Cañada de Gómez, Santa Fe, Argentina
m Rizobacter Argentina S.A., Pergamino, Buenos Aires, Argentina
n Laboratorio de Microbiología, Facultad de Ciencias Agrarias, Universidad Nacional de Lomas de Zamora, Provincia de Buenos Aires, Argentina
o Universidad Nacional de La Pampa, Facultad de Agronomía, Área de Recursos Naturales, Cátedra de Microbiología Agrícola, La Pampa, Argentina
p Laboratorio de Bacteriología, Coordinación de Plagas, Enfermedades de las plantas y Bioinsumos, SENASA, Buenos Aires, Argentina
q Private Advisor
r Stoller Biociencias S.R.L., Ciudad Autónoma de Buenos Aires, Argentina
s Nitrasoil Argentina S.A., Quilmes, Buenos Aires, Argentina
t Barenbrug Argentina, Pergamino, Buenos Aires, Argentina
u Laboratorio Integrado de Microbiología Agrícola y de los Alimentos (LIMAyA), Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires, Azul, Buenos Aires, Argentina
v Laformed S.A., Laboratorio de Especialidades Medicinales y Veterinarias, Formosa, Argentina
w Marketing Agrícola S.R.L., Córdoba, Argentina
x ALTER-BIO S.A., Bragado, Buenos Aires, Argentina
y Novozymes BioAg S.A., Pilar, Buenos Aires, Argentina
z Estación Experimental Agroindustrial Obispo Colombres (EEAOC), Sección Caña de Azúcar, Subprograma Agronomía, Argentina
aa Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste; IMIT-CONICET, Argentina
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"apellidos" => "Valenzuela" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">aa</span>" "identificador" => "aff0135" ] ] ] 37 => array:3 [ "nombre" => "Daniela" "apellidos" => "Vallejo" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] ] ] ] "afiliaciones" => array:27 [ 0 => array:3 [ "entidad" => "Universidad de Buenos Aires, Facultad de Agronomía, Departamento de Biología Aplicada y Alimentos, Cátedra de Microbiología Agrícola, Buenos Aires, Argentina" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "CONICET, Buenos Aires, Argentina" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Instituto Nacional de Tecnología Agropecuaria (INTA), Instituto de Microbiología y Zoología Agrícola, Argentina" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Laboratorio de Control de Inoculantes (LABOCOIN)-Cátedra de Microbiología Agrícola-Facultad de Agronomía y Zootecnia-Universidad Nacional de Tucumán, Argentina" "etiqueta" => "d" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Universidad Nacional de Santiago del Estero, Facultad de Agronomía y Agroindustrias, Cátedra de Microbiología Agrícola, Santiago del Estero, Argentina" "etiqueta" => "e" "identificador" => "aff0025" ] 5 => array:3 [ "entidad" => "Instituto Nacional de Investigación Agropecuaria (INIA), Programa de Producción y Sustentabilidad Ambiental, Plataforma Bioinsumos, Laboratorio de Microbiología de Suelos, Estación Experimental INIA Las Brujas, Ruta 48 km 10, 90200 Canelones, Uruguay" "etiqueta" => "f" "identificador" => "aff0030" ] 6 => array:3 [ "entidad" => "Facultad de Ciencias Agropecuarias UNER, Cátedra Microbiología Agrícola, Argentina" "etiqueta" => "g" "identificador" => "aff0035" ] 7 => array:3 [ "entidad" => "BASF Agricultural Specialities S.A., Santo Tomé, Santa Fé, Argentina" "etiqueta" => "h" "identificador" => "aff0040" ] 8 => array:3 [ "entidad" => "Universidad Nacional de Rosario, Facultad de Ciencias Agrarias, Departamento de Ciencias de la Tierra y Tecnología, Cátedra de Microbiología Agrícola, Santa Fe, Argentina" "etiqueta" => "i" "identificador" => "aff0045" ] 9 => array:3 [ "entidad" => "Laboratorio de Fisiología Vegetal e Interacción Planta-Microorganismo, Instituto de Investigaciones Agrobiotecnológicas (INIAB-CONICET), Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina" "etiqueta" => "j" "identificador" => "aff0050" ] 10 => array:3 [ "entidad" => "Laboratorio de Microbiología Agrícola, Facultad de Ciencias Exactas y Naturales, Universidad Nacional La Pampa, Argentina" "etiqueta" => "k" "identificador" => "aff0055" ] 11 => array:3 [ "entidad" => "Bio Nova - Nova S.A., Cañada de Gómez, Santa Fe, Argentina" "etiqueta" => "l" "identificador" => "aff0060" ] 12 => array:3 [ "entidad" => "Rizobacter Argentina S.A., Pergamino, Buenos Aires, Argentina" "etiqueta" => "m" "identificador" => "aff0065" ] 13 => array:3 [ "entidad" => "Laboratorio de Microbiología, Facultad de Ciencias Agrarias, Universidad Nacional de Lomas de Zamora, Provincia de Buenos Aires, Argentina" "etiqueta" => "n" "identificador" => "aff0070" ] 14 => array:3 [ "entidad" => "Universidad Nacional de La Pampa, Facultad de Agronomía, Área de Recursos Naturales, Cátedra de Microbiología Agrícola, La Pampa, Argentina" "etiqueta" => "o" "identificador" => "aff0075" ] 15 => array:3 [ "entidad" => "Laboratorio de Bacteriología, Coordinación de Plagas, Enfermedades de las plantas y Bioinsumos, SENASA, Buenos Aires, Argentina" "etiqueta" => "p" "identificador" => "aff0080" ] 16 => array:3 [ "entidad" => "Private Advisor" "etiqueta" => "q" "identificador" => "aff0085" ] 17 => array:3 [ "entidad" => "Stoller Biociencias S.R.L., Ciudad Autónoma de Buenos Aires, Argentina" "etiqueta" => "r" "identificador" => "aff0090" ] 18 => array:3 [ "entidad" => "Nitrasoil Argentina S.A., Quilmes, Buenos Aires, Argentina" "etiqueta" => "s" "identificador" => "aff0095" ] 19 => array:3 [ "entidad" => "Barenbrug Argentina, Pergamino, Buenos Aires, Argentina" "etiqueta" => "t" "identificador" => "aff0100" ] 20 => array:3 [ "entidad" => "Laboratorio Integrado de Microbiología Agrícola y de los Alimentos (LIMAyA), Facultad de Agronomía, Universidad Nacional del Centro de la Provincia de Buenos Aires, Azul, Buenos Aires, Argentina" "etiqueta" => "u" "identificador" => "aff0105" ] 21 => array:3 [ "entidad" => "Laformed S.A., Laboratorio de Especialidades Medicinales y Veterinarias, Formosa, Argentina" "etiqueta" => "v" "identificador" => "aff0110" ] 22 => array:3 [ "entidad" => "Marketing Agrícola S.R.L., Córdoba, Argentina" "etiqueta" => "w" "identificador" => "aff0115" ] 23 => array:3 [ "entidad" => "ALTER-BIO S.A., Bragado, Buenos Aires, Argentina" "etiqueta" => "x" "identificador" => "aff0120" ] 24 => array:3 [ "entidad" => "Novozymes BioAg S.A., Pilar, Buenos Aires, Argentina" "etiqueta" => "y" "identificador" => "aff0125" ] 25 => array:3 [ "entidad" => "Estación Experimental Agroindustrial Obispo Colombres (EEAOC), Sección Caña de Azúcar, Subprograma Agronomía, Argentina" "etiqueta" => "z" "identificador" => "aff0130" ] 26 => array:3 [ "entidad" => "Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste; IMIT-CONICET, Argentina" "etiqueta" => "aa" "identificador" => "aff0135" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "La técnica de la microgota como alternativa para el recuento de <span class="elsevierStyleItalic">Azospirillum</span> spp. dentro del protocolo de la Red de Control de Calidad de Inoculantes (REDCAI)" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 378 "Ancho" => 1305 "Tamanyo" => 71558 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Congo red (RC) Petri plates with 20<span class="elsevierStyleHsp" style=""></span>μl drop volume of 10<span class="elsevierStyleSup">−4</span>, 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, 10<span class="elsevierStyleSup">−7</span> dilutions, in quadruplicate. a. Drops distribution on the RC medium surface. b. Typical colonies of <span class="elsevierStyleItalic">Azospirillum</span> spp. in numbers in accordance with the ten-fold dilutions. Photo credits: Dr. Mariana Puente (a) and Dr. Luciana Di Salvo (b).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0025" class="elsevierStylePara elsevierViewall">The genus <span class="elsevierStyleItalic">Azospirillum</span> is a member of a phylogenetic subgroup in the α-subclass of Proteobacteria. It comprises free-living, diazotrophic bacteria capable of colonizing the internal and external tissues of plant roots<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">2</span></a>. <span class="elsevierStyleItalic">Azospirillum</span> is one of the most studied genera within plant growth-promoting rhizobacteria – or PGPR – due to its ability to improve the growth and grain yield of many agronomically important crops. <span class="elsevierStyleItalic">Azospirillum</span> spp. are distributed worldwide and have been isolated from the root surface and rhizosphere of various plants, including cereal crops, forage grasses, and cacti<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">13</span></a>.</p><p id="par0030" class="elsevierStylePara elsevierViewall">Okon and Labandera González<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">10</span></a> summarized the results of several field experiments performed in different countries for 20 years and reported that <span class="elsevierStyleItalic">Azospirillum</span> inoculation positively affected plant growth in 60–70% of the cases analyzed, with grain yield increases in the range of 5–30%. Additionally, Díaz-Zorita et al.<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">7</span></a> reviewed more than 40 articles, which evidenced 347 cases of positive response to <span class="elsevierStyleItalic">Azospirillum</span> inoculation, with yield increases of 14%, 9.5%, and 6.6% in winter cereals, summer cereals, and legumes, respectively. One of the main mechanisms that explain plant growth promotion by <span class="elsevierStyleItalic">Azosprillum</span> is its ability to produce or metabolize compounds such as phytoregulators<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">10</span></a>. These compounds include auxins, especially indole 3-acetic acid, gibberellins, cytokinins, nitric oxide, ethylene, and other molecules regulating plant growth under abiotic stress conditions such as abscisic acid and cadaverine diamine<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">5</span></a>.</p><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Azospirillum brasilense</span> Az39 strain was isolated in Argentina in the 1980s within the context of a program carried out to identify microorganisms with potential to be used as agricultural bioinputs. This strain is deposited at the PGPR Culture Collection, Instituto de Microbiología y Zoología Agrícola, Instituto Nacional de Tecnología Agropecuaria (INTA), Castelar (Buenos Aires, Argentina). Due to its ability to increase wheat and corn yields, INTA and the Servicio Nacional de Sanidad Agropecuaria (SENASA) recommend <span class="elsevierStyleItalic">A. brasilense</span> Az39 to produce inoculant formulations for corn, wheat, and other non-legume crops. For this reason, this strain is used to manufacture 75% of the inoculants formulated in Argentina<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">1,6</span></a>.</p><p id="par0040" class="elsevierStylePara elsevierViewall">There is an increasing demand for bioinputs to maximize crop production, and, thus, the quality of these products must be guaranteed. In this context, several scientific researchers from public and private organizations of Argentina and abroad established the REDCAI network (Red de Control de Calidad de Inoculantes), a workgroup of the División Microbiología Agrícola y Ambiental (DIMAyA), and member of the Asociación Argentina de Microbiología (AAM). In 2013, the REDCAI network elaborated a handbook of microbiological procedures for inoculant evaluation<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">3</span></a> to promote and standardize the commercial use of inoculants. The REDCAI network has already published a complete consensus protocol describing a methodology for detecting contaminating microorganisms in inoculant samples and enumerating viable <span class="elsevierStyleItalic">Azospirillum</span> cells by the spread plate technique on a solid culture medium<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3,4</span></a>. These two important parameters for inoculant quality assessment have been evaluated and validated by more than 20 laboratories from Argentina and abroad, belonging to the REDCAI network. However, the routine analysis of many inoculant samples by the spread plate technique described in the REDCAI consensus protocol is laborious and expensive. In this sense, another method for the enumeration of viable cells using fewer Petri plates, with the possibility of including a high number of replicates, has been previously described. This technique, known as the drop plate method<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">9</span></a>, was proposed for assessing <span class="elsevierStyleItalic">A. brasilense</span>-based inoculants<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">11</span></a>. The aims of this work were: (1) to standardize and validate the drop plate method for <span class="elsevierStyleItalic">A. brasilense</span>-containing inoculants; (2) to compare the results obtained through this method with those obtained through the spread plate technique previously described in the REDCAI consensus protocol.</p><p id="par0045" class="elsevierStylePara elsevierViewall">To compare the results obtained through the drop plate method and the spread plate technique, both enumeration methods were described in detail in a single protocol, which had to be carefully followed across a total of three independent trials, performed in different years using different inoculant samples processed by different laboratories belonging to the REDCAI (Table S1). Standard samples of <span class="elsevierStyleItalic">A. brasilense</span>-based inoculants without trademark identification were analyzed. The same inoculant sample was further divided and sent to each laboratory involved in each trial. A total of 14 laboratories belonging to the REDCAI participated in the first trial (hereinafter, ‘trial 1’). Of them, 7 were private laboratories, and the remaining 7 were laboratories belonging to public institutions, including INIA-Uruguay, INTA-Argentina, and several Argentine national universities. The second trial (hereinafter, ‘trial 2’) involved 13 private laboratories and 12 laboratories belonging to public institutions (INTA, CONICET, and Argentine national universities) comprising 25 operators. This trial constituted an INTERLAB trial, characterized by the inclusion of both trained and inexperienced operators. A total of 17 REDCAI laboratories belonging to the REDCAI participated in the last trial (hereinafter, ‘trial 3’), including 4 private laboratories and 13 public laboratories (INTA, SENASA, and Argentine national universities) (Table S1).</p><p id="par0050" class="elsevierStylePara elsevierViewall">The protocol used in all trials included a complete description of the methodology for sample conservation, homogenates and dilution preparation, culture media formulation, incubation conditions, and detection of contaminating microorganisms, according to the REDCAI consensus protocol<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">3</span></a>. Each laboratory received the inoculant sample corresponding to the trial and divided it into three subsamples, which were considered technical replicates. To enumerate <span class="elsevierStyleItalic">Azospirillum</span> viable cells through the spread plate technique, 100<span class="elsevierStyleHsp" style=""></span>μl of the dilutions 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, and 10<span class="elsevierStyleSup">−7</span> were sown in duplicate (spreading replicates) in Petri plates containing RC culture medium<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">12</span></a>, according to the methodology previously described<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">3</span></a>.</p><p id="par0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Azospirillum</span> enumeration by the drop plate method in trial 1 was performed using a 10<span class="elsevierStyleHsp" style=""></span>μl-drop volume of the dilutions 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, and 10<span class="elsevierStyleSup">−7</span>, and a 20<span class="elsevierStyleHsp" style=""></span>μl-drop volume of the dilutions 10<span class="elsevierStyleSup">−4</span>, 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, and 10<span class="elsevierStyleSup">−7</span>, applied by quadruplicate (spreading replicates) on Petri plates previously filled with RC culture medium<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">12</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>a and b). In trials 2 and 3, bacterial cell enumeration was performed using 20<span class="elsevierStyleHsp" style=""></span>μl- and 10<span class="elsevierStyleHsp" style=""></span>μl-drop volumes, respectively, of the dilutions 10<span class="elsevierStyleSup">−4</span>, 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, and 10<span class="elsevierStyleSup">−7</span>, applied by quadruplicate (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>a and b). For this enumeration method, water condensation on the agar surface is undesirable because it affects drop absorption and may cause the confluence of different drops. For this reason, the absence of condensed water on the culture medium was carefully checked before the drop distribution. After inoculum application, Petri plates were kept non-inverted until the drops were completely absorbed.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">Petri plates corresponding to both cell enumeration methods were incubated at 28–30<span class="elsevierStyleHsp" style=""></span>°C for 4 days. Colony counting was performed after the incubation period and repeated 2 days later (6 days after sowing) in order to confirm the typical <span class="elsevierStyleItalic">A.</span><span class="elsevierStyleItalic">brasilense</span> morphology in the RC culture medium<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">12</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>b). Total colony-forming units per milliliter of inoculant (CFU/ml) was calculated taking into account those dilutions which exhibited a range of 5–50 colonies per drop, in the case of the drop plate method, and of 30–300 colonies per plate, in the case of the spread plate technique. For each trial, all participants reported a total of 6 results, 3 for each cell enumeration technique, corresponding to the three subsamples processed as technical replicates. Statistical analyses were carried out using the INFOSTAT/Professional 1.1 software<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">8</span></a> to evaluate the reproducibility of these techniques across laboratories and compare both enumeration techniques.</p><p id="par0065" class="elsevierStylePara elsevierViewall">First, the Cochran's test (0.05%) was performed to determine the consistency of the results reported by each participant of the different trials. This analysis compares the variance of a data set with the total variance of the data supplied by all trial participants. Results reported in trial 1 and trial 2 were consistent, while one result reported by one participant of trial 3 was inconsistent (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). This participant reported highly variable results for viable cell enumeration by the drop plate method, exceeding Cochran's test critical value. In addition, this laboratory reported highly variable results for viable cell enumeration by the spread plate technique compared with those from the other laboratories. For this reason, all results reported by this laboratory were excluded in further analyses.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">Second, the Grubbs’ test (0.05%) was conducted to identify outlier occurrence. This analysis determines if an average value reported by a given laboratory differs significantly from the average values reported by the remaining laboratories involved in the trial. Only in trial 2, two laboratories reported results obtained by the drop plate method that were considered outliers (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). For this reason, the results provided by these laboratories were excluded from further analyses.</p><p id="par0075" class="elsevierStylePara elsevierViewall">Third, data normality was tested by the Shapiro-Wilk's test. In the case of normal distribution, the Z-score of each trial participant was calculated considering the mean values and standard deviations (SD). There was normal distribution in trials 2 and 3. Conversely, when data distribution was other than normal, Z-scores were calculated considering the median values and the median absolute deviations (MADe). This occurred in trial 1. In the three trials, the Z-scores showed that averages for viable cell numbers were mostly satisfactory (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). In other words, most of the averages were within 2 SD. Only two participants in trial 2 reported unsatisfactory viable cell enumeration averages, one for both enumeration methods and the other only for the drop plate method. These two participants reported viable cell enumeration averages higher than 3 SD. Moreover, in the three trials, some participants reported “questionable” viable cell enumeration averages (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>) by the spread plate technique (two participants in trial 1, four participants in trial 2, and one participant in trial 3), by the drop plate method using a 10<span class="elsevierStyleHsp" style=""></span>μl-drop volume (one participant in trial 1 and one participant in trial 3), and by the drop plate method using a 20<span class="elsevierStyleHsp" style=""></span>μl-drop volume (two members in trial 1 and one member in trial 2). “Questionable” viable cell enumeration averages were within 2 and 3 SD. Unsatisfactory and questionable viable cell enumeration averages were excluded from the comparative analyses between both enumeration methods in all cases. Thus, only the results obtained by those participants who reported consistent, robust, and satisfactory values by both enumeration methods in the three trials were included.</p><p id="par0080" class="elsevierStylePara elsevierViewall">Considering that data from trial 2 and trial 3 had a normal distribution, but those from trial 1 did not, the comparison between both enumeration methods was performed by the paired-sample T-test and Friedman's test, respectively. <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> shows the number of participants whose results were included in the comparison. In addition, the average values for viable cell numbers found in different samples of <span class="elsevierStyleItalic">Azospirillum</span> inoculants, evaluated in the three trials by both enumeration methods, are shown. No differences between the drop plate method and the spread plate technique were observed (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>). Based on these results, we concluded that <span class="elsevierStyleItalic">Azospirillum</span> viable cell enumeration performed by the drop plate method using 10<span class="elsevierStyleHsp" style=""></span>μl- or 20<span class="elsevierStyleHsp" style=""></span>μl-drop volumes is equivalent to the <span class="elsevierStyleItalic">Azospirillum</span> viable cell enumeration performed by the spread plate technique, previously validated and published<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3,4</span></a>.</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0085" class="elsevierStylePara elsevierViewall">The drop plate method validation performed in this work was achieved thanks to the contribution of many REDCAI members from different institutions and geographical areas of Argentina and abroad. This method allows to include more replicates using fewer Petri plates and culture medium amounts, making it a more cost-effective method than the spread plate technique<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">9</span></a>. Furthermore, fewer Petri plates and culture media consumption implies a reduction in waste amounts, which would result in reduced environmental impact. With regard to the complexity of the enumeration techniques, this work shows that the only requirement to carry out the drop plate method is to have minimal training in microbiological techniques. These trials, especially trial 2, involved both trained and inexperienced participants, and even so, reliable results were obtained. Based on this work, we can say that the inexperience in the drop plate method is not expected to constitute a limitation if a clear and comprehensive protocol is available to facilitate the work and to guarantee reliable results, with the commitment to comply with this consensus protocol.</p><p id="par0090" class="elsevierStylePara elsevierViewall">Finally, it is important to point out that the performance and participation of individual laboratories were confidential. Additionally, commercial inoculants fractionated in white bladders without trademark identification were distributed because the aim of this work was not to evaluate the quality of the inoculants. This work is in line with the goals of the REDCAI network, among which, the standardization and validation of consensus protocols for the quality assessment of microbial inoculants stand out. The validation of the drop plate method for other <span class="elsevierStyleItalic">Azospirillum</span> species remains to be accomplished. We validated the drop plate method as a viable cell enumeration technique for <span class="elsevierStyleItalic">A. brasilense</span>. Therefore, this method will be included as an alternative method for the quality control of <span class="elsevierStyleItalic">Azospirillum-</span>containing inoculants in the consensus protocol of the REDCAI network (DIMAyA-AAM).</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conflict of interest</span><p id="par0095" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:8 [ 0 => array:3 [ "identificador" => "xres1733191" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:3 [ "identificador" => "xres1733190" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1529458" "titulo" => "Keywords" ] 3 => array:3 [ "identificador" => "xres1733189" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0015" ] ] ] 4 => array:2 [ "identificador" => "xpalclavsec1529457" "titulo" => "Palabras clave" ] 5 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflict of interest" ] 6 => array:2 [ "identificador" => "xack611774" "titulo" => "Acknowledgements" ] 7 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2020-11-24" "fechaAceptado" => "2021-05-12" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1529458" "palabras" => array:5 [ 0 => "PGPR" 1 => "Quality evaluation" 2 => "Microbiological procedures" 3 => "Spread plate technique" 4 => "Bioinputs" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1529457" "palabras" => array:5 [ 0 => "PGPR" 1 => "Evaluación de calidad" 2 => "Procedimientos microbiológicos" 3 => "Recuento en placa" 4 => "Bioinsumos" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">•</span><p id="par0005" class="elsevierStylePara elsevierViewall">The drop plate method was validated by 55 participants in 3 independent trials.</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">•</span><p id="par0010" class="elsevierStylePara elsevierViewall">Reliability, minimal heterogeneity among results, and economic benefits were met.</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">•</span><p id="par0015" class="elsevierStylePara elsevierViewall">Both methods showed similar number of <span class="elsevierStyleItalic">Azospirillum</span> viable cells.</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">•</span><p id="par0020" class="elsevierStylePara elsevierViewall">Drop plate method will be included in the REDCAI consensus protocol for <span class="elsevierStyleItalic">Azospirillum</span> spp.</p></li></ul></p></span>" ] "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Quality evaluation of commercial inoculants is essential to warrant an adequate crop response to inoculation within a biosecurity framework. In this sense, this work is aimed at standardizing and validating the drop plate method for the enumeration of <span class="elsevierStyleItalic">Azospirillum</span> viable cells as an alternative to the spread plate technique, which is currently proposed in the consensus protocol of the REDCAI network. Between 14 and 25 private and public laboratories participated in three independent trials. We obtained consistent and robust results that allowed to confirm that both techniques are equivalent, concluding that the drop plate method is an alternative enumeration technique that is adequate to be included in the abovementioned consensus protocol.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La evaluación de la calidad de los inoculantes comerciales es fundamental para garantizar una adecuada respuesta de los cultivos a la inoculación dentro de un marco de bioseguridad. En este sentido, el objetivo de este trabajo fue la estandarización y validación de la técnica de la microgota para la cuantificación de <span class="elsevierStyleItalic">Azospirillum</span> como metodología alternativa a la técnica de siembra en superficie, propuesta actualmente en el protocolo consenso de la Red de Calidad de Inoculantes, REDCAI. Entre 14 y 25 laboratorios, tanto privados como públicos, participaron de tres ensayos independientes. A partir de ellos se obtuvieron resultados reproducibles y robustos que permiten confirmar que ambas técnicas son equivalentes y concluir que la técnica de recuento por la microgota es una alternativa adecuada para ser incluida dentro del mencionado protocolo consenso.</p></span>" ] ] "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "1" "nota" => "<p class="elsevierStyleNotepara" id="npar0020"><span class="elsevierStyleItalic">ex aequo</span>.</p>" "identificador" => "fn0005" ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "<p id="par0110" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0015" ] ] ] ] "multimedia" => array:4 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 378 "Ancho" => 1305 "Tamanyo" => 71558 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Congo red (RC) Petri plates with 20<span class="elsevierStyleHsp" style=""></span>μl drop volume of 10<span class="elsevierStyleSup">−4</span>, 10<span class="elsevierStyleSup">−5</span>, 10<span class="elsevierStyleSup">−6</span>, 10<span class="elsevierStyleSup">−7</span> dilutions, in quadruplicate. a. Drops distribution on the RC medium surface. b. Typical colonies of <span class="elsevierStyleItalic">Azospirillum</span> spp. in numbers in accordance with the ten-fold dilutions. Photo credits: Dr. Mariana Puente (a) and Dr. Luciana Di Salvo (b).</p>" ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:1 [ "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="\n \t\t\t\t\ttable-head\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col">Trial \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col">Method for viable cell enumeration \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Consistency (Cochran's test)</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col">Number of participants reporting outliers (Grubbs’ test) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="3" align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Number of participants reporting Z-scores categorized as</th></tr><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Consistent \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Inconsistent \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Satisfactory (≤2 SD<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Questionable (>2–≤3 SD) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Unsatisfactory (>3 SD) \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (10<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (20<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">11 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (20<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">21 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (10<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">15 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] ] ] "notaPie" => array:2 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">SD: Standard Deviation.</p>" ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">The spread plate method was carried out following the consensus protocol of the REDCAI network (DIMAyA-AAM)<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3,4</span></a>.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Drop plate method results: standardization and validation.</p>" ] ] 2 => array:8 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:1 [ "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" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Trial \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Method for viable cell enumeration \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Number of participants (n) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Enumeration results (log CFU/ml) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">p</span> value (Friedman's test) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Bilateral T value (T test) \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">a</span></a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.56 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.6472 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">NA \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (10<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.44 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (20<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.26 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">18 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.27 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">NA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.4326 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (20<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.31 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Spread plate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">8.00 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">NA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.8896 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Drop plate (10<span class="elsevierStyleHsp" style=""></span>μl) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="\n \t\t\t\t\ttop\n \t\t\t\t">7.99 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0015" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0015">The spread plate method was carried out following the consensus protocol of the REDCAI network (DIMAyA-AAM)<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">3,4</span></a>. NA: the test was not applied in this trial.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Comparison between different viable cell enumeration methods.</p>" ] ] 3 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.docx" "ficheroTamanyo" => 47104 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:13 [ 0 => array:3 [ "identificador" => "bib0070" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Biofertilizers in Argentina" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:4 [ 0 => "A.L. Anriquez" 1 => "J.E. Silberman" 2 => "J.A.D. Nuñez" 3 => "A.S. 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Rodríguez Cáceres" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1128/aem.44.4.990-991.1982" "Revista" => array:6 [ "tituloSerie" => "Appl Environ Microbiol" "fecha" => "1982" "volumen" => "44" "paginaInicial" => "990" "paginaFinal" => "991" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/16346123" "web" => "Medline" ] ] ] ] ] ] ] ] 12 => array:3 [ "identificador" => "bib0130" "etiqueta" => "13" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "<span class="elsevierStyleItalic">Azospirillum</span>, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "O. Steenhoudt" 1 => "J. Vanderleyden" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1111/j.1574-6976.2000.tb00552.x" "Revista" => array:6 [ "tituloSerie" => "FEMS Microbiol Rev" "fecha" => "2000" "volumen" => "24" "paginaInicial" => "487" "paginaFinal" => "506" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/10978548" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack611774" "titulo" => "Acknowledgements" "texto" => "<p id="par0100" class="elsevierStylePara elsevierViewall">We are grateful to the former coordinators of the <span class="elsevierStyleItalic">Azospirillum</span> workgroup in the REDCAI, Dr. Rosana Massa, Dr. Cecilia Creus and Dr. Fabricio Cassán, to REDCAI coordinator Dr. Silvia Toresani, and to the companies which provided us the inoculant samples used in our trials. We thank Luisina Andriolo, Lucas Dalmasso, Andrés Laurent, Romina Molina, Gisel Peralta, María Eugenia Schiavon, and Juan Silberman for their contributions to this work. We specially thank Ing. Agr. Enrique Rodríguez Cáceres, whose generosity in sharing his large experience working with <span class="elsevierStyleItalic">Azospirillum</span> genus has been valuable enriched our workgroup discussions. Finally, we are also grateful to editors and anonymous reviewers for their comments and suggestions.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/03257541/0000005400000002/v2_202206160255/S0325754121000560/v2_202206160255/en/main.assets" "Apartado" => array:4 [ "identificador" => "41740" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Microbiología de alimentos" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/03257541/0000005400000002/v2_202206160255/S0325754121000560/v2_202206160255/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754121000560?idApp=UINPBA00004N" ]
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