Characterization and survival of broad-spectrum biocontrol agents against phytopathogenic fungi

array:24 ["pii" => "S0325754121001024" "issn" => "03257541" "doi" => "10.1016/j.ram.2021.10.005" "estado" => "S300" "fechaPublicacion" => "2022-07-01" "aid" => "479" "copyright" => "Asociación Argentina de Microbiología" "copyrightAnyo" => "2021" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2022;54:233-42" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "itemSiguiente" => array:19 [ "pii" => "S0325754122000219" "issn" => "03257541" "doi" => "10.1016/j.ram.2022.03.003" "estado" => "S300" "fechaPublicacion" => "2022-07-01" "aid" => "487" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2022;54:243-6" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "en" => array:14 [ "idiomaDefecto" => true "cabecera" => "Brief report" "titulo" => "Fist report on fumagillin production by Aspergillus fumigatus sensu stricto gliotoxigenic strains recovered from raw cow milk and clinical samples in Argentina" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:3 [ 0 => "en" 1 => "en" 2 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "243" "paginaFinal" => "246" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Primer reporte en Argentina sobre la producción de fumagilina por cepas de Aspergillus fumigatus sensu stricto productoras de gliotoxina, aisladas de leche cruda y de casos clínicos" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "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" => 1241 "Ancho" => 2500 "Tamanyo" => 117204 ] ] "descripcion" => array:1 [ "en" => "Chromatogram obtained with the injection of 20μl of a 10μg/ml solution of fumagillin." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Verónica A. Alonso, Marina A. Velasco Manini, Gabriela A. Pena, Lilia R. Cavaglieri" "autores" => array:4 [ 0 => array:2 [ "nombre" => "Verónica A." "apellidos" => "Alonso" ] 1 => array:2 [ "nombre" => "Marina A." "apellidos" => "Velasco Manini" ] 2 => array:2 [ "nombre" => "Gabriela A." "apellidos" => "Pena" ] 3 => array:2 [ "nombre" => "Lilia R." "apellidos" => "Cavaglieri" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•A. fumigatus strains from farm and clinical samples were able to produce fumagillin.</li><li class="elsevierStyleListItem" id="lsti0010">•A. fumigatus strains were gliotoxin and fumagillin producers.</li><li class="elsevierStyleListItem" id="lsti0015">•Fumagillin producers represent public health risk of toxin transference to raw milk.</li></ul>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754122000219?idApp=UINPBA00004N" "url" => "/03257541/0000005400000003/v1_202209300808/S0325754122000219/v1_202209300808/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S0325754121000456" "issn" => "03257541" "doi" => "10.1016/j.ram.2021.02.010" "estado" => "S300" "fechaPublicacion" => "2022-07-01" "aid" => "455" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2022;54:224-32" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:1 [ "total" => 0 ] "en" => array:14 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Potential of rhizobacteria native to Argentina for the control of Meloidogyne javanica" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:3 [ 0 => "en" 1 => "en" 2 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "224" "paginaFinal" => "232" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Potencial de rizobacterias nativas de Argentina para el control de Meloidogyne javanica" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "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" => 716 "Ancho" => 2258 "Tamanyo" => 192446 ] ] "descripcion" => array:1 [ "en" => "Effect of rhizobacteria inoculation on the number of galls (A) and egg masses (B) on the root system of lettuce infested with M. javanica. MJC: nematode infestation control (with nematode, without bacteria). B19S: Bacillus sp. strain B19S. B9T: Bacillus sp. strain B9T. CHA0: P. protegens strain CHA0. MME3: P.fluorescens strain MME3. TAE4: P.fluorescens strain TAE4. Error bars correspond to standard error means. Different letters indicate significant differences in means according to the LSD-Tukey's test (p<0.05)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "María P. Borrajo, Eduardo A. Mondino, Guillermo A. Maroniche, Macarena Fernández, Cecilia M. Creus" "autores" => array:5 [ 0 => array:2 [ "nombre" => "María P." "apellidos" => "Borrajo" ] 1 => array:2 [ "nombre" => "Eduardo A." "apellidos" => "Mondino" ] 2 => array:2 [ "nombre" => "Guillermo A." "apellidos" => "Maroniche" ] 3 => array:2 [ "nombre" => "Macarena" "apellidos" => "Fernández" ] 4 => array:2 [ "nombre" => "Cecilia M." "apellidos" => "Creus" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Autochthonous rhizobacteria against Meloidogyne javanica.</li><li class="elsevierStyleListItem" id="lsti0015">•Biocontrol by bacteria and their cell free supernatants.</li><li class="elsevierStyleListItem" id="lsti0025">•Impact of rhizobacteria in lettuce infested with Meloidogyne javanica.</li></ul>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754121000456?idApp=UINPBA00004N" "url" => "/03257541/0000005400000003/v1_202209300808/S0325754121000456/v1_202209300808/en/main.assets" ] "en" => array:22 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Characterization and survival of broad-spectrum biocontrol agents against phytopathogenic fungi" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "233" "paginaFinal" => "242" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Saba Azeem, Syed Inayatullah Agha, Neelam Jamil, Bushra Tabassum, Shan Ahmed, Asif Raheem, Nusrat Jahan, Niaz Ali, Anwar Khan" "autores" => array:9 [ 0 => array:3 [ "nombre" => "Saba" "apellidos" => "Azeem" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "1" "identificador" => "fn0005" ] ] ] 1 => array:3 [ "nombre" => "Syed Inayatullah" "apellidos" => "Agha" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "1" "identificador" => "fn0005" ] ] ] 2 => array:3 [ "nombre" => "Neelam" "apellidos" => "Jamil" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 3 => array:3 [ "nombre" => "Bushra" "apellidos" => "Tabassum" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] 1 => array:2 [ "etiqueta" => "d" "identificador" => "aff0020" ] ] ] 4 => array:3 [ "nombre" => "Shan" "apellidos" => "Ahmed" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 5 => array:3 [ "nombre" => "Asif" "apellidos" => "Raheem" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 6 => array:3 [ "nombre" => "Nusrat" "apellidos" => "Jahan" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 7 => array:3 [ "nombre" => "Niaz" "apellidos" => "Ali" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "e" "identificador" => "aff0025" ] ] ] 8 => array:4 [ "nombre" => "Anwar" "apellidos" => "Khan" "email" => array:1 [ 0 => "anwarleo2003@gmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:5 [ 0 => array:3 [ "entidad" => "Department of Biotechnology and Informatics, BUITEMS, Quetta, Pakistan" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Microbiology, BUITEMS, Quetta, Pakistan" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Center of Excellence in Molecular Biology, University of the Punjab, Lahore, Pakistan" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "School of Biological Sciences, University of the Punjab, Lahore, Pakistan" "etiqueta" => "d" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Department of Botany, Hazara University, Mansehra, Pakistan" "etiqueta" => "e" "identificador" => "aff0025" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Caracterización y supervivencia de agentes de control biológico de amplio espectro frente a hongos fitopatógenos" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1204 "Ancho" => 2508 "Tamanyo" => 216595 ] ] "descripcion" => array:1 [ "en" => "Graphical representation of the% suppression of growth of phytopathogenic fungi under study using biocontrol bacteria. The y-axis shows the inhibition percentages, while the x-axis represents the bacterial isolates. The bars show the standard error mean computed by using Microsoft Excel." ] ] ] "textoCompleto" => "IntroductionAgriculture is undoubtedly the backbone of least developed countries, and plays a major role in ensuring food security and economic rise. Pakistan's economy is greatly reliant on agriculture<a class="elsevierStyleCrossRef" href="#bib0280">23</a>. Agricultural resources are critically threatened by plant diseases caused by microorganisms including bacteria, viruses and fungi. Among them, fungal pathogens are the most devastating infectious agents<a class="elsevierStyleCrossRef" href="#bib0225">12</a>. It is estimated that fungi are the major threat (approximately 65%) of pathogen-driven plant-host loss<a class="elsevierStyleCrossRef" href="#bib0170">1</a>. Some of the most common plant-pathogenic fungi belong to the genera Alternaria, Fusarium, Botrytis, Geotrichum, Penicillium and Sclerotinia. These fungi are responsible for causing considerable crop yield loss worldwide<a class="elsevierStyleCrossRef" href="#bib0245">16</a>. Efficient plant disease management is the prerequisite of sustainable agriculture. Plant diseases need to be contained to sustain the quantity and quality of food and fiber produced by agriculturists throughout the world. Various strategies might be utilized to avoid, alleviate or restrict plant diseases<a class="elsevierStyleCrossRef" href="#bib0185">4</a>. In the past few decades, synthetic fungicides played a fundamental function in suppressing plant diseases and enhancing crop yield to reduce food insecurity in today's world<a class="elsevierStyleCrossRef" href="#bib0325">32</a>. However, recent studies, reported that the prolonged use of chemicals could cause harmful effects, including environmental and health hazards, residual toxicity and resistance of pathogens, among others. Furthermore, agrochemicals are not very cost effective<a class="elsevierStyleCrossRef" href="#bib0325">32</a>. Consequently, scientists have focused their efforts on formulating alternate sources to synthetic agrochemicals for limiting pests and diseases. Among these alternatives, biological controls are much preferred. Biological control in plant pathology refers to the suppression of growth or reproduction of a pathogenic organism using another organism. It utilizes the natural enemies of pests or pathogens to eliminate or contain their population.Nowadays more attention is paid to developing useful approaches for environmentally friendly and sustainable agricultural practices, mainly depending on the application and use of beneficial microorganisms, particularly plant growth promoting bacteria (PGPB) as biofertilizers or bio-pesticides<a class="elsevierStyleCrossRef" href="#bib0210">9</a>. PGPB are capable to stimulate plant yield and restrict phytopathogens and could be used as an alternative source to limiting the usage of chemical fungicides. PGPBs are defined as a wide array of bacteria that colonize the plant phyllosphere/rhizosphere and are usually involved in several beneficial activities such as the improvement of plant growth by increasing seed development, plant weight, and crop yield. They can influence plant health either directly or indirectly. The direct mechanisms include production of hormones (indole acetic acid, cytokinins, gibberellins, among others), phosphate solubilization, nitrogen fixation, biofilm formation, siderophores production, mineral solubilization and plant resistance to abiotic stresses. The indirect mechanisms include restricting plant pathogens by producing enzymes (i.e. cellulase, chitinase, glucanase), volatile compounds (VC), secondary metabolites and by competing for space and nutrients<a class="elsevierStyleCrossRef" href="#bib0210">9</a>. The most reported biocontrol bacteria belong to the Bacillus and Pseudomonas genera that can possibly promote plant growth and inhibit fungal pathogens<a class="elsevierStyleCrossRefs" href="#bib0205">8,17</a>. Furthermore, a wide range of bacteria including Agrobacterium spp., Burkholderia spp., Azotobacter spp., Frankia spp., Azospirillum spp., Bradyrhizobium spp., Rhizobium spp., Serratia spp. and Thiobacillus spp. are also considered PGPBs<a class="elsevierStyleCrossRef" href="#bib0175">2</a>.Unfortunately, laboratory results for the application of bacterial inoculants such as biofungicides usually do not correlate with in vivo results<a class="elsevierStyleCrossRef" href="#bib0270">21</a>; therefore, an extensive research and market survey is required to bring a successful bacterial inoculum from the laboratory to the farms. Microbial incorporation for plant disease management and growth promotion in agricultural frameworks and eradication of the use of agrochemical is reliant on the effective selection, screening and safety analysis of potential PGPR strains<a class="elsevierStyleCrossRef" href="#bib0305">28</a>. A number of bacterial biocontrol and plant growth-promoting products are currently in the developmental stages. Most products are generally based on gram positive bacteria such as Bacillus spp. because of their easy formulation and long-term survival due to spore-producing quality<a class="elsevierStyleCrossRef" href="#bib0190">5</a>.This study focuses on the assessment of bacterial antagonism against fungal pathogens and plant growth-promoting traits. Furthermore, the study also aims to determine the survival of biocontrol bacterial strains in cost-effective liquid carrier materials for mass production, which is one of the initial steps toward the commercialization of formulated biofungicides.Materials and methodsIsolation of bacteria in pure cultureSamples of the phyllosphere from different crops including maize (Zea mays), potato (Solanum tuberosum) and wheat (Triticum aestivum) were collected from different fields of Quetta, Pakistan. The collected plant samples were packed in sterilized polythene bags and referred to “Applied Biotechnology Laboratory, BUITEMS”, Quetta, for the isolation of biocontrol bacteria.Bacteria were isolated from the phyllosphere of different crops according to Ramzan et al.<a class="elsevierStyleCrossRef" href="#bib0275">22</a>. Briefly, 1g of the collected samples was thoroughly rinsed under running tap water and subsequently crushed in saline solution (0.85% NaCl). The resulting suspension was serially diluted to 10−3 and 1ml of each dilution was spread on LB agar plates. The plates were incubated at 37°C for 24h pure cultures were obtained by sub-culturing on additional Luria-Bertani (LB) plates.Preliminary screening of bacterial isolates for antifungal activityThe bacterial isolates were screened for antifungal activity against phytopathogenic fungi. The phytopathogenic fungi used in this study Alternaria alternata, Fusarium oxysporum, Fusarium verticillioides and Rhizoctonia solani were kindly provided by ARS USDA. The fungi were cultured on potato dextrose agar (PDA) and incubated at 28°C for 7 days for further experimentation. The bacteria with inhibitory activity were selected for further characterization.Qualitative and quantitative assessment for antagonistic activity in vitroThe qualitative assessment was performed according to Awais et al.<a class="elsevierStyleCrossRef" href="#bib0305">28</a>. The bacterial strains were cultured against each of the fungus on separate PDA plates using the agar plug method. About 4mm agar discs of previously cultivated phytopathogenic fungi were inoculated at the center of PDA plates. Bacterial isolates were inoculated with a sterilized wire loop on two sides of Petri dishes at a distance of 3cm from the fungal plug. The dishes were incubated at 28°C for 5 days.The bacterial isolates with antifungal properties were subjected to quantitative evaluation. The dual culture method was performed according to Haidar et al.<a class="elsevierStyleCrossRef" href="#bib0200">7</a>. Briefly, fungal strains were grown on PDA plates for about 7 days, a 4mm agar disc was excised with a disinfected scalpel and placed at the center of a separate plate. The bacterial isolates to be assessed were co-inoculated on the same agar plate at a distance of 2.5cm from the fungal disc in a straight line. Control plates were cultured only with the fungal pathogen. Dishes were incubated for 5 days at 28°C. The experiment was performed in triplicate. The inhibition percentage was calculated by using a given formula;<elsevierMultimedia ident="eq0005"></elsevierMultimedia>where R2 is the growth of fungus toward the control side of the Petri dish and R1 is the outward growth of the fungus in the direction of the antagonistic bacteria.Molecular identification and phylogenetic analysisThe selected bacterial strains were primarily identified by Gram staining and endospore staining followed by molecular identification.DNA extractionThe total genomic DNA from freshly cultured bacterial isolates was extracted by using Thermo Scientific™ #K0721 as per the manufacturer's protocol. Proteinase K and RNase A were used for protein digestion and removal of RNA respectively.16S rRNA gene amplificationThe amplification of the 16S rRNA gene was performed according to the method described by Ramzan et al.<a class="elsevierStyleCrossRef" href="#bib0275">22</a>. The primers used to amplify a 1.5kb gene fragment were 27F and 1492R.<a class="elsevierStyleCrossRef" href="#bib0320">31</a> The polymerase chain reaction was performed in a thermal cycler (T100 Thermal Cycler) in 20μl reaction mixture containing 0.1μmol/l of each primer, 2.5μmol/l MgCl2, 1μmol/l of each deoxynucleoside triphosphate (dNTP), 50ng/μl of template DNA and 2U/μl Taq DNA polymerase (Thermoscientific, USA). The PCR amplification consisted of DNA denaturation at 95°C for 5min followed by 35 cycles of denaturation at 95°C for 1min, annealing at 57°C for 1min, extension at 72°C for 1.5min and final extension at 72°C for 10min. The PCR products were analyzed by electrophoresis in a 1% agarose gel in 1× TBE (Tris–borate–EDTA) buffer with ethidium bromide staining. The purified PCR products were sequenced by using the facility of Macrogen (Korea).Similarity analysis and dendrogram constructionThe 16S rRNA gene sequences were compared with the NCBI database using BlastN. Further, identification of phylogenetic neighbors and calculation of pairwise similarity of these sequences were done using ClustalW and MEGA 6.4<a class="elsevierStyleCrossRef" href="#bib0235">14</a> software as described by Ramazan et al.<a class="elsevierStyleCrossRef" href="#bib0275">22</a>. The phylogenetic tree was constructed by using a neighbor-joining method. The bootstrap replications (1000 replicates) were used for statistical support.Evaluation of biocontrol bacteria for plant growth promoting traitsThe biocontrol bacteria were evaluated for their plant growth-promoting traits. The parameters selected for evaluating PGP activity were: phosphate solubilizing activity, indole acetic acid (IAA), hydrogen cyanide (HCN), cellulase, siderophore and VOC production.Phosphate solubilization assayNational Botanical Research Institute Phosphate growth medium (NBRIP) agar containing insoluble tri-calcium phosphate was prepared as previously described<a class="elsevierStyleCrossRef" href="#bib0255">18</a>. The pH of NBRIP agar was adjusted to 7.0. The bacterial strains were spot inoculated at the center of NBRIP agar plates. NBRIP agar without bacterial inoculation was taken as control. The dishes were kept at 37°C for 72h and were observed for formation of a clear halo zone. The quantification of phosphate solubilization was performed according to Chandra et al.<a class="elsevierStyleCrossRef" href="#bib0180">3</a> by measuring the yellow color on a spectrophotometer at 880nm.Indole-3-acetic acid assayThe bacterial isolates were screened for indole 3-acetic acid (IAA) production according to Sivasankari<a class="elsevierStyleCrossRef" href="#bib0300">27</a>. Briefly, isolated bacteria were cultured in autoclaved LB broth in a 100ml Erlenmeyer flask with and without the addition of 0.1g of l-tryptophan (Sigma Aldrich). The 100ml Erlenmeyer flask containing uninoculated sterile LB broth was taken as negative control. All flasks were incubated in a shaking incubator at 37°C and 100rpm for 48h. Salkowski's reagent (1ml of 0.5M FeCl3·6H2O in 50ml of 35% perchloric acid) was prepared for IAA detection. In properly labeled test tubes, 1ml of culture supernatants was mixed with the addition of 2ml Salkowski's reagent. The color change was observed. The experiment was repeated in triplicate. The quantitative screening of the isolates was performed according to Chandra et al.<a class="elsevierStyleCrossRef" href="#bib0180">3</a>. Briefly, after the development of a red color from the qualitative screening, the isolates were placed in the dark for about 2h and analyzed on a spectrophotometer at 530nm against different standards ranging from 20 to 200μg/ml.Detection of cellulolytic activityThe bacterial strains were inoculated in carboxymethylcellulose media (KH2PO4, Na2HPO4·7H2O, (NH4)2SO4, MgSO4·7H2O, CaCl2, FeSO4·7H2O, MnSO4, CMC and agar, pH 7.0) as described by Kumar et al.<a class="elsevierStyleCrossRef" href="#bib0230">13</a> with slight modifications, followed by incubation for 24–48h at 37°C. The 2ml of Gram iodine was added for 10min followed by the addition of a 2M NaCl solution. The plates were examined for clear halo zones.Hydrogen cyanide productionHydrogen cyanide formation was detected using the method described by Passari et al.<a class="elsevierStyleCrossRef" href="#bib0260">19</a>. Briefly, each isolate was streaked on a nutrient agar medium added with glycine (4.4g/L). The freshly streaked agar was covered with filter paper (Whattman no. 1) previously flooded with solution (0.5% picric acid and 2% sodium carbonate). The parafilm wrapped plates were incubated at 37°C for 7 days. The change of color from yellow to orange indicates positive results for hydrogen cyanide production.Siderophore productionThe bacterial strains were assessed for siderophore production by using Chrome Azurol-S agar medium, as described by Sheeba et al.<a class="elsevierStyleCrossRef" href="#bib0290">25</a>. The isolates were point inoculated at the center of a CAS agar medium plate and incubated at 30°C for 48–72h; the formation of a yellow to orange halo zone around the colony shows siderophore production.Molecular volatile organic compound production assayThe divide plate method was used to evaluate the production of VOC as described by Yuan et al.<a class="elsevierStyleCrossRef" href="#bib0330">33</a> with slight modifications. Briefly, the two compartments of divide plates were filled with LB agar and PDA respectively. The LB agar containing sides were inoculated with bacterial isolates except the control plate. The PDA side was used for fungal strains. The bacterial isolates that showed positive results were further evaluated by the dry fungal biomass assay as mentioned by Khan et al.<a class="elsevierStyleCrossRef" href="#bib0220">11</a>. Briefly, one portion of a centrally partitioned plate was filled with 10ml of LB agar for the growth of biocontrol bacteria while the other side with 10ml PDA for the fungal counterpart. For control, the LB agar side of the divide plate was left uninoculated. The plates were sealed with parafilm and kept at incubation for 7 days at 37°C. The plates were observed for the antifungal effect of volatile organic compounds released by bacterial isolates in terms of the reduction of the fungal dry mass in the treated plate as compared to control. For the observation of the fungal dry mass, the PDA portion was placed on pre-weighed filter paper and desiccated at 65°C. Readings were taken for assessing the reduction in the fungal dry biomass. The experiment was performed in triplicate.Survival study of bacterial isolates in different liquid carrier materialThe selected isolates were analyzed on a cost-effective liquid broth that may have the potential of being used as carrier material on a commercial scale. Three recipes were prepared, with different C, N and P ratios, which can be used as carrier materials (i.e. all of them contain molasses as carbon source, KH2PO4 as phosphorus source and NH4SO4 as nitrogen source), for evaluating the survival of selected bacterial strains. LB broth (enriched media) was used as control. The biocontrol bacteria were inoculated separately in all treatments. Three replicates were prepared for each treatment. The bacterial population was tested at different time intervals from day 0 up to 3 months using the serial dilution method on LB agar medium. The medium after inoculation was kept at 37°C for 72h. Then, the number of colony forming units (CFUs) was counted.ResultsThe aim of this study was to isolate and characterize potential broad spectrum antifungal bacterial isolates that can be used on a commercial scale as bacterial control agents. Along with their antifungal properties, the isolates were characterized for plant growth-promoting activities. The selected isolates were kept on a cost-effective liquid culture to analyze the survival of the isolates.Isolation and screening of bacteria with antifungal activityInitially, 113 bacteria were isolated from the phyllosphere of different crops (i.e. Zea mays, Solanum tuberosum, and Triticum aestivum), 14 isolates (M11, M33, M35, M40, M42, W71, W75, W79, W88, P92, P97, P102, P107 and P110) were selected on the basis of antifungal activity. Looking for bacteria with a wide array of fungicidal activity, further two isolates (M11 and M33) from maize were selected after evaluating them against a panel of phytopathogenic fungi (A. alternata, R. solani, F. oxysporum and F. verticillioides). The two selected bacteria showed strong inhibitory activity against four fungi under study (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). The inhibitory percentages are shown in <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>.<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia>Identification, characterization and phylogenetic analysisMorphologically, isolates M11 and M33 were rod-shaped, endospore-producing Gram positive bacteria. Molecular identification showed that both isolates belonged to the Bacillus genera. Bacterial isolate M11 showed 100% sequence similarity with B. amyloliquefaciens while M33 shared 100% sequence homology with B. subtilis. The phylogenetic tree constructed by using the MEGA X 64 program is shown in <a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>. The bootstrap support was >75%. The sequences of M11 and M33 were deposited in Genbank under accession numbers MW531180 and MW531181 respectively.<elsevierMultimedia ident="fig0015"></elsevierMultimedia>Screening for PGPR traitsIAA production and phosphate solubilizationThe 14 isolates showing inhibitory activity were assessed for IAA production. All of them showed positive results in the presence of l-tryptophan by development of the color (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The phosphate solubilization assay showed that 5 out of 14 isolates were able to solubilize tricalcium phosphate, while the bacterial isolates that showed strong antifungal activity (M11 and M33) were unable to solubilize phosphate (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The quantification data of IAA and phosphate solubilization is shown in <a class="elsevierStyleCrossRef" href="#sec0160">Suppl. Table 1</a>.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Cellulolytic activityThe hydrolyzing zones were clearly observed on CMC agar dishes after the addition of Gram iodine, in the case of all 14 biocontrol bacterial strains including M11 and M33 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).Production of HCN and siderophoresOur data suggested that 10 isolates, including M11, produced HCN as the change of color from yellow to orange, which was clearly observed, while M33 showed a negative result for HCN production (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Siderophores were produced by 7 isolates, including M11 and M33 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).Volatile organic compound productionVolatile organic compound production was assessed by using the divide plate method. Only two bacterial isolates (M11 and M33) showed positive results for VOCs. The significant reduction of fungal dry mass was observed in the treated plates as compared to control. The reduction in the fungal dry mass of A. alternata, R. solani, F. oxysporum and F. verticillioides, due to VOCs, produced by M33 and M11 respectively, is shown in <a class="elsevierStyleCrossRef" href="#fig0020">Figure 4</a>.<elsevierMultimedia ident="fig0020"></elsevierMultimedia>Survival studyThe survival study was conducted only for M11 and M33 as they showed a strong broad spectrum biofungicidal activity. The results showed that B. amyloliquefaciens (M11) and B. subtilis (M33) survived in all three treatments containing molasses with negligible difference in population rate, up to a test duration of 3 months. Therefore, the composition of only one treatment is documented in this paper. The survival rate of isolates in LB media was high as expected; however, with no significant difference between enriched and molasses-based medium (MBM). The survival rate after 90 days of B. amyloliquefaciens (M11) in LB and molasses media was 8.2×107 and 7.1×107 (CFU/ml) respectively, while the survival rate of B. subtilis (M33) was 9×107 and 4.2×107 (CFU/ml) respectively. The graph was plotted using R software (<a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a>).<elsevierMultimedia ident="fig0025"></elsevierMultimedia>DiscussionThe practice of using biological control in fungal disease suppression is an effective alternative to the use of chemical fungicides, which often has deleterious effects on living things and the environment. Nowadays, the researchers are trying to develop eco-friendly methodologies based on biological sources. Although various microorganisms have been used as biological control agents, biofungicidal bacteria are widely utilized for the suppression or inhibition of fungal phytopathogens<a class="elsevierStyleCrossRef" href="#bib0265">20</a>. The present study demonstrates that biocontrol bacteria isolated from the corn phyllosphere are potential candidates to be used as antagonists to phytopathogenic fungi. The screening strategy carried out in this paper consists of the isolation of bacterial strains capable of inhibiting phytopathogenic fungi.Fourteen bacterial strains (M11, M33, M35, M40, M42, W71, W75, W79, W88, P92, P97, P102, P107 and P110) with antifungal activity were isolated; the two isolates from the maize plant (M11 and M33) showed strong inhibition against all four phytopathogenic fungi under study. The bacterial isolates with strong antifungal activity were Gram positive and endospore-producing. They were identified as B. amyloliquefaciens and B. subtilis respectively by 16S rRNA gene sequencing. Among the bacterial antagonists, the Bacillus species are widely reported biocontrol agents<a class="elsevierStyleCrossRef" href="#bib0285">24</a>.VOC production, cell-wall degrading activities and production of secondary metabolites, i.e. HCN and siderophores, seemed to be the possible mechanisms responsible for antagonism in the case of B. amyloliquefaciens and B. subtilis, since cellulolytic activity, VOCs, HCN and siderophore production were clearly detected. It has been previously reported that enzymatic activities, VOCs, HCN and siderophore production correlate with antifungal activity<a class="elsevierStyleCrossRef" href="#bib0240">15</a>. The antagonistic bacterial isolates showed positive results for VOCs and siderophore production whereas HCN production was detected only in the case of B. subtilis. The role of VOCs and HCN (produced by the Bacillus species) in plant-bacterial interactions (i.e. triggering plant growth and defense) has been well-documented<a class="elsevierStyleCrossRefs" href="#bib0295">26,30</a>. Bacillus species are known to produce several VOCs, such as, 2-propanone, phenol, 1-decanol and so on<a class="elsevierStyleCrossRef" href="#bib0220">11</a>. The production of HCN is an important plant growth-promoting activity and has significant toxicity against the number of phytopathogens<a class="elsevierStyleCrossRef" href="#bib0295">26</a>. Bacterial HCN is effective in the control of fungal infections, restraining the cytochrome-C terminal oxidase in the fungal respiratory chains and cause extreme damage to the fungal metabolism. Furthermore, bacterial siderophores indirectly enhance plant growth via inhibiting phytopathogens and creating competition for ferric iron resources in soil<a class="elsevierStyleCrossRef" href="#bib0310">29</a>. Thus, siderophores play a role as iron solubilizing agents by solubilizing iron from minerals or organic compounds under low iron conditions<a class="elsevierStyleCrossRef" href="#bib0215">10</a>.M11 and M33 isolates were found to produce IAA in the presence of L-tryptophan but were unable to solubilize inorganic phosphate. Approximately 80% of the isolated bacteria from the rhizosphere/phyllosphere of different crops can produce and release auxins as secondary metabolites<a class="elsevierStyleCrossRef" href="#bib0215">10</a>. Bacterial IAA promotes plant growth, especially stimulates the overproduction of root hairs to increase the surface area so that the plant can easily uptake water and soil nutrients<a class="elsevierStyleCrossRef" href="#bib0195">6</a>. The studies proved that significant increase is observed in the growth rate of plants inoculated with bacterial IAA when compared to non-inoculated plants<a class="elsevierStyleCrossRef" href="#bib0305">28</a>.Previous studies suggest that using bacterial inoculants such as Bacillus spp., Pseudomonas spp., Azospirillum spp. and others, is beneficial for plant growth promotion and the control of fungal diseases. Based on these qualities (i.e. growth promotion and biocontrol activity) along with their eco-friendly behavior, microbial inoculants are potential candidates for a vast market share around the globe with 15% growth rate per year<a class="elsevierStyleCrossRef" href="#bib0305">28</a>. However, a number of biocontrol agents perform quite well in the laboratory and greenhouse conditions but failed to perform in the field<a class="elsevierStyleCrossRef" href="#bib0210">9</a>. The major limitation for commercialization is the development of an effective bacterial formulation with high survival and rhizosphere colonization rate. Generally, PGPRs are inoculated directly to plant material without a suitable carrier or in inappropriate quantities that are insignificant under field conditions for rhizosphere colonization. In addition, the fumigation of soils with broad spectrum biocidal chemicals affect soil–microbial interaction, causing a lower rate of rhizosphere colonization. The issue can be resolved by a comprehension of the ecological parameters that influence biocontrol agents. To develop the final bioproduct, the selection criteria of the optimal strategy will depend on the balance between stability, efficacy, economic feasibility, and ease of use. Additionally, the transition of PGPR from laboratory to farmers requires an extensive research about survival and mass production of these strains in cost-effective carrier materials. Our data suggested that B. amyloliquefaciens and B. subtilis can easily survive in a cost effective self-prepared media (containing molasses as carbon source) up to 3 months with a significant population rate.ConclusionThe purpose of this study was to characterize the indigenous population of biocontrol bacteria that have broad spectrum fungicidal activity to be used as biofungicides for commercial purposes. It is concluded that the bacterial isolates mentioned in the study not only had broad spectrum fungicidal activity but also additional properties of plant growth-promoting activity. The mentioned isolates had good survival rate in the molasses-based medium, which is a cost-effective nutrient medium compared to the commercial media available in the market. Therefore, the mentioned isolates could be used for commercial purposes to control phytopathogens on a cost-effective nutrient medium.FundingThe authors wish to thank the Higher Education Commission, Pakistan (HEC) for the financial support for this study in the form of research grant HEC-TDF02-13.Conflict of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres1777053" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:3 [ "identificador" => "xres1777054" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1560258" "titulo" => "Keywords" ] 3 => array:3 [ "identificador" => "xres1777055" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0015" ] ] ] 4 => array:2 [ "identificador" => "xpalclavsec1560257" "titulo" => "Palabras clave" ] 5 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 6 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Isolation of bacteria in pure culture" ] 1 => array:3 [ "identificador" => "sec0020" "titulo" => "Preliminary screening of bacterial isolates for antifungal activity" "secciones" => array:1 [ 0 => array:2 [ "identificador" => "sec0025" "titulo" => "Qualitative and quantitative assessment for antagonistic activity in vitro" ] ] ] 2 => array:3 [ "identificador" => "sec0030" "titulo" => "Molecular identification and phylogenetic analysis" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "DNA extraction" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "16S rRNA gene amplification" ] 2 => array:2 [ "identificador" => "sec0045" "titulo" => "Similarity analysis and dendrogram construction" ] ] ] 3 => array:3 [ "identificador" => "sec0050" "titulo" => "Evaluation of biocontrol bacteria for plant growth promoting traits" "secciones" => array:6 [ 0 => array:2 [ "identificador" => "sec0055" "titulo" => "Phosphate solubilization assay" ] 1 => array:2 [ "identificador" => "sec0060" "titulo" => "Indole-3-acetic acid assay" ] 2 => array:2 [ "identificador" => "sec0065" "titulo" => "Detection of cellulolytic activity" ] 3 => array:2 [ "identificador" => "sec0070" "titulo" => "Hydrogen cyanide production" ] 4 => array:2 [ "identificador" => "sec0075" "titulo" => "Siderophore production" ] 5 => array:2 [ "identificador" => "sec0080" "titulo" => "Molecular volatile organic compound production assay" ] ] ] 4 => array:2 [ "identificador" => "sec0085" "titulo" => "Survival study of bacterial isolates in different liquid carrier material" ] ] ] 7 => array:3 [ "identificador" => "sec0090" "titulo" => "Results" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0095" "titulo" => "Isolation and screening of bacteria with antifungal activity" ] 1 => array:2 [ "identificador" => "sec0100" "titulo" => "Identification, characterization and phylogenetic analysis" ] 2 => array:3 [ "identificador" => "sec0105" "titulo" => "Screening for PGPR traits" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0110" "titulo" => "IAA production and phosphate solubilization" ] 1 => array:2 [ "identificador" => "sec0115" "titulo" => "Cellulolytic activity" ] 2 => array:2 [ "identificador" => "sec0120" "titulo" => "Production of HCN and siderophores" ] 3 => array:2 [ "identificador" => "sec0125" "titulo" => "Volatile organic compound production" ] ] ] 3 => array:2 [ "identificador" => "sec0130" "titulo" => "Survival study" ] ] ] 8 => array:2 [ "identificador" => "sec0135" "titulo" => "Discussion" ] 9 => array:2 [ "identificador" => "sec0140" "titulo" => "Conclusion" ] 10 => array:2 [ "identificador" => "sec0145" "titulo" => "Funding" ] 11 => array:2 [ "identificador" => "sec0150" "titulo" => "Conflict of interest" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2020-10-24" "fechaAceptado" => "2021-10-03" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1560258" "palabras" => array:4 [ 0 => "Phytopathogen" 1 => "Antagonistic" 2 => "Broad spectrum" 3 => "Biofungicides" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1560257" "palabras" => array:4 [ 0 => "Fitopatógeno" 1 => "Antagonista" 2 => "Amplio espectro" 3 => "Biofungicida" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Bacteria had broad-spectrum activity against phytopathogenic fungi (>50% inhibition).</li><li class="elsevierStyleListItem" id="lsti0010">•Selected isolates were identified with molecular methods and analyzed for plant growth-promoting activities.</li><li class="elsevierStyleListItem" id="lsti0015">•The selected isolates had a good survival rate in a cost-effective medium.</li><li class="elsevierStyleListItem" id="lsti0020">•Assessed medium can be used for commercial fermentation of bio-control agents.</li></ul>" ] "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "The current study intended to isolate, characterize and identify biocontrol bacteria possessing broad-spectrum antifungal activity from the phyllosphere of different crops including maize, wheat and potato and to assess their growth-promoting activity. In this study 14/113 biocontrol bacteria showed antifungal activity. Bacterial isolates M11 and M33 from maize out of 113 were re-selected on the basis of their strong (more than 50%) broad spectrum antifungal activity after their assessment against four economically important phytopathogenic fungi including Alternaria alternata, Rhizoctonia solani, Fusarium oxysporum and Fusarium verticillioides. The isolates were further assessed for plant growth promoting traits, i.e., indole-3-acetic acid production, phosphate solubilization, production of cellulase, microbial volatile compounds, hydrogen cyanide and siderophores. All fourteen isolates showed positive results for the production of indole-3-acetic acid hormone and cellulase enzyme, 10 isolates were positive for hydrogen cyanide production; siderophores production was observed in 7 isolates while 5 isolates showed ability to solubilize inorganic phosphate. Microbial volatile compounds were only synthesized by M11 and M33, which were identified as Bacillus amyloliquefaciens and Bacillus subtilis respectively by 16S rRNA gene sequencing. The survival study revealed that biocontrol bacteria B. amyloliquefaciens and B. subtilis have the ability to survive in cost effective molasses containing carrier material up to a three-month period." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Este estudio tuvo como objetivo aislar, caracterizar e identificar bacterias de control biológico que poseen actividad antifúngica de amplio espectro de la filosfera de diferentes cultivos, incluidos el maíz, el trigo y la papa, así como evaluar su actividad en la promoción del crecimiento. En este estudio, 14/113 bacterias de control biológico mostraron actividad antifúngica. Los aislamientos bacterianos M11 y M33 (de maíz), del total de 113, fueron reseleccionados debido a su fuerte actividad antifúngica de amplio espectro (más del 50%) después de su evaluación contra cuatro hongos fitopatógenos que afectan cultivos de alta importancia económica, entre ellos, Alternaria alternata, Rhizoctonia solani, Fusarium oxysporum y Fusarium verticillioides. Los aislamientos se evaluaron, adicionalmente, para determinar los rasgos que promueven el crecimiento de las plantas, es decir, producción de ácido indolacético, solubilización de fosfato, producción de celulasa, compuestos orgánicos volátiles microbianos, cianuro de hidrógeno y sideróforos. Las 14 cepas aisladas mostraron resultados positivos para la producción de la hormona ácido indolacético y la enzima celulasa; 10 cepas fueron positivas para la producción de cianuro de hidrógeno. Además, se observó producción de sideróforos en el caso de 7 cepas, mientras que 5 pudieron solubilizar fosfato inorgánico. Los compuestos orgánicos volátiles microbianos solo fueron sintetizados por los aislamientos M11 y M33, que fueron identificados como Bacillus amyloliquefaciens y Bacillus subtilis, respectivamente, mediante secuenciación del gen ARNr 16S. El estudio de supervivencia mostró que las bacterias de control biológico, es decir, B. amyloliquefaciens y B. subtilis, tienen la capacidad de sobrevivir sobre un sustrato a base de melasa, por un período de tres meses." ] ] "NotaPie" => array:1 [ 0 => array:3 [ "etiqueta" => "1" "nota" => "Co-first author, both the authors contributed equally." "identificador" => "fn0005" ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "The following are the supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0160" ] ] ] ] "multimedia" => array:8 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2141 "Ancho" => 2508 "Tamanyo" => 612525 ] ] "descripcion" => array:1 [ "en" => "Antagonistic activity of bacterial isolates (M11 and M33) against (a) A. alternata, (b) R. solani, (c) F. oxysporum and (d) F. verticillioides." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1204 "Ancho" => 2508 "Tamanyo" => 216595 ] ] "descripcion" => array:1 [ "en" => "Graphical representation of the% suppression of growth of phytopathogenic fungi under study using biocontrol bacteria. The y-axis shows the inhibition percentages, while the x-axis represents the bacterial isolates. The bars show the standard error mean computed by using Microsoft Excel." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2685 "Ancho" => 2508 "Tamanyo" => 476322 ] ] "descripcion" => array:1 [ "en" => "Cladogram constructed by using ClustalW and MEGA 6.4 software. Node values show bootstrap support when neighbor-joining was done for 1000 resampled datasets. The scale bar represents the nucleotide substitutions per 100 nucleotides." ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 1349 "Ancho" => 2486 "Tamanyo" => 156747 ] ] "descripcion" => array:1 [ "en" => "Graphical representation of fungal dry mass reduction (%) by VOCs produced by bacterial isolates (M11 and M33). The y-axis represents reduction percentages, while the x-axis shows two selected bacterial isolates (M11 and M33). The bars show the standard error mean computed using Microsoft Excel." ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 812 "Ancho" => 2508 "Tamanyo" => 118057 ] ] "descripcion" => array:1 [ "en" => "Survival of biocontrol bacteria in molasses-based medium (MBM) compared to control, where the x-axis represents the sampling days (0–90 days) and the y-axis shows the CFU count. (A) B. amyloliquefaciens (M11) survival in MBM compared to LB control medium; (B) B. subtilis (M33) in two different media, LB medium (control) and molasses-based medium (MBM)." ] ] 5 => 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 [ "leyenda" => "IAA: indole acetic acid; PS: phosphate solubilization; Cel: cellulase production; HCN: hydrogen cyanide; Sid: siderophores. The (+/−) indicates positive and negative results respectively." "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">Bacterial isolates \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">IAA \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">PS \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">Cel \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">HCN \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">Sid \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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">M11 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">M33 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">M35 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">M40 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">M42 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">W71 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">W75 \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="left" 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="left" 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="left" 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="left" 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="left" 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="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">W79 \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="left" 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="left" 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="left" 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="left" 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="left" 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 ; 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Caracterización y supervivencia de agentes de control biológico de amplio espectro frente a hongos fitopatógenos

Saba Azeema,1, Syed Inayatullah Aghaa,1, Neelam Jamilb, Bushra Tabassumc,d, Shan Ahmeda, Asif Raheemb, Nusrat Jahana, Niaz Alie, Anwar Khanb,

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anwarleo2003@gmail.com

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a Department of Biotechnology and Informatics, BUITEMS, Quetta, Pakistan

b Department of Microbiology, BUITEMS, Quetta, Pakistan

c Center of Excellence in Molecular Biology, University of the Punjab, Lahore, Pakistan

d School of Biological Sciences, University of the Punjab, Lahore, Pakistan

e Department of Botany, Hazara University, Mansehra, Pakistan

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Some of the most common plant-pathogenic fungi belong to the genera <span class="elsevierStyleItalic">Alternaria</span>&#44; <span class="elsevierStyleItalic">Fusarium</span>&#44; <span class="elsevierStyleItalic">Botrytis</span>&#44; <span class="elsevierStyleItalic">Geotrichum</span>&#44; <span class="elsevierStyleItalic">Penicillium</span> and <span class="elsevierStyleItalic">Sclerotinia</span>&#46; These fungi are responsible for causing considerable crop yield loss worldwide<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">16</span></a>&#46; Efficient plant disease management is the prerequisite of sustainable agriculture&#46; Plant diseases need to be contained to sustain the quantity and quality of food and fiber produced by agriculturists throughout the world&#46; Various strategies might be utilized to avoid&#44; alleviate or restrict plant diseases<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">4</span></a>&#46; In the past few decades&#44; synthetic fungicides played a fundamental function in suppressing plant diseases and enhancing crop yield to reduce food insecurity in today&#39;s world<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">32</span></a>&#46; However&#44; recent studies&#44; reported that the prolonged use of chemicals could cause harmful effects&#44; including environmental and health hazards&#44; residual toxicity and resistance of pathogens&#44; among others&#46; Furthermore&#44; agrochemicals are not very cost effective<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">32</span></a>&#46; Consequently&#44; scientists have focused their efforts on formulating alternate sources to synthetic agrochemicals for limiting pests and diseases&#46; Among these alternatives&#44; biological controls are much preferred&#46; Biological control in plant pathology refers to the suppression of growth or reproduction of a pathogenic organism using another organism&#46; It utilizes the natural enemies of pests or pathogens to eliminate or contain their population&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Nowadays more attention is paid to developing useful approaches for environmentally friendly and sustainable agricultural practices&#44; mainly depending on the application and use of beneficial microorganisms&#44; particularly plant growth promoting bacteria &#40;PGPB&#41; as biofertilizers or bio-pesticides<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">9</span></a>&#46; PGPB are capable to stimulate plant yield and restrict phytopathogens and could be used as an alternative source to limiting the usage of chemical fungicides&#46; PGPBs are defined as a wide array of bacteria that colonize the plant phyllosphere&#47;rhizosphere and are usually involved in several beneficial activities such as the improvement of plant growth by increasing seed development&#44; plant weight&#44; and crop yield&#46; They can influence plant health either directly or indirectly&#46; The direct mechanisms include production of hormones &#40;indole acetic acid&#44; cytokinins&#44; gibberellins&#44; among others&#41;&#44; phosphate solubilization&#44; nitrogen fixation&#44; biofilm formation&#44; siderophores production&#44; mineral solubilization and plant resistance to abiotic stresses&#46; The indirect mechanisms include restricting plant pathogens by producing enzymes &#40;i&#46;e&#46; cellulase&#44; chitinase&#44; glucanase&#41;&#44; volatile compounds &#40;VC&#41;&#44; secondary metabolites and by competing for space and nutrients<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">9</span></a>&#46; The most reported biocontrol bacteria belong to the <span class="elsevierStyleItalic">Bacillus</span> and <span class="elsevierStyleItalic">Pseudomonas</span> genera that can possibly promote plant growth and inhibit fungal pathogens<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">8&#44;17</span></a>&#46; 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The phytopathogenic fungi used in this study <span class="elsevierStyleItalic">Alternaria alternata</span>&#44; <span class="elsevierStyleItalic">Fusarium oxysporum</span>&#44; <span class="elsevierStyleItalic">Fusarium verticillioides</span> and <span class="elsevierStyleItalic">Rhizoctonia solani</span> were kindly provided by ARS USDA&#46; The fungi were cultured on potato dextrose agar &#40;PDA&#41; and incubated at 28<span class="elsevierStyleHsp" style=""></span>&#176;C for 7 days for further experimentation&#46; The bacteria with inhibitory activity were selected for further characterization&#46;</p><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Qualitative and quantitative assessment for antagonistic activity in vitro</span><p id="par0060" class="elsevierStylePara elsevierViewall">The qualitative assessment was performed according to Awais et al&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">28</span></a>&#46; The bacterial strains were cultured against each of the fungus on separate PDA plates using the agar plug method&#46; About 4<span class="elsevierStyleHsp" style=""></span>mm agar discs of previously cultivated phytopathogenic fungi were inoculated at the center of PDA plates&#46; Bacterial isolates were inoculated with a sterilized wire loop on two sides of Petri dishes at a distance of 3<span class="elsevierStyleHsp" style=""></span>cm from the fungal plug&#46; The dishes were incubated at 28<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 days&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The bacterial isolates with antifungal properties were subjected to quantitative evaluation&#46; The dual culture method was performed according to Haidar et al&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">7</span></a>&#46; Briefly&#44; fungal strains were grown on PDA plates for about 7 days&#44; a 4<span class="elsevierStyleHsp" style=""></span>mm agar disc was excised with a disinfected scalpel and placed at the center of a separate plate&#46; The bacterial isolates to be assessed were co-inoculated on the same agar plate at a distance of 2&#46;5<span class="elsevierStyleHsp" style=""></span>cm from the fungal disc in a straight line&#46; Control plates were cultured only with the fungal pathogen&#46; Dishes were incubated for 5 days at 28<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The experiment was performed in triplicate&#46; The inhibition percentage was calculated by using a given formula&#59;<elsevierMultimedia ident="eq0005"></elsevierMultimedia>where <span class="elsevierStyleItalic">R</span>2 is the growth of fungus toward the control side of the Petri dish and R1 is the outward growth of the fungus in the direction of the antagonistic bacteria&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Molecular identification and phylogenetic analysis</span><p id="par0070" class="elsevierStylePara elsevierViewall">The selected bacterial strains were primarily identified by Gram staining and endospore staining followed by molecular identification&#46;</p><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">DNA extraction</span><p id="par0075" class="elsevierStylePara elsevierViewall">The total genomic DNA from freshly cultured bacterial isolates was extracted by using Thermo Scientific&#8482; &#35;K0721 as per the manufacturer&#39;s protocol&#46; Proteinase K and RNase A were used for protein digestion and removal of RNA respectively&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">16S rRNA gene amplification</span><p id="par0080" class="elsevierStylePara elsevierViewall">The amplification of the 16S rRNA gene was performed according to the method described by Ramzan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">22</span></a>&#46; The primers used to amplify a 1&#46;5<span class="elsevierStyleHsp" style=""></span>kb gene fragment were 27F and 1492R&#46;<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">31</span></a> The polymerase chain reaction was performed in a thermal cycler &#40;T100 Thermal Cycler&#41; in 20<span class="elsevierStyleHsp" style=""></span>&#956;l reaction mixture containing 0&#46;1<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;l of each primer&#44; 2&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;l MgCl<span class="elsevierStyleInf">2</span>&#44; 1<span class="elsevierStyleHsp" style=""></span>&#956;mol&#47;l of each deoxynucleoside triphosphate &#40;dNTP&#41;&#44; 50<span class="elsevierStyleHsp" style=""></span>ng&#47;&#956;l of template DNA and 2<span class="elsevierStyleHsp" style=""></span>U&#47;&#956;l <span class="elsevierStyleItalic">Taq</span> DNA polymerase &#40;Thermoscientific&#44; USA&#41;&#46; The PCR amplification consisted of DNA denaturation at 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min followed by 35 cycles of denaturation at 95<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#44; annealing at 57<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#44; extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 1&#46;5<span class="elsevierStyleHsp" style=""></span>min and final extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 10<span class="elsevierStyleHsp" style=""></span>min&#46; The PCR products were analyzed by electrophoresis in a 1&#37; agarose gel in 1&#215; TBE &#40;Tris&#8211;borate&#8211;EDTA&#41; buffer with ethidium bromide staining&#46; The purified PCR products were sequenced by using the facility of Macrogen &#40;Korea&#41;&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Similarity analysis and dendrogram construction</span><p id="par0085" class="elsevierStylePara elsevierViewall">The 16S rRNA gene sequences were compared with the NCBI database using BlastN&#46; Further&#44; identification of phylogenetic neighbors and calculation of pairwise similarity of these sequences were done using ClustalW and MEGA 6&#46;4<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">14</span></a> software as described by Ramazan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">22</span></a>&#46; The phylogenetic tree was constructed by using a neighbor-joining method&#46; The bootstrap replications &#40;1000 replicates&#41; were used for statistical support&#46;</p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Evaluation of biocontrol bacteria for plant growth promoting traits</span><p id="par0090" class="elsevierStylePara elsevierViewall">The biocontrol bacteria were evaluated for their plant growth-promoting traits&#46; The parameters selected for evaluating PGP activity were&#58; phosphate solubilizing activity&#44; indole acetic acid &#40;IAA&#41;&#44; hydrogen cyanide &#40;HCN&#41;&#44; cellulase&#44; siderophore and VOC production&#46;</p><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Phosphate solubilization assay</span><p id="par0095" class="elsevierStylePara elsevierViewall">National Botanical Research Institute Phosphate growth medium &#40;NBRIP&#41; agar containing insoluble tri-calcium phosphate was prepared as previously described<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">18</span></a>&#46; The pH of NBRIP agar was adjusted to 7&#46;0&#46; The bacterial strains were spot inoculated at the center of NBRIP agar plates&#46; NBRIP agar without bacterial inoculation was taken as control&#46; The dishes were kept at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 72<span class="elsevierStyleHsp" style=""></span>h and were observed for formation of a clear halo zone&#46; The quantification of phosphate solubilization was performed according to Chandra et al&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">3</span></a> by measuring the yellow color on a spectrophotometer at 880<span class="elsevierStyleHsp" style=""></span>nm&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Indole-3-acetic acid assay</span><p id="par0100" class="elsevierStylePara elsevierViewall">The bacterial isolates were screened for indole 3-acetic acid &#40;IAA&#41; production according to Sivasankari<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">27</span></a>&#46; Briefly&#44; isolated bacteria were cultured in autoclaved LB broth in a 100<span class="elsevierStyleHsp" style=""></span>ml Erlenmeyer flask with and without the addition of 0&#46;1<span class="elsevierStyleHsp" style=""></span>g of <span class="elsevierStyleSmallCaps">l</span>-tryptophan &#40;Sigma Aldrich&#41;&#46; The 100<span class="elsevierStyleHsp" style=""></span>ml Erlenmeyer flask containing uninoculated sterile LB broth was taken as negative control&#46; All flasks were incubated in a shaking incubator at 37<span class="elsevierStyleHsp" style=""></span>&#176;C and 100<span class="elsevierStyleHsp" style=""></span>rpm for 48<span class="elsevierStyleHsp" style=""></span>h&#46; Salkowski&#39;s reagent &#40;1<span class="elsevierStyleHsp" style=""></span>ml of 0&#46;5<span class="elsevierStyleHsp" style=""></span>M FeCl<span class="elsevierStyleInf">3</span>&#183;6H<span class="elsevierStyleInf">2</span>O in 50<span class="elsevierStyleHsp" style=""></span>ml of 35&#37; perchloric acid&#41; was prepared for IAA detection&#46; In properly labeled test tubes&#44; 1<span class="elsevierStyleHsp" style=""></span>ml of culture supernatants was mixed with the addition of 2<span class="elsevierStyleHsp" style=""></span>ml Salkowski&#39;s reagent&#46; The color change was observed&#46; The experiment was repeated in triplicate&#46; The quantitative screening of the isolates was performed according to Chandra et al&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">3</span></a>&#46; Briefly&#44; after the development of a red color from the qualitative screening&#44; the isolates were placed in the dark for about 2<span class="elsevierStyleHsp" style=""></span>h and analyzed on a spectrophotometer at 530<span class="elsevierStyleHsp" style=""></span>nm against different standards ranging from 20 to 200<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Detection of cellulolytic activity</span><p id="par0105" class="elsevierStylePara elsevierViewall">The bacterial strains were inoculated in carboxymethylcellulose media &#40;KH<span class="elsevierStyleInf">2</span>PO<span class="elsevierStyleInf">4</span>&#44; Na<span class="elsevierStyleInf">2</span>HPO<span class="elsevierStyleInf">4</span>&#183;7H<span class="elsevierStyleInf">2</span>O&#44; &#40;NH<span class="elsevierStyleInf">4</span>&#41;<span class="elsevierStyleInf">2</span>SO<span class="elsevierStyleInf">4</span>&#44; MgSO<span class="elsevierStyleInf">4</span>&#183;7H<span class="elsevierStyleInf">2</span>O&#44; CaCl<span class="elsevierStyleInf">2</span>&#44; FeSO<span class="elsevierStyleInf">4</span>&#183;7H<span class="elsevierStyleInf">2</span>O&#44; MnSO<span class="elsevierStyleInf">4</span>&#44; CMC and agar&#44; pH 7&#46;0&#41; as described by Kumar et al&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">13</span></a> with slight modifications&#44; followed by incubation for 24&#8211;48<span class="elsevierStyleHsp" style=""></span>h at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The 2<span class="elsevierStyleHsp" style=""></span>ml of Gram iodine was added for 10<span class="elsevierStyleHsp" style=""></span>min followed by the addition of a 2<span class="elsevierStyleHsp" style=""></span>M NaCl solution&#46; The plates were examined for clear halo zones&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Hydrogen cyanide production</span><p id="par0110" class="elsevierStylePara elsevierViewall">Hydrogen cyanide formation was detected using the method described by Passari et al&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">19</span></a>&#46; Briefly&#44; each isolate was streaked on a nutrient agar medium added with glycine &#40;4&#46;4<span class="elsevierStyleHsp" style=""></span>g&#47;L&#41;&#46; The freshly streaked agar was covered with filter paper &#40;Whattman no&#46; 1&#41; previously flooded with solution &#40;0&#46;5&#37; picric acid and 2&#37; sodium carbonate&#41;&#46; The parafilm wrapped plates were incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 7 days&#46; The change of color from yellow to orange indicates positive results for hydrogen cyanide production&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Siderophore production</span><p id="par0115" class="elsevierStylePara elsevierViewall">The bacterial strains were assessed for siderophore production by using Chrome Azurol-S agar medium&#44; as described by Sheeba et al&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">25</span></a>&#46; The isolates were point inoculated at the center of a CAS agar medium plate and incubated at 30<span class="elsevierStyleHsp" style=""></span>&#176;C for 48&#8211;72<span class="elsevierStyleHsp" style=""></span>h&#59; the formation of a yellow to orange halo zone around the colony shows siderophore production&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Molecular volatile organic compound production assay</span><p id="par0120" class="elsevierStylePara elsevierViewall">The divide plate method was used to evaluate the production of VOC as described by Yuan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">33</span></a> with slight modifications&#46; Briefly&#44; the two compartments of divide plates were filled with LB agar and PDA respectively&#46; The LB agar containing sides were inoculated with bacterial isolates except the control plate&#46; The PDA side was used for fungal strains&#46; The bacterial isolates that showed positive results were further evaluated by the dry fungal biomass assay as mentioned by Khan et al&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">11</span></a>&#46; Briefly&#44; one portion of a centrally partitioned plate was filled with 10<span class="elsevierStyleHsp" style=""></span>ml of LB agar for the growth of biocontrol bacteria while the other side with 10<span class="elsevierStyleHsp" style=""></span>ml PDA for the fungal counterpart&#46; For control&#44; the LB agar side of the divide plate was left uninoculated&#46; The plates were sealed with parafilm and kept at incubation for 7 days at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; The plates were observed for the antifungal effect of volatile organic compounds released by bacterial isolates in terms of the reduction of the fungal dry mass in the treated plate as compared to control&#46; For the observation of the fungal dry mass&#44; the PDA portion was placed on pre-weighed filter paper and desiccated at 65<span class="elsevierStyleHsp" style=""></span>&#176;C&#46; Readings were taken for assessing the reduction in the fungal dry biomass&#46; The experiment was performed in triplicate&#46;</p></span></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Survival study of bacterial isolates in different liquid carrier material</span><p id="par0125" class="elsevierStylePara elsevierViewall">The selected isolates were analyzed on a cost-effective liquid broth that may have the potential of being used as carrier material on a commercial scale&#46; Three recipes were prepared&#44; with different C&#44; N and P ratios&#44; which can be used as carrier materials &#40;i&#46;e&#46; all of them contain molasses as carbon source&#44; KH<span class="elsevierStyleInf">2</span>PO<span class="elsevierStyleInf">4</span> as phosphorus source and NH<span class="elsevierStyleInf">4</span>SO<span class="elsevierStyleInf">4</span> as nitrogen source&#41;&#44; for evaluating the survival of selected bacterial strains&#46; LB broth &#40;enriched media&#41; was used as control&#46; The biocontrol bacteria were inoculated separately in all treatments&#46; Three replicates were prepared for each treatment&#46; The bacterial population was tested at different time intervals from day 0 up to 3 months using the serial dilution method on LB agar medium&#46; The medium after inoculation was kept at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 72<span class="elsevierStyleHsp" style=""></span>h&#46; Then&#44; the number of colony forming units &#40;CFUs&#41; was counted&#46;</p></span></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Results</span><p id="par0130" class="elsevierStylePara elsevierViewall">The aim of this study was to isolate and characterize potential broad spectrum antifungal bacterial isolates that can be used on a commercial scale as bacterial control agents&#46; Along with their antifungal properties&#44; the isolates were characterized for plant growth-promoting activities&#46; The selected isolates were kept on a cost-effective liquid culture to analyze the survival of the isolates&#46;</p><span id="sec0095" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Isolation and screening of bacteria with antifungal activity</span><p id="par0135" class="elsevierStylePara elsevierViewall">Initially&#44; 113 bacteria were isolated from the phyllosphere of different crops &#40;i&#46;e&#46; <span class="elsevierStyleItalic">Zea mays</span>&#44; <span class="elsevierStyleItalic">Solanum tuberosum</span>&#44; and <span class="elsevierStyleItalic">Triticum aestivum</span>&#41;&#44; 14 isolates &#40;M11&#44; M33&#44; M35&#44; M40&#44; M42&#44; W71&#44; W75&#44; W79&#44; W88&#44; P92&#44; P97&#44; P102&#44; P107 and P110&#41; were selected on the basis of antifungal activity&#46; Looking for bacteria with a wide array of fungicidal activity&#44; further two isolates &#40;M11 and M33&#41; from maize were selected after evaluating them against a panel of phytopathogenic fungi &#40;<span class="elsevierStyleItalic">A&#46; alternata</span>&#44; <span class="elsevierStyleItalic">R&#46; solani</span>&#44; <span class="elsevierStyleItalic">F&#46; oxysporum</span> and <span class="elsevierStyleItalic">F&#46; verticillioides</span>&#41;&#46; The two selected bacteria showed strong inhibitory activity against four fungi under study &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; The inhibitory percentages are shown in <a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0100" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Identification&#44; characterization and phylogenetic analysis</span><p id="par0140" class="elsevierStylePara elsevierViewall">Morphologically&#44; isolates M11 and M33 were rod-shaped&#44; endospore-producing Gram positive bacteria&#46; Molecular identification showed that both isolates belonged to the <span class="elsevierStyleItalic">Bacillus</span> genera&#46; Bacterial isolate M11 showed 100&#37; sequence similarity with <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> while M33 shared 100&#37; sequence homology with <span class="elsevierStyleItalic">B&#46; subtilis</span>&#46; The phylogenetic tree constructed by using the MEGA X 64 program is shown in <a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>&#46; The bootstrap support was &#62;75&#37;&#46; The sequences of M11 and M33 were deposited in Genbank under accession numbers MW531180 and MW531181 respectively&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0105" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Screening for PGPR traits</span><span id="sec0110" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">IAA production and phosphate solubilization</span><p id="par0145" class="elsevierStylePara elsevierViewall">The 14 isolates showing inhibitory activity were assessed for IAA production&#46; All of them showed positive results in the presence of <span class="elsevierStyleSmallCaps">l</span>-tryptophan by development of the color &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The phosphate solubilization assay showed that 5 out of 14 isolates were able to solubilize tricalcium phosphate&#44; while the bacterial isolates that showed strong antifungal activity &#40;M11 and M33&#41; were unable to solubilize phosphate &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The quantification data of IAA and phosphate solubilization is shown in <a class="elsevierStyleCrossRef" href="#sec0160">Suppl&#46; Table 1</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0115" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Cellulolytic activity</span><p id="par0150" class="elsevierStylePara elsevierViewall">The hydrolyzing zones were clearly observed on CMC agar dishes after the addition of Gram iodine&#44; in the case of all 14 biocontrol bacterial strains including M11 and M33 &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p></span><span id="sec0120" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Production of HCN and siderophores</span><p id="par0155" class="elsevierStylePara elsevierViewall">Our data suggested that 10 isolates&#44; including M11&#44; produced HCN as the change of color from yellow to orange&#44; which was clearly observed&#44; while M33 showed a negative result for HCN production &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Siderophores were produced by 7 isolates&#44; including M11 and M33 &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p></span><span id="sec0125" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Volatile organic compound production</span><p id="par0160" class="elsevierStylePara elsevierViewall">Volatile organic compound production was assessed by using the divide plate method&#46; Only two bacterial isolates &#40;M11 and M33&#41; showed positive results for VOCs&#46; The significant reduction of fungal dry mass was observed in the treated plates as compared to control&#46; The reduction in the fungal dry mass of <span class="elsevierStyleItalic">A&#46; alternata</span>&#44; <span class="elsevierStyleItalic">R&#46; solani</span>&#44; <span class="elsevierStyleItalic">F&#46; oxysporum</span> and <span class="elsevierStyleItalic">F&#46; verticillioides</span>&#44; due to VOCs&#44; produced by M33 and M11 respectively&#44; is shown in <a class="elsevierStyleCrossRef" href="#fig0020">Figure 4</a>&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span></span><span id="sec0130" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0155">Survival study</span><p id="par0165" class="elsevierStylePara elsevierViewall">The survival study was conducted only for M11 and M33 as they showed a strong broad spectrum biofungicidal activity&#46; The results showed that <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> &#40;M11&#41; and <span class="elsevierStyleItalic">B&#46; subtilis</span> &#40;M33&#41; survived in all three treatments containing molasses with negligible difference in population rate&#44; up to a test duration of 3 months&#46; Therefore&#44; the composition of only one treatment is documented in this paper&#46; The survival rate of isolates in LB media was high as expected&#59; however&#44; with no significant difference between enriched and molasses-based medium &#40;MBM&#41;&#46; The survival rate after 90 days of <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> &#40;M11&#41; in LB and molasses media was 8&#46;2<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span> and 7&#46;1<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span> &#40;CFU&#47;ml&#41; respectively&#44; while the survival rate of <span class="elsevierStyleItalic">B&#46; subtilis</span> &#40;M33&#41; was 9<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span> and 4&#46;2<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">7</span> &#40;CFU&#47;ml&#41; respectively&#46; The graph was plotted using R software &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>&#41;&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia></span></span><span id="sec0135" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0160">Discussion</span><p id="par0170" class="elsevierStylePara elsevierViewall">The practice of using biological control in fungal disease suppression is an effective alternative to the use of chemical fungicides&#44; which often has deleterious effects on living things and the environment&#46; Nowadays&#44; the researchers are trying to develop eco-friendly methodologies based on biological sources&#46; Although various microorganisms have been used as biological control agents&#44; biofungicidal bacteria are widely utilized for the suppression or inhibition of fungal phytopathogens<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">20</span></a>&#46; The present study demonstrates that biocontrol bacteria isolated from the corn phyllosphere are potential candidates to be used as antagonists to phytopathogenic fungi&#46; The screening strategy carried out in this paper consists of the isolation of bacterial strains capable of inhibiting phytopathogenic fungi&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">Fourteen bacterial strains &#40;M11&#44; M33&#44; M35&#44; M40&#44; M42&#44; W71&#44; W75&#44; W79&#44; W88&#44; P92&#44; P97&#44; P102&#44; P107 and P110&#41; with antifungal activity were isolated&#59; the two isolates from the maize plant &#40;M11 and M33&#41; showed strong inhibition against all four phytopathogenic fungi under study&#46; The bacterial isolates with strong antifungal activity were Gram positive and endospore-producing&#46; They were identified as <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> and <span class="elsevierStyleItalic">B&#46; subtilis</span> respectively by 16S rRNA gene sequencing&#46; Among the bacterial antagonists&#44; the <span class="elsevierStyleItalic">Bacillus</span> species are widely reported biocontrol agents<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">24</span></a>&#46;</p><p id="par0180" class="elsevierStylePara elsevierViewall">VOC production&#44; cell-wall degrading activities and production of secondary metabolites&#44; i&#46;e&#46; HCN and siderophores&#44; seemed to be the possible mechanisms responsible for antagonism in the case of <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> and <span class="elsevierStyleItalic">B&#46; subtilis</span>&#44; since cellulolytic activity&#44; VOCs&#44; HCN and siderophore production were clearly detected&#46; It has been previously reported that enzymatic activities&#44; VOCs&#44; HCN and siderophore production correlate with antifungal activity<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">15</span></a>&#46; The antagonistic bacterial isolates showed positive results for VOCs and siderophore production whereas HCN production was detected only in the case of <span class="elsevierStyleItalic">B&#46; subtilis</span>&#46; The role of VOCs and HCN &#40;produced by the <span class="elsevierStyleItalic">Bacillus</span> species&#41; in plant-bacterial interactions &#40;i&#46;e&#46; triggering plant growth and defense&#41; has been well-documented<a class="elsevierStyleCrossRefs" href="#bib0295"><span class="elsevierStyleSup">26&#44;30</span></a>&#46; <span class="elsevierStyleItalic">Bacillus</span> species are known to produce several VOCs&#44; such as&#44; 2-propanone&#44; phenol&#44; 1-decanol and so on<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">11</span></a>&#46; The production of HCN is an important plant growth-promoting activity and has significant toxicity against the number of phytopathogens<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">26</span></a>&#46; Bacterial HCN is effective in the control of fungal infections&#44; restraining the cytochrome-C terminal oxidase in the fungal respiratory chains and cause extreme damage to the fungal metabolism&#46; Furthermore&#44; bacterial siderophores indirectly enhance plant growth via inhibiting phytopathogens and creating competition for ferric iron resources in soil<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">29</span></a>&#46; Thus&#44; siderophores play a role as iron solubilizing agents by solubilizing iron from minerals or organic compounds under low iron conditions<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0185" class="elsevierStylePara elsevierViewall">M11 and M33 isolates were found to produce IAA in the presence of L-tryptophan but were unable to solubilize inorganic phosphate&#46; Approximately 80&#37; of the isolated bacteria from the rhizosphere&#47;phyllosphere of different crops can produce and release auxins as secondary metabolites<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">10</span></a>&#46; Bacterial IAA promotes plant growth&#44; especially stimulates the overproduction of root hairs to increase the surface area so that the plant can easily uptake water and soil nutrients<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">6</span></a>&#46; The studies proved that significant increase is observed in the growth rate of plants inoculated with bacterial IAA when compared to non-inoculated plants<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">28</span></a>&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">Previous studies suggest that using bacterial inoculants such as <span class="elsevierStyleItalic">Bacillus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Pseudomonas</span> spp&#46;&#44; <span class="elsevierStyleItalic">Azospirillum</span> spp&#46; and others&#44; is beneficial for plant growth promotion and the control of fungal diseases&#46; Based on these qualities &#40;i&#46;e&#46; growth promotion and biocontrol activity&#41; along with their eco-friendly behavior&#44; microbial inoculants are potential candidates for a vast market share around the globe with 15&#37; growth rate per year<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">28</span></a>&#46; However&#44; a number of biocontrol agents perform quite well in the laboratory and greenhouse conditions but failed to perform in the field<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">9</span></a>&#46; The major limitation for commercialization is the development of an effective bacterial formulation with high survival and rhizosphere colonization rate&#46; Generally&#44; PGPRs are inoculated directly to plant material without a suitable carrier or in inappropriate quantities that are insignificant under field conditions for rhizosphere colonization&#46; In addition&#44; the fumigation of soils with broad spectrum biocidal chemicals affect soil&#8211;microbial interaction&#44; causing a lower rate of rhizosphere colonization&#46; The issue can be resolved by a comprehension of the ecological parameters that influence biocontrol agents&#46; To develop the final bioproduct&#44; the selection criteria of the optimal strategy will depend on the balance between stability&#44; efficacy&#44; economic feasibility&#44; and ease of use&#46; Additionally&#44; the transition of PGPR from laboratory to farmers requires an extensive research about survival and mass production of these strains in cost-effective carrier materials&#46; Our data suggested that <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> and <span class="elsevierStyleItalic">B&#46; subtilis</span> can easily survive in a cost effective self-prepared media &#40;containing molasses as carbon source&#41; up to 3 months with a significant population rate&#46;</p></span><span id="sec0140" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0165">Conclusion</span><p id="par0195" class="elsevierStylePara elsevierViewall">The purpose of this study was to characterize the indigenous population of biocontrol bacteria that have broad spectrum fungicidal activity to be used as biofungicides for commercial purposes&#46; It is concluded that the bacterial isolates mentioned in the study not only had broad spectrum fungicidal activity but also additional properties of plant growth-promoting activity&#46; The mentioned isolates had good survival rate in the molasses-based medium&#44; which is a cost-effective nutrient medium compared to the commercial media available in the market&#46; Therefore&#44; the mentioned isolates could be used for commercial purposes to control phytopathogens on a cost-effective nutrient medium&#46;</p></span><span id="sec0145" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0170">Funding</span><p id="par0200" class="elsevierStylePara elsevierViewall">The authors wish to thank the <span class="elsevierStyleGrantSponsor" id="gs1">Higher Education Commission&#44; Pakistan &#40;HEC&#41;</span> for the financial support for this study in the form of research grant <span class="elsevierStyleGrantNumber" refid="gs1">HEC-TDF02-13</span>&#46;</p></span><span id="sec0150" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0175">Conflict of interest</span><p id="par0205" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Materials and methods"
          "secciones" => array:5 [
            0 => array:2 [
              "identificador" => "sec0015"
              "titulo" => "Isolation of bacteria in pure culture"
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            1 => array:3 [
              "identificador" => "sec0020"
              "titulo" => "Preliminary screening of bacterial isolates for antifungal activity"
              "secciones" => array:1 [
                0 => array:2 [
                  "identificador" => "sec0025"
                  "titulo" => "Qualitative and quantitative assessment for antagonistic activity in vitro"
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              "titulo" => "Molecular identification and phylogenetic analysis"
              "secciones" => array:3 [
                0 => array:2 [
                  "identificador" => "sec0035"
                  "titulo" => "DNA extraction"
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                1 => array:2 [
                  "identificador" => "sec0040"
                  "titulo" => "16S rRNA gene amplification"
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                  "titulo" => "Similarity analysis and dendrogram construction"
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              "identificador" => "sec0050"
              "titulo" => "Evaluation of biocontrol bacteria for plant growth promoting traits"
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                0 => array:2 [
                  "identificador" => "sec0055"
                  "titulo" => "Phosphate solubilization assay"
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                  "titulo" => "Indole-3-acetic acid assay"
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                2 => array:2 [
                  "identificador" => "sec0065"
                  "titulo" => "Detection of cellulolytic activity"
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                  "identificador" => "sec0070"
                  "titulo" => "Hydrogen cyanide production"
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                4 => array:2 [
                  "identificador" => "sec0075"
                  "titulo" => "Siderophore production"
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                  "identificador" => "sec0080"
                  "titulo" => "Molecular volatile organic compound production assay"
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              "identificador" => "sec0085"
              "titulo" => "Survival study of bacterial isolates in different liquid carrier material"
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          "titulo" => "Results"
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              "titulo" => "Isolation and screening of bacteria with antifungal activity"
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            1 => array:2 [
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              "titulo" => "Identification&#44; characterization and phylogenetic analysis"
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              "titulo" => "Screening for PGPR traits"
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                  "identificador" => "sec0110"
                  "titulo" => "IAA production and phosphate solubilization"
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                  "identificador" => "sec0115"
                  "titulo" => "Cellulolytic activity"
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                2 => array:2 [
                  "identificador" => "sec0120"
                  "titulo" => "Production of HCN and siderophores"
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                3 => array:2 [
                  "identificador" => "sec0125"
                  "titulo" => "Volatile organic compound production"
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              "titulo" => "Survival study"
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          "titulo" => "Discussion"
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    "fechaRecibido" => "2020-10-24"
    "fechaAceptado" => "2021-10-03"
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    "highlights" => array:2 [
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      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">Bacteria had broad-spectrum activity against phytopathogenic fungi &#40;&#62;50&#37; inhibition&#41;&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Selected isolates were identified with molecular methods and analyzed for plant growth-promoting activities&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">The selected isolates had a good survival rate in a cost-effective medium&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">&#8226;</span><p id="par0020" class="elsevierStylePara elsevierViewall">Assessed medium can be used for commercial fermentation of bio-control agents&#46;</p></li></ul></p></span>"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">The current study intended to isolate&#44; characterize and identify biocontrol bacteria possessing broad-spectrum antifungal activity from the phyllosphere of different crops including maize&#44; wheat and potato and to assess their growth-promoting activity&#46; In this study 14&#47;113 biocontrol bacteria showed antifungal activity&#46; Bacterial isolates M11 and M33 from maize out of 113 were re-selected on the basis of their strong &#40;more than 50&#37;&#41; broad spectrum antifungal activity after their assessment against four economically important phytopathogenic fungi including <span class="elsevierStyleItalic">Alternaria alternata</span>&#44; <span class="elsevierStyleItalic">Rhizoctonia solani</span>&#44; <span class="elsevierStyleItalic">Fusarium oxysporum</span> and <span class="elsevierStyleItalic">Fusarium verticillioides</span>&#46; The isolates were further assessed for plant growth promoting traits&#44; i&#46;e&#46;&#44; indole-3-acetic acid production&#44; phosphate solubilization&#44; production of cellulase&#44; microbial volatile compounds&#44; hydrogen cyanide and siderophores&#46; All fourteen isolates showed positive results for the production of indole-3-acetic acid hormone and cellulase enzyme&#44; 10 isolates were positive for hydrogen cyanide production&#59; siderophores production was observed in 7 isolates while 5 isolates showed ability to solubilize inorganic phosphate&#46; Microbial volatile compounds were only synthesized by M11 and M33&#44; which were identified as <span class="elsevierStyleItalic">Bacillus amyloliquefaciens</span> and <span class="elsevierStyleItalic">Bacillus subtilis</span> respectively by 16S rRNA gene sequencing&#46; The survival study revealed that biocontrol bacteria <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> and <span class="elsevierStyleItalic">B&#46; subtilis</span> have the ability to survive in cost effective molasses containing carrier material up to a three-month period&#46;</p></span>"
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        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Este estudio tuvo como objetivo aislar&#44; caracterizar e identificar bacterias de control biol&#243;gico que poseen actividad antif&#250;ngica de amplio espectro de la filosfera de diferentes cultivos&#44; incluidos el ma&#237;z&#44; el trigo y la papa&#44; as&#237; como evaluar su actividad en la promoci&#243;n del crecimiento&#46; En este estudio&#44; 14&#47;113 bacterias de control biol&#243;gico mostraron actividad antif&#250;ngica&#46; Los aislamientos bacterianos M11 y M33 &#40;de ma&#237;z&#41;&#44; del total de 113&#44; fueron reseleccionados debido a su fuerte actividad antif&#250;ngica de amplio espectro &#40;m&#225;s del 50&#37;&#41; despu&#233;s de su evaluaci&#243;n contra cuatro hongos fitopat&#243;genos que afectan cultivos de alta importancia econ&#243;mica&#44; entre ellos&#44; <span class="elsevierStyleItalic">Alternaria alternata</span>&#44; <span class="elsevierStyleItalic">Rhizoctonia solani</span>&#44; <span class="elsevierStyleItalic">Fusarium oxysporum</span> y <span class="elsevierStyleItalic">Fusarium verticillioides</span>&#46; Los aislamientos se evaluaron&#44; adicionalmente&#44; para determinar los rasgos que promueven el crecimiento de las plantas&#44; es decir&#44; producci&#243;n de &#225;cido indolac&#233;tico&#44; solubilizaci&#243;n de fosfato&#44; producci&#243;n de celulasa&#44; compuestos org&#225;nicos vol&#225;tiles microbianos&#44; cianuro de hidr&#243;geno y sider&#243;foros&#46; Las 14 cepas aisladas mostraron resultados positivos para la producci&#243;n de la hormona &#225;cido indolac&#233;tico y la enzima celulasa&#59; 10 cepas fueron positivas para la producci&#243;n de cianuro de hidr&#243;geno&#46; Adem&#225;s&#44; se observ&#243; producci&#243;n de sider&#243;foros en el caso de 7 cepas&#44; mientras que 5 pudieron solubilizar fosfato inorg&#225;nico&#46; Los compuestos org&#225;nicos vol&#225;tiles microbianos solo fueron sintetizados por los aislamientos M11 y M33&#44; que fueron identificados como <span class="elsevierStyleItalic">Bacillus amyloliquefaciens</span> y <span class="elsevierStyleItalic">Bacillus subtilis</span>&#44; respectivamente&#44; mediante secuenciaci&#243;n del gen ARNr 16S&#46; El estudio de supervivencia mostr&#243; que las bacterias de control biol&#243;gico&#44; es decir&#44; <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> y <span class="elsevierStyleItalic">B&#46; subtilis&#44;</span> tienen la capacidad de sobrevivir sobre un sustrato a base de melasa&#44; por un per&#237;odo de tres meses&#46;</p></span>"
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            "apendice" => "<p id="par0215" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
            "etiqueta" => "Appendix A"
            "titulo" => "Supplementary data"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Antagonistic activity of bacterial isolates &#40;M11 and M33&#41; against &#40;a&#41; <span class="elsevierStyleItalic">A&#46; alternata</span>&#44; &#40;b&#41; <span class="elsevierStyleItalic">R&#46; solani</span>&#44; &#40;c&#41; <span class="elsevierStyleItalic">F&#46; oxysporum</span> and &#40;d&#41; <span class="elsevierStyleItalic">F&#46; verticillioides</span>&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Graphical representation of the&#37; suppression of growth of phytopathogenic fungi under study using biocontrol bacteria&#46; The <span class="elsevierStyleItalic">y</span>-axis shows the inhibition percentages&#44; while the <span class="elsevierStyleItalic">x</span>-axis represents the bacterial isolates&#46; The bars show the standard error mean computed by using Microsoft Excel&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Cladogram constructed by using ClustalW and MEGA 6&#46;4 software&#46; Node values show bootstrap support when neighbor-joining was done for 1000 resampled datasets&#46; The scale bar represents the nucleotide substitutions per 100 nucleotides&#46;</p>"
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Graphical representation of fungal dry mass reduction &#40;&#37;&#41; by VOCs produced by bacterial isolates &#40;M11 and M33&#41;&#46; The <span class="elsevierStyleItalic">y</span>-axis represents reduction percentages&#44; while the <span class="elsevierStyleItalic">x</span>-axis shows two selected bacterial isolates &#40;M11 and M33&#41;&#46; The bars show the standard error mean computed using Microsoft Excel&#46;</p>"
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Survival of biocontrol bacteria in molasses-based medium &#40;MBM&#41; compared to control&#44; where the <span class="elsevierStyleItalic">x</span>-axis represents the sampling days &#40;0&#8211;90 days&#41; and the <span class="elsevierStyleItalic">y</span>-axis shows the CFU count&#46; &#40;A&#41; <span class="elsevierStyleItalic">B&#46; amyloliquefaciens</span> &#40;M11&#41; survival in MBM compared to LB control medium&#59; &#40;B&#41; <span class="elsevierStyleItalic">B&#46; subtilis</span> &#40;M33&#41; in two different media&#44; LB medium &#40;control&#41; and molasses-based medium &#40;MBM&#41;&#46;</p>"
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      5 => array:8 [
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          "leyenda" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">IAA&#58; indole acetic acid&#59; PS&#58; phosphate solubilization&#59; Cel&#58; cellulase production&#59; HCN&#58; hydrogen cyanide&#59; Sid&#58; siderophores&#46; The &#40;&#43;&#47;&#8722;&#41; indicates positive and negative results respectively&#46;</p>"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2021.10.005

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Year/Month	Html	Pdf	Total

2024 November	3	0	3
2024 October	54	11	65
2024 September	56	6	62
2024 August	73	9	82
2024 July	67	14	81
2024 June	39	13	52
2024 May	59	30	89
2024 April	209	24	233
2024 March	60	11	71
2024 February	52	13	65
2024 January	71	13	84
2023 December	68	13	81
2023 November	101	19	120
2023 October	104	21	125
2023 September	87	13	100
2023 August	72	23	95
2023 July	100	18	118
2023 June	131	20	151
2023 May	176	30	206
2023 April	119	15	134
2023 March	53	24	77
2023 February	16	15	31
2023 January	10	7	17
2022 December	17	11	28
2022 November	26	17	43
2022 October	24	16	40
2022 September	14	30	44
2022 August	10	24	34
2022 July	10	10	20
2022 June	7	8	15
2022 May	8	9	17
2022 April	12	13	25
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2022 January	7	10	17

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