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Functional Analysis and Genome Mining Reveal High Potential of Biocontrol and Plant Growth Promotion in Nodule-Inhabiting Bacteria Within Paenibacillus polymyxa Complex.

ABSTRACT: Bacteria belonging to the genus Paenibacillus were frequently isolated from legume nodules. The nodule-inhabiting Paenibacillus as a resource of biocontrol and plant growth-promoting endophytes has rarely been explored. This study explored the nodule-inhabiting Paenibacillus' antifungal activities and biocontrol potentials against broad-spectrum important phytopathogenic fungi. We collected strains which were isolated from nodules of Robinia pseudoacacia, Dendrolobium triangulare, Ormosia semicastrata, Cicer arietinum, Acacia crassicarpa, or Acacia implexa and belong to P. peoriae, P. kribbensis, P. endophyticus, P. enshidis, P. puldeungensis, P. taichungensis, or closely related to P. kribbensis, or P. anseongense. These nodule-inhabiting Paenibacillus showed diverse antagonistic activities against five phytopathogenic fungi (Fusarium graminearum, Magnaporthe oryzae, Rhizoctonia solani, Sclerotinia sclerotiorum, and Botrytis cinerea). Six strains within the P. polymyxa complex showed broad-spectrum and potent activities against all the five pathogens, and produced multiple hydrolytic enzymes, siderophores, and lipopeptide fusaricidins. Fusaricidins are likely the key antimicrobials responsible for the broad-spectrum antifungal activities. The nodule-inhabiting strains within the P. polymyxa complex were able to epiphytically and endophytically colonize the non-host wheat plants, produce indole acetic acids (IAA), and dissolve calcium phosphate and calcium phytate. P. peoriae strains RP20, RP51, and RP62 could fix N₂. P. peoriae RP51 and Paenibacillus sp. RP31, which showed potent plant colonization and plant growth-promotion competence, effectively control fungal infection in planta. Genome mining revealed that all strains (n = 76) within the P. polymyxa complex contain ipdC gene encoding indole-3-pyruvate decarboxylase for biosynthesis of IAA, 96% (n = 73) contain the fus cluster for biosynthesis of fusaricidins, and 43% (n = 33) contain the nif cluster for nitrogen fixation. Together, our study highlights that endophytic strains within the P. polymyxa complex have a high probability to be effective biocontrol agents and biofertilizers and we propose an effective approach to screen strains within the P. polymyxa complex.

SUBMITTER: Ali MA

PROVIDER: S-EPMC7848036 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Functional Analysis and Genome Mining Reveal High Potential of Biocontrol and Plant Growth Promotion in Nodule-Inhabiting Bacteria Within Paenibacillus polymyxa Complex.

Ali Md Arshad MA Lou Yang Y Hafeez Rahila R Li Xuqing X Hossain Afsana A Xie Ting T Lin Li L Li Bin B Yin Yanni Y Yan Jianli J An Qianli Q

Frontiers in microbiology 20210118

Bacteria belonging to the genus Paenibacillus were frequently isolated from legume nodules. The nodule-inhabiting Paenibacillus as a resource of biocontrol and plant growth-promoting endophytes has rarely been explored. This study explored the nodule-inhabiting Paenibacillus' antifungal activities and biocontrol potentials against broad-spectrum important phytopathogenic fungi. We collected strains which were isolated from nodules of Robinia pseudoacacia, Dendrolob ...[more]

PMID: 33537018

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Project description:Paenibacillus polymyxa (formerly known as Bacillus polymyxa) has been extensively studied for agricultural applications as a plant-growth-promoting rhizobacterium and is also an important biocontrol agent. Our team has developed the P. polymyxa strain HY96-2 from the tomato rhizosphere as the first microbial biopesticide based on P. polymyxa for controlling plant diseases around the world, leading to the commercialization of this microbial biopesticide in China. However, further research is essential for understanding its precise biocontrol mechanisms. In this paper, we report the complete genome sequence of HY96-2 and the results of a comparative genomic analysis between different P. polymyxa strains. The complete genome size of HY96-2 was found to be 5.75 Mb and 5207 coding sequences were predicted. HY96-2 was compared with seven other P. polymyxa strains for which complete genome sequences have been published, using phylogenetic tree, pan-genome, and nucleic acid co-linearity analysis. In addition, the genes and gene clusters involved in biofilm formation, antibiotic synthesis, and systemic resistance inducer production were compared between strain HY96-2 and two other strains, namely, SC2 and E681. The results revealed that all three of the P. polymyxa strains have the ability to control plant diseases via the mechanisms of colonization (biofilm formation), antagonism (antibiotic production), and induced resistance (systemic resistance inducer production). However, the variation of the corresponding genes or gene clusters between the three strains may lead to different antimicrobial spectra and biocontrol efficacies. Two possible pathways of biofilm formation in P. polymyxa were reported for the first time after searching the KEGG database. This study provides a scientific basis for the further optimization of the field applications and quality standards of industrial microbial biopesticides based on HY96-2. It may also serve as a reference for studying the differences in antimicrobial spectra and biocontrol capability between different biocontrol agents.

Project description:Paenibacillus polymyxa is a plant growth-promoting rhizobacterium that has immense potential to be used as an environmentally friendly replacement of chemical fertilizers and pesticides. In the present study, Paenibacillus polymyxa SK1 was isolated from bulbs of Lilium lancifolium. The isolated endophytic strain showed antifungal activities against important plant pathogens like Botryosphaeria dothidea, Fusarium oxysporum, Botrytis cinerea, and Fusarium fujikuroi. The highest percentage of growth inhibition, i.e., 66.67?±?2.23%, was observed for SK1 against Botryosphaeria dothidea followed by 61.19?±?3.12%, 60.71?±?3.53%, and 55.54?±?2.89% against Botrytis cinerea, Fusarium fujikuroi, and Fusarium oxysporum, respectively. The metabolite profiling of ethyl acetate fraction was assessed through the UHPLC-LTQ-IT-MS/MS analysis, and putative identification was done with the aid of the GNPS molecular networking workflow. A total of 29 compounds were putatively identified which included dipeptides, tripeptides, cyclopeptides (cyclo-(Leu-Leu), cyclo(Pro-Phe)), 2-heptyl-3-hydroxy 4-quinolone, 6-oxocativic acid, anhydrobrazilic acid, 1-(5-methoxy-1H-indol-3-yl)-2-piperidin-1-ylethane-1,2-dione, octadecenoic acid, pyochelin, 15-hydroxy-5Z,8Z,11Z, 13E-eicosatetraenoic acid, (Z)-7-[(2R,3S)-3-[(2Z,5E)-Undeca-2,5-dienyl]oxiran-2-yl]hept-5-enoic acid, arginylasparagine, cholic acid, sphinganine, elaidic acid, gossypin, L-carnosine, tetrodotoxin, and ursodiol. The high antifungal activity of SK1 might be attributed to the presence of these bioactive compounds. The isolated strain SK1 showed plant growth-promoting traits such as the production of organic acids, ACC deaminase, indole-3-acetic acid (IAA), siderophores, nitrogen fixation, and phosphate solubilization. IAA production was strongly correlated with the application of exogenous tryptophan concentrations in the medium. Furthermore, inoculation of SK1 enhanced plant growth of two Lilium varieties, Tresor and White Heaven, under greenhouse condition. In the light of these findings, the P. polymyxa SK1 may be utilized as a source of plant growth promotion and disease control in sustainable agriculture.

Dataset Information

Functional Analysis and Genome Mining Reveal High Potential of Biocontrol and Plant Growth Promotion in Nodule-Inhabiting Bacteria Within Paenibacillus polymyxa Complex.

Publications

Functional Analysis and Genome Mining Reveal High Potential of Biocontrol and Plant Growth Promotion in Nodule-Inhabiting Bacteria Within <i>Paenibacillus polymyxa</i> Complex.

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