Publications by authors named "Xuewen Gao"

55 Publications

Melatonin and Its Homologs Induce Immune Responses Receptors trP47363-trP13076 in .

Front Plant Sci 2021 30;12:691835. Epub 2021 Jun 30.

Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Department of Plant Pathology, College of Plant Protection, Ministry of Education, Nanjing Agricultural University, Nanjing, China.

Melatonin (N-acetyl-5-methoxytryptamine), a naturally occurring small molecule, can protect plants against abiotic stress after exogenous treatmenting with it. It is not known if melatonin homologs, such as 5-methoxytryptamine and 5-methoxyindole, that are easy and more cost-effective to synthesize can stimulate the plant immune system in the same manner as melatonin. In the present study, we assessed the biological activity of the melatonin homologs, 5-methoxytryptamin and 5-methoxyindole. The results showed that melatonin and its homologs all induced disease resistance against in plants. The application of all three compounds also induced stomatal closure and the production of reactive oxygen species. Gene expression analysis indicated that the expression of genes involved in hydrogen peroxide (HO), nitric oxide (NO) production, and salicylic acid (SA) biosynthesis was significantly upregulated by all three compounds. Four homologs of the melatonin receptors were identified by blasting search with the phytomelatonin receptor in . Molecular docking studies were also used to identify four putative melatonin receptors in . Further experimentation revealed that silencing of the melatonin receptors trP47363 and trP13076 in compromised the induction of stomatal closure, gene expression and SA accumulation by all three compounds. Collectively, our data indicate that the induction of defense responses in by melatonin, 5-methoxytryptamine, and 5-methoxyindole involves the melatonin receptors trP47363 and trP13076.
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http://dx.doi.org/10.3389/fpls.2021.691835DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8278317PMC
June 2021

Discovery and preliminary mechanism of 1-carbamoyl β-carbolines as new antifungal candidates.

Eur J Med Chem 2021 Oct 2;222:113563. Epub 2021 Jun 2.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China. Electronic address:

Natural β-carboline alkaloids are ideal models for the discovery of pharmaceutically important entities. Various 1-substituted β-carbolines were synthesized from commercially inexpensive tryptophan and demonstrated significant in vitro antifungal activity against G. graminis. Significantly, compound 4m (EC = 0.45 μM) with carboxamide at 1-position displayed the best efficacy and nearly 20 folds enhancement in antifungal potential compared to Silthiopham (EC = 8.95 μM). Moreover, compounds 6, 7, and 4i exhibited excellent in vitro antifungal activities and in vivo protective and curative activities against B. cinerea and F. graminearum. Preliminary mechanism studies revealed that compound 4m caused reactive oxygen species accumulation, cell membrane destruction, and deregulation of histone acetylation. These findings indicated that 1-carbamoyl β-carboline can be selected as a promising model for the discovery of novel and broad-spectrum fungicide candidates.
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http://dx.doi.org/10.1016/j.ejmech.2021.113563DOI Listing
October 2021

Nematicidal Volatiles from GBSC56 Promote Growth and Stimulate Induced Systemic Resistance in Tomato against .

Int J Mol Sci 2021 May 10;22(9). Epub 2021 May 10.

Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.

volatiles to control plant nematodes is a topic of great interest among researchers due to its safe and environmentally friendly nature. strain GBSC56 isolated from the Tibet region of China showed high nematicidal activity against , with 90% mortality as compared with control in a partition plate experiment. Pure volatiles produced by GBSC56 were identified through gas chromatography and mass spectrometry (GC-MS). Among 10 volatile organic compounds (VOCs), 3 volatiles, i.e., dimethyl disulfide (DMDS), methyl isovalerate (MIV), and 2-undecanone (2-UD) showed strong nematicidal activity with a mortality rate of 87%, 83%, and 80%, respectively, against . The VOCs induced severe oxidative stress in nematodes, which caused rapid death. Moreover, in the presence of volatiles, the activity of antioxidant enzymes, i.e., SOD, CAT, POD, and APX, was observed to be enhanced in -infested roots, which might reduce the adverse effect of oxidative stress-induced after infection. Moreover, genes responsible for plant growth promotion , , and showed an upsurge in expression, while was downregulated in infested plants. Furthermore, the defense-related genes (, , and ) in infested tomato plants were upregulated after treatment with MIV and 2-UD. These findings suggest that GBSC56 possesses excellent biocontrol potential against . Furthermore, the study provides new insight into the mechanism by which GBSC56 nematicidal volatiles regulate antioxidant enzymes, the key genes involved in plant growth promotion, and the defense mechanism -infested tomato plants use to efficiently manage root-knot disease.
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http://dx.doi.org/10.3390/ijms22095049DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8126219PMC
May 2021

The Gene of BL21(DE3) is Associated with Nematicidal Activity against the Root-Knot Nematode .

Pathogens 2021 Feb 18;10(2). Epub 2021 Feb 18.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, 1 Weigang Road, Nanjing 210095, Jiangsu, China.

Biological nematicides have been widely used to lower the losses generated by phytoparasitic nematodes. The purpose of this study was to evaluate the nematicidal effects of BL21(DE3) against and to identify nematicide-related genes. Culture filtrates of BL21(DE3) caused juvenile mortality and inhibited egg hatching in a dose-dependent manner. In the greenhouse, treatment of tomato seedlings with BL21(DE3) culture filtrates at 50 and 100% concentrations not only reduced the amount of egg masses and galls, but improved plant root and shoot fresh weight. Culture filtrate analysis indicated that the nematicidal active ingredients of strain BL21(DE3) were non-proteinaceous, heat and cold resistant, sensitive to pH and volatile. To identify the genes associated with nematicidal activity, a BL21(DE3) library of 5000 mutants was produced using Tn5 transposase insertion. The culture filtrate of the MB12 mutant showed no nematicidal activity after 72 h of treatment and thermal asymmetrical interlaced PCR demonstrated that the gene was disrupted. Nematicidal activity was restored when the pH of the MB12 culture filtrate was adjusted to the original pH value (4.15) or following MB12 complementation with the gene, confirming a role for in mediating pH value and nematicidal activity. The outcomes of this pilot study indicate that BL21(DE3) is a potential microorganism for the continuable biological control of root-knot nematode in tomato and that affects the nematicidal activity of BL21(DE3) by modulating the pH environment.
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http://dx.doi.org/10.3390/pathogens10020222DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7923116PMC
February 2021

Exploring the pathogenic function of Pantoea ananatis endogenous plasmid by an efficient and simple plasmid elimination strategy.

Microbiol Res 2021 May 28;246:126710. Epub 2021 Jan 28.

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Education, Nanjing 210095, China. Electronic address:

The bacterium Pantoea ananatis is associated with devastating plant diseases that cause serious economic losses. Strain DZ-12 was previously isolated from maize brown rot leaves in Hebei Province, China and its genome sequencing revealed that it belongs to P. ananatis. It contains a large, endogenous plasmid, pDZ-12. Different studies have shown that virulence determinants are frequently carried on plasmids. To determine whether pDZ-12 from P. ananatis has any effect on pathogenicity, the plasmid was eliminated by substituting its native replication genes with temperature-sensitive replication genes. The resulting temperature-sensitive plasmid could be cured by growing cells at high temperature (37℃). Loss of pDZ-12 from P. ananatis DZ-12 led to a decreased disease severity in maize plants suggesting that the endogenous plasmid is important for pathogenesis. Loss of pDZ-12 also affected the ability of the bacterium to form biofilms. The study provides the first evidence that the endogenous plasmid of P. ananatis DZ-12 is important for pathogenesis in maize plants and carries genes involved in biofilm formation. This study also presents the first report on curing a plasmid from P. ananatis.
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http://dx.doi.org/10.1016/j.micres.2021.126710DOI Listing
May 2021

The "pseudo-pathogenic" effect of plant growth-promoting Bacilli on starchy plant storage organs is due to their α-amylase activity which is stimulating endogenous opportunistic pathogens.

Appl Microbiol Biotechnol 2020 Mar 30;104(6):2701-2714. Epub 2020 Jan 30.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Education, Nanjing, China.

Many representatives of the Bacillus subtilis species complex are known as plant growth-promoting rhizobacteria (PGPR) and are widely used in agriculture as biofertilizers and biocontrol agents. Two bacterial strains, "Korea isolate" and ZL918, taxonomically classified as being Bacillus amyloliquefaciens, isolated from disease-damaged plant organs, were alleged to cause bacterial rot in starchy storage plant organs. The aim of this study was to elucidate whether these findings have consequences for the general use of beneficial Bacilli in agriculture. Whole genome sequencing revealed that the pathogenic ZL918 was a representative of Bacillus velezensis. B. velezensis FZB42 and other representatives of the B. subtilis species complex caused the same symptoms of bacterial rot only when injected inside of potato tubers and onion bulbs, but not when inoculated onto the surface of the storage organs. It seemed that the pathogenic effect was due to starch hydrolyzing activity that likely stimulates propagation of endophytic bacteria inside of starchy tissues. After removing the inherent microbiota via Co γ-ray irradiation, the storage organs inoculated by either FZB42 or purified α-amylase did not develop rot symptoms. Two opportunistic pathogens, Pantoea ananatis and Pantoea agglomerans, isolated from the rotted area, were shown to cause bacterial rot in x-ray treated potato tuber and onion starchy tissues when the proteobacteria were applied in high concentration. This suggests that opportunistic pathogenic bacteria residing inside of the starchy storage organ are the causal agents of bacterial soft rot disease in potato tubers and other starchy plant storage organs.
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http://dx.doi.org/10.1007/s00253-020-10367-8DOI Listing
March 2020

Zn(II) suppresses biofilm formation in Bacillus amyloliquefaciens by inactivation of the Mn(II) uptake.

Environ Microbiol 2020 04 25;22(4):1547-1558. Epub 2019 Nov 25.

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Education, Nanjing, 210095, China.

Biofilms are architecturally complex communities of microbial cells held together by a self-produced extracellular matrix. Considerable research has focused on the environmental signals that trigger or inhibit biofilm formation by affecting cellular signalling pathways; however, response to soil cues in plant-associated Bacillus has remained largely unaddressed. Therefore, we aimed to investigate the effect of Zn(II) ions in biofilm formation of Bacillus amyloliquefaciens FZB42. We demonstrated that the biofilm formation of B. amyloliquefaciens FZB42 was abolished by Zn(II) at non-deleterious concentrations. Moreover, Zn(II) blocked matrix exopolysaccharide and TasA accumulations. Furthermore, the presence of Zn(II) suppressed expression of the response regulator Spo0F but not of sensor histidine kinases KinA-D. Suppression of phosphorelay by excess Zn interferes with sinI induction under biofilm-inducing conditions, leading to repression of transcription of operons epsA-O and tapA-sigW-tasA. Addition of Zn(II) decreased the intracellular Mn(II) level by competing for binding to the solute-binding protein MntA during Mn(II) uptake. These results suggest that the metal ion Zn(II) has a negative effect on biofilm formation in the plant growth promoting and biocontrol bacterium B. amyloliquefaciens FZB42.
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http://dx.doi.org/10.1111/1462-2920.14859DOI Listing
April 2020

Suppression of by the Induction of Systemic Resistance and Regulation of Antioxidant Pathways in Tomato Using Fengycin Produced by FZB42.

Biomolecules 2019 10 16;9(10). Epub 2019 Oct 16.

College of Plant Protection, Department of Plant Pathology, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Agriculture, Nanjing 210095, China.

Lipopeptides from species exhibit promising biological control activity against plant pathogens. This study aimed to explore the potential of purified fengycin to induce systemic resistance in tomato against . FZB42, its mutant AK1S, and their corresponding metabolites showed in vitro inhibition of mycelium. Fengycin derived from an AK1S mutant was purified and identified through HPLC and MALDI-TOF-MS, respectively. Scanning electron microscopy (SEM) and transmission electron microscopy (TEM) revealed structural deformities in the fungal mycelium. Moreover, fengycin induced the accumulation of reactive oxygen species (ROS) in mycelium and downregulated the expression of ROS-scavenging genes viz., superoxide dismutase (), peroxidase (), and catalase () compared to the untreated control. Furthermore, the lesion size was dramatically reduced in fengycin-treated tomato plants compared to plants infected with only in a greenhouse experiment. Additionally, the transcriptional regulation of defense-related genes , , , , and showed the highest upsurge in expression at 48 h post-inoculation (hpi). However, their expression was subsequently decreased at 96 hpi in fengycin + treatment compared to the plants treated with fengycin only. Conversely, the expression of increased in a linear manner up to 96 hpi.
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http://dx.doi.org/10.3390/biom9100613DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6843208PMC
October 2019

Genetic Screening and Expression Analysis of Psychrophilic spp. Reveal Their Potential to Alleviate Cold Stress and Modulate Phytohormones in Wheat.

Microorganisms 2019 Sep 10;7(9). Epub 2019 Sep 10.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing 210095, China.

Abiotic stress in plants pose a major threat to cereal crop production worldwide and cold stress is also notorious for causing a decrease in plant growth and yield in wheat. The present study was designed to alleviate cold stress on plants by inoculating psychrophilic PGPR bacteria belonging to Bacillus genera isolated from extreme rhizospheric environments of Qinghai-Tibetan plateau. The genetic screening of psychrophilic spp. CJCL2, RJGP41 and temperate FZB42 revealed presence of genetic features corresponding to cold stress response, membrane transport, signal transduction and osmotic regulation. Subsequently, the time frame study for the expression of genes involved in these pathways was also significantly higher in psychrophilic strains as analyzed through qPCR analysis at 4 ℃. The inoculated cold tolerant Bacillus strains also aided in inducing stress response in wheat by regulating abscisic acid, lipid peroxidation and proline accumulation pathways in a beneficial manner. Moreover, during comparative analysis of growth promotion in wheat all three Bacillus strains showed significant results at 25 ℃. Whereas, psychrophilic Bacillus strains CJCL2 and RJGP41 were able to positively regulate the expression of phytohormones leading to significant improvement in plant growth under cold stress.
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http://dx.doi.org/10.3390/microorganisms7090337DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6780275PMC
September 2019

Transcriptional Profiling of Diffusible Lipopeptides and Fungal Virulence Genes During EZ1509-Mediated Suppression of .

Phytopathology 2020 Feb 13;110(2):317-326. Epub 2019 Dec 13.

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Agriculture, Nanjing 210095, China.

is a devastating necrotrophic pathogen that infects multiple crops, and its control is an unremitting challenge. In this work, we attempted to gain insights into the pivotal role of lipopeptides (LPs) in the antifungal activity of EZ1509. In a comparative study involving five strains, EZ1509 harboring four LPs biosynthetic genes (viz. surfactin, iturin, fengycin, and bacilysin) exhibited promising antifungal activity against in a dual-culture assay. Our data demonstrated a remarkable upsurge in LPs biosynthetic gene expression through quantitative reverse transcription PCR during in vitro interaction assay with . Maximum upregulation in LPs biosynthetic genes was observed on the second and third days of in vitro interaction, with iturin and fengycin being the highly expressed genes. Subsequently, Matrix-assisted laser desorption/ionization-time of flight-mass spectrometry analysis confirmed the presence of LPs in the inhibition zone. Scanning electron microscope analysis showed disintegration, shrinkage, plasmolysis, and breakdown of fungal hyphae. During in planta evaluation, previously challenged with EZ1509 showed significant suppression in pathogenicity on detached leaves of tobacco and rapeseed. The oxalic acid synthesis was also significantly reduced in previously confronted with antagonistic bacterium. The expression of major virulence genes of , including endopolygalacturonase-3, oxalic acid hydrolase, and endopolygalacturonase-6, was significantly downregulated during in vitro confrontation with EZ1509.
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http://dx.doi.org/10.1094/PHYTO-05-19-0156-RDOI Listing
February 2020

Corrigendum: FZB42 in 2018: The Gram-Positive Model Strain for Plant Growth Promotion and Biocontrol.

Front Microbiol 2019 11;10:1279. Epub 2019 Jun 11.

Institut für Biologie, Humboldt Universität Berlin, Berlin, Germany.

[This corrects the article DOI: 10.3389/fmicb.2018.02491.].
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http://dx.doi.org/10.3389/fmicb.2019.01279DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580152PMC
June 2019

Cold-adapted Bacilli isolated from the Qinghai-Tibetan Plateau are able to promote plant growth in extreme environments.

Environ Microbiol 2019 Jun 24. Epub 2019 Jun 24.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, People's Republic of China.

Nearly 1400 Bacillus strains growing in the plant rhizosphere were sampled from different sites on the Qinghai-Tibetan Plateau. Forty-five of the isolates, selected due to their biocontrol activity, were genome-sequenced and their taxonomic identification revealed that they were representatives of the Bacillus subtilis species complex (20) and the Bacillus cereus group (9). Majority of the remaining strains were found closely related to Bacillus pumilus, but their average nucleotide identity based on BLAST and electronic DNA/DNA hybridization values excluded closer taxonomic identification. A total of 45 different gene clusters involved in synthesis of secondary metabolites were detected by mining the genomes of the 45 selected strains. Except eight mesophilic strains, the 37 remaining strains were found either cold-adapted or psychrophilic, able to propagate at 10°C and below (Bacillus wiedmannii NMSL88 and Bacillus sp. RJGP41). Pot experiments performed at 10°C with winter wheat seedlings revealed that cold-adapted representatives of B. pumilus, B. safensis and B. atrophaeus promoted growth of the seedlings under cold conditions, suggesting that these bacilli isolated from a cold environment are promising candidates for developing of bioformulations useful for application in sustainable agriculture under environmental conditions unfavourable for the mesophilic bacteria presently in use.
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http://dx.doi.org/10.1111/1462-2920.14722DOI Listing
June 2019

Fengycin Produced by FZB42 Inhibits Growth and Mycotoxins Biosynthesis.

Toxins (Basel) 2019 05 24;11(5). Epub 2019 May 24.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing 210095, China.

is a notorious pathogen that causes Fusarium head blight (FHB) in cereal crops. It produces secondary metabolites, such as deoxynivalenol, diminishing grain quality and leading to lesser crop yield. Many strategies have been developed to combat this pathogenic fungus; however, considering the lack of resistant cultivars and likelihood of environmental hazards upon using chemical pesticides, efforts have shifted toward the biocontrol of plant diseases, which is a sustainable and eco-friendly approach. Fengycin, derived from FZB42, was purified from the crude extract by HPLC and further analyzed by MALDI-TOF-MS. Its application resulted in structural deformations in fungal hyphae, as observed via scanning electron microscopy. In planta experiment revealed the ability of fengycin to suppress growth and highlighted its capacity to combat disease incidence. Fengycin significantly suppressed , and also reduced the deoxynivalenol (DON), 3-acetyldeoxynivalenol (3-ADON), 15-acetyldeoxynivalenol (15-ADON), and zearalenone (ZEN) production in infected grains. To conclude, we report that fengycin produced by FZB42 has potential as a biocontrol agent against and can also inhibit the mycotoxins produced by this fungus.
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http://dx.doi.org/10.3390/toxins11050295DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6563212PMC
May 2019

Mannan oligosaccharides trigger multiple defence responses in rice and tobacco as a novel danger-associated molecular pattern.

Mol Plant Pathol 2019 08 16;20(8):1067-1079. Epub 2019 May 16.

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, PR China.

Oligosaccharide, a typical danger-associated molecular pattern (DAMP), has been studied and applied as plant defence elicitor for several years. Here, we report a novel oligosaccharide, mannan oligosaccharide (MOS) with a degree of polymerization of 2-6, which was hydrolysed from locust bean gum by a newly reported enzyme, BpMan5. The MOS treatment can significantly enhance the generation of signalling molecules such as intracellular Ca and reactive oxygen species. Subsequent defence events like stomata closure and cell death were also caused by MOS, eventually leading to the prevention of pathogen invasion or expansion. Transcriptional expression assay indicated that MOS activated mitogen-activated protein kinase cascades in tobacco and rice via different cascading pathways. The expression levels of the defence-related genes PR-1a and LOX were both up-regulated after MOS treatment, suggesting that MOS may simultaneously activate salicylic acid and jasmonic acid-dependent signalling pathways. Furthermore, liquid chromatography-mass spectrometry analysis showed that MOS led to the accumulation of four phytoalexins (momilactone A, phytocassane A, phytocassane D, and phytocassane E) in rice seedling leaves within 12-24 h. Finally, MOS conferred resistance in rice and tobacco against Xanthomonas oryzae and Phytophthora nicotianae, respectively. Taken together, our results indicated that MOS, a novel DAMP, could trigger multiple defence responses to prime plant resistance and has a great potential as plant defence elicitor for the management of plant disease.
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http://dx.doi.org/10.1111/mpp.12811DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6640537PMC
August 2019

FZB42 in 2018: The Gram-Positive Model Strain for Plant Growth Promotion and Biocontrol.

Front Microbiol 2018 16;9:2491. Epub 2018 Oct 16.

Institut für Biologie, Humboldt Universität Berlin, Berlin, Germany.

FZB42, the model strain for Gram-positive plant-growth-promoting and biocontrol rhizobacteria, has been isolated in 1998 and sequenced in 2007. In order to celebrate these anniversaries, we summarize here the recent knowledge about FZB42. In last 20 years, more than 140 articles devoted to FZB42 have been published. At first, research was mainly focused on antimicrobial compounds, apparently responsible for biocontrol effects against plant pathogens, recent research is increasingly directed to expression of genes involved in bacteria-plant interaction, regulatory small RNAs (sRNAs), and on modification of enzymes involved in synthesis of antimicrobial compounds by processes such as acetylation and malonylation. Till now, 13 gene clusters involved in non-ribosomal and ribosomal synthesis of secondary metabolites with putative antimicrobial action have been identified within the genome of FZB42. These gene clusters cover around 10% of the whole genome. Antimicrobial compounds suppress not only growth of plant pathogenic bacteria and fungi, but could also stimulate induced systemic resistance (ISR) in plants. It has been found that besides secondary metabolites also volatile organic compounds are involved in the biocontrol effect exerted by FZB42 under biotic (plant pathogens) and abiotic stress conditions. In order to facilitate easy access to the genomic data, we have established an integrating data bank 'AmyloWiki' containing accumulated information about the genes present in FZB42, available mutant strains, and other aspects of FZB42 research, which is structured similar as the famous SubtiWiki data bank.
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http://dx.doi.org/10.3389/fmicb.2018.02491DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6198173PMC
October 2018

Contribution of the cold shock protein CspA to virulence in Xanthomonas oryzae pv. oryzae.

Mol Plant Pathol 2019 03 16;20(3):382-391. Epub 2018 Nov 16.

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Education, Nanjing, 210095, China.

Xanthomonas oryzae pv. oryzae (Xoo) causes a damaging bacterial leaf blight disease in rice. Cold shock proteins (Csps) are highly conserved nucleic acid-binding proteins present in various bacterial genera, but relatively little is known about their functions in Xanthomonas. Herein, we identified four Csps (CspA-CspD) in the Xoo PXO99 strain. Deletion of cspA decreased cold adaptation and a few known pathogenic factors, including bacterial pathogenicity, biofilm formation and polysaccharide production. Furthermore, we performed transcriptomic and chromosome immunoprecipitation (ChIP) experiments to identify direct targets of CspA and to determine its DNA-binding sequence. Integrative data analysis revealed that CspA directly regulates two genes, PXO_RS11830 and PXO_RS01060, by binding to a conserved CCAAT sequence in the promoter region. We generated single-deletion mutants of each gene and the results indicate that both are responsible for Xanthomonas pathogenicity. In addition, quantitative real-time polymerase chain reaction and western blotting showed that CspA suppressed the expression of its direct targets. In summary, our study clarifies the characteristics of Csps in Xanthomonas and greatly advances our understanding of the mechanisms underlying the contribution of CspA to bacterial virulence.
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http://dx.doi.org/10.1111/mpp.12763DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6637868PMC
March 2019

Acetoin and 2,3-butanediol from Bacillus amyloliquefaciens induce stomatal closure in Arabidopsis thaliana and Nicotiana benthamiana.

J Exp Bot 2018 11;69(22):5625-5635

College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Disease and Pest Insects, Ministry of Education, Nanjing, China.

Plants live in close association with large communities of microbes, some of which are foliar pathogens that invade tissues, primarily via stomata on the leaf surface. Stomata are considered part of an integral, innate immunity system capable of efficiently preventing pathogens from entering the host plant. Although Bacillus, a typical plant growth-promoting rhizobacterium, is known to induce stomatal closure, the substances participating in this closure and the mechanism involved in its regulation remain poorly understood. Here, we screened a mutant library and conducted site-specific mutagenesis experiments in order to identify such substances. We found that acetoin and 2,3-butanediol from B. amyloliquefaciens FZB42 induced stomatal closure in Arabidopsis thaliana and Nicotiana benthamiana. These two components could function either via root absorption or volatilization to restrict stomatal apertures, but root absorption was more efficient. Both substances invoked the salicylic acid and abscisic acid signaling pathways to close the stomata and stimulated accumulation of hydrogen peroxide and nitric oxide. The results present comprehensive evidence of how soil rhizobacteria may affect plant stomata, in a way that reinforces the evolved mutualism between the two groups of organisms, and provide potential alternative avenues of research towards reducing the incidence of disease in crops.
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http://dx.doi.org/10.1093/jxb/ery326DOI Listing
November 2018

Volatile Compounds of Endophytic Bacillus spp. have Biocontrol Activity Against Sclerotinia sclerotiorum.

Phytopathology 2018 Dec 31;108(12):1373-1385. Epub 2018 Oct 31.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, PR China.

To develop an effective biological agent to control Sclerotinia sclerotiorum, three endophytic Bacillus spp. strains with high antagonistic activity were isolated from maize seed and characterized. In vitro assays revealed that the Bacillus endophytes could produce volatile organic compounds (VOC) that reduced sclerotial production and inhibited mycelial growth of S. sclerotiorum. Gas chromatography-mass spectrometry revealed that the selected strains produced 16 detectable VOC. Eight of the produced VOC exhibited negative effects on S. sclerotiorum, while a further four induced accumulation of reactive oxygen species in mycelial cells. A mixture of VOC produced by Bacillus velezensis VM11 caused morphological changes in the ultrastructure and organelle membranes of S. sclerotiorum mycelial cells. The bromophenol blue assay revealed a yellow color of untreated fungal mycelium, which grew faster and deeper from 24 to 72 h postinoculation, as an indication of reduced pH. The potassium permanganate (KMnO) titration assay showed that the rate of oxalic acid accumulation was higher in minimal salt liquid medium cultures inoculated with untreated fungal plugs compared with the Bacillus VOC-treated ones. Interestingly, biological control assays using host-plant leaves challenged with treated fungal mycelial plugs produced reduced lesions compared with the control. These findings provide new viable possibilities of controlling diseases caused by S. sclerotiorum using VOC produced by Bacillus endophytes.
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http://dx.doi.org/10.1094/PHYTO-04-18-0118-RDOI Listing
December 2018

Stomatal Closure and SA-, JA/ET-Signaling Pathways Are Essential for FZB42 to Restrict Leaf Disease Caused by in .

Front Microbiol 2018 27;9:847. Epub 2018 Apr 27.

College of Plant Protection, Nanjing Agricultural University, Nanjing, China.

FZB42 is a plant growth-promoting rhizobacterium that induces resistance to a broad spectrum of pathogens. This study analyzed the mechanism by which FZB42 restricts leaf disease caused by in . The oomycete foliar pathogen is able to reopen stomata which had been closed by the plant innate immune response to initiate penetration and infection. Here, we showed that root colonization by FZB42 restricted pathogen-mediated stomatal reopening in . Abscisic acid (ABA) and salicylic acid (SA)-regulated pathways mediated FZB42-induced stomatal closure after pathogen infection. Moreover, the defense-related genes , , and , involved in the SA and jasmonic acid (JA)/ethylene (ET) signaling pathways, respectively, were overexpressed, and levels of the hormones SA, JA, and ET increased in the leaves of FZB42-treated wild type plants. Disruption of one of these three pathways in plants increased susceptibility to the pathogen. These suggest that SA- and JA/ET-dependent signaling pathways were important in plant defenses against the pathogen. Our data thus explain a biocontrol mechanism of soil rhizobacteria in a plant.
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http://dx.doi.org/10.3389/fmicb.2018.00847DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5934478PMC
April 2018

Draft Genome Sequences of Plant-Associated Bacillus Strains Isolated from the Qinghai-Tibetan Plateau.

Genome Announc 2018 May 10;6(19). Epub 2018 May 10.

Department of Plant Pathology, College of Plant Protection, Nanjing Agriculture University, Nanjing, China

Here, we report the draft genome sequences of 45 plant-associated strains isolated from the Qinghai-Tibetan plateau. According to their genome sequences, 28 isolates were assigned to 10 species. Seventeen strains could not be assigned and are subjects of further research.
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http://dx.doi.org/10.1128/genomeA.00375-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5946045PMC
May 2018

Histone H3 lysine 9 methyltransferase FvDim5 regulates fungal development, pathogenicity and osmotic stress responses in Fusarium verticillioides.

FEMS Microbiol Lett 2017 Oct;364(19)

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Education, Nanjing 210095, China.

Histone methylation plays important biological roles in eukaryotic cells. Methylation of lysine 9 at histone H3 (H3K9me) is critical for regulating chromatin structure and gene transcription. Dim5 is a lysine histone methyltransferase (KHMTase) enzyme, which is responsible for the methylation of H3K9 in eukaryotes. In the current study, we identified a single ortholog of Neurospora crassa Dim5 in Fusarium verticillioides. In this study, we report that FvDim5 regulates the trimethylation of H3K9 (H3K9me3). The FvDIM5 deletion mutant (ΔFvDim5) showed significant defects in conidiation, perithecium production and fungal virulence. Unexpectedly, we found that deletion of FvDIM5 resulted in increased tolerance to osmotic stresses and upregulated FvHog1 phosphorylation. These results indicate the importance of FvDim5 for the regulation of fungal development, pathogenicity and osmotic stress responses in F. verticillioides.
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http://dx.doi.org/10.1093/femsle/fnx184DOI Listing
October 2017

FvSet2 regulates fungal growth, pathogenicity, and secondary metabolism in Fusarium verticillioides.

Fungal Genet Biol 2017 10 1;107:24-30. Epub 2017 Aug 1.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Ministry of Education, Nanjing, China.

Histone H3 lysine 36 methylation (H3K36me) is generally associated with activation of gene expression in most eukaryotic cells. However, the function of H3K36me in filamentous fungi is largely unknown. Set2 is the sole lysine histone methyltransferase (KHMTase) enzyme responsible for the methylation of H3K36 in Saccharomyces cerevisiae. In the current study, we identified a single ortholog of S. cerevisiae Set2 in Fusarium verticillioides. We report that FvSet2 is responsible for the trimethylation of H3K36 (H3K36me3). The FvSET2 deletion mutant (ΔFvSet2) showed significant defects in vegetative growth, FB biosynthesis, pigmentation, and fungal virulence. Furthermore, trimethylation of H3K36 was found to be important for active transcription of genes involved in FB and bikaverin biosyntheses. These data indicate that FvSet2 plays an important role in the regulation of secondary metabolism, vegetative growth and fungal virulence in F. verticillioides.
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http://dx.doi.org/10.1016/j.fgb.2017.07.007DOI Listing
October 2017

Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles.

BMC Plant Biol 2017 08 2;17(1):133. Epub 2017 Aug 2.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Weigang No.1, Nanjing, 210095, People's Republic of China.

Background: Microbial volatiles play an expedient role in the agricultural ecological system by enhancing plant growth and inducing systemic resistance against plant pathogens, without causing hazardous effects on the environment. To explore the effects of VOCs of Ralstonia solanacearum TBBS1 (Rs) on tobacco plant growth and on plant growth promoting efficiency of VOCs produced by Bacillus subtilis SYST2, experiments were conducted both in vitro and in planta.

Results: The VOCs produced by SYST2 significantly enhanced the plant growth and induced the systemic resistance (ISR) against wilt pathogen Rs in all experiments. The SYST2-VOCs significantly increased PPO and PAL activity and over-expressed the genes relating to expansin, wilt resistance, and plant defense while repressed the genes relating to ethylene production. More interestingly, VOCs produced by pathogen, Rs had no significant effect on plant growth; however, Rs-VOCs decreased the growth promoting potential of SYST2-VOCs when plants were exposed to VOCs produced by both SYST2 and Rs. The co-culture of SYST2 and Rs revealed that they inhibited the growth of each other; however, the inhibition of Rs by SYST2-VOCs appeared to be greater than that of SYST2 by Rs-VOCs.

Conclusion: Our findings provide new insights regarding the interaction among SYST2-VOCs, Rs-VOCs and plant, resulting in growth promotion and induced systemic resistance against the bacterial wilt pathogen Rs. This is the first report of the effect of VOCs produced by pathogenic microorganism on plant growth and on plant growth-promoting and systemic resistance-inducing potential of PGPR strain SYST2.
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http://dx.doi.org/10.1186/s12870-017-1083-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5541429PMC
August 2017

Bacillomycin D Produced by Bacillus amyloliquefaciens Is Involved in the Antagonistic Interaction with the Plant-Pathogenic Fungus Fusarium graminearum.

Appl Environ Microbiol 2017 10 15;83(19). Epub 2017 Sep 15.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, People's Republic of China.

(teleomorph: Ascomycota, Hypocreales, , ) is a destructive fungal pathogen that threatens the production and quality of wheat and barley worldwide. Controlling this toxin-producing pathogen is a significant challenge. In the present study, the commercially available strain (, , , ) FZB42 showed strong activity against The lipopeptide bacillomycin D, produced by FZB42, was shown to contribute to the antifungal activity. Purified bacillomycin D showed strong activity against , and its 50% effective concentration was determined to be approximately 30 μg/ml. Analyses using scanning and transmission electron microscopy revealed that bacillomycin D caused morphological changes in the plasma membranes and cell walls of hyphae and conidia. Fluorescence microscopy combined with different dyes showed that bacillomycin D induced the accumulation of reactive oxygen species and caused cell death in hyphae and conidia. secondary metabolism also responded to bacillomycin D challenge, by increasing the production of deoxynivalenol. Biological control experiments demonstrated that bacillomycin D exerted good control of on corn silks, wheat seedlings, and wheat heads. In response to bacillomycin D, genes involved in scavenging reactive oxygen species were downregulated, whereas genes involved in the synthesis of deoxynivalenol were upregulated. Phosphorylation of MGV1 and HOG1, the mitogen-activated protein kinases of , was increased in response to bacillomycin D. Taken together, these findings reveal the mechanism of the antifungal action of bacillomycin D. Biological control of plant disease caused by is desirable. FZB42 is a representative of the biocontrol bacterial strains. In this work, the lipopeptide bacillomycin D, produced by FZB42, showed strong fungicidal activity against Bacillomycin D caused morphological changes in the plasma membrane and cell wall of , induced accumulation of reactive oxygen species, and ultimately caused cell death in Interestingly, when was challenged with bacillomycin D, the deoxynivalenol production, gene expression, mitogen-activated protein kinase phosphorylation, and pathogenicity of were significantly altered. These findings clarified the mechanisms of the activity of bacillomycin D against and highlighted the potential of FZB42 as a biocontrol agent against .
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http://dx.doi.org/10.1128/AEM.01075-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5601353PMC
October 2017

Volatile organic compounds produced by a soil-isolate, Bacillus subtilis FA26 induce adverse ultra-structural changes to the cells of Clavibacter michiganensis ssp. sepedonicus, the causal agent of bacterial ring rot of potato.

Microbiology (Reading) 2017 04 18;163(4):523-530. Epub 2017 Apr 18.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing 210095, PR China.

Rhizobacterial volatile organic compounds (VOCs) play an important role in the suppression of soil-borne phytopathogens. In this study, the VOCs produced by a soil-isolate, Bacillus subtilis FA26, were evaluated in vitro for their antibacterial activity against Clavibacter michiganensis ssp. sepedonicus (Cms), the causal agent of bacterial ring rot of potato. The VOCs emitted by FA26 inhibited the growth of Cms significantly compared with the control. Scanning and transmission electron microscopy analyses revealed distorted colony morphology and a wide range of abnormalities in Cms cells exposed to the VOCs of FA26. Varying the inoculation strategy and inoculum size showed that the production and activity of the antibacterial VOCs of FA26 were dependent on the culture conditions. Headspace solid-phase microextraction/gas chromatography-mass spectrometry analyses revealed that FA26 produced 11 VOCs. Four VOCs (benzaldehyde, nonanal, benzothiazole and acetophenone) were associated with the antibacterial activity against Cms. The results suggested that the VOCs produced by FA26 could control the causal agent of bacterial ring rot of potato. This information will increase our understanding of the microbial interactions mediated by VOCs in nature and aid the development of safer strategies for controlling plant disease.
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http://dx.doi.org/10.1099/mic.0.000451DOI Listing
April 2017

Plant Growth Promotion by Volatile Organic Compounds Produced by SYST2.

Front Microbiol 2017 7;8:171. Epub 2017 Feb 7.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Diseases and Pests, Ministry of Education Nanjing, China.

Bacterial volatiles play a significant role in promoting plant growth by regulating the synthesis or metabolism of phytohormones. and growth chamber experiments were conducted to investigate the effect of volatile organic compounds (VOCs) produced by the plant growth promoting rhizobacterium strain SYST2 on hormone regulation and growth promotion in tomato plants. We observed a significant increase in plant biomass under both experimental conditions; we observed an increase in photosynthesis and in the endogenous contents of gibberellin, auxin, and cytokinin, while a decrease in ethylene levels was noted. VOCs emitted by SYST2 were identified through gas chromatography-mass spectrometry analysis. Of 11 VOCs tested in glass jars containing plants in test tubes, only two, albuterol and 1,3-propanediole, were found to promote plant growth. Furthermore, tomato plants showed differential expression of genes involved in auxin (), gibberellin (), cytokinin (), expansin (), and ethylene () biosynthesis or metabolism in roots and leaves in response to SYST2 VOCs. Our findings suggest that SYST2-derived VOCs promote plant growth by triggering growth hormone activity, and provide new insights into the mechanism of plant growth promotion by bacterial VOCs.
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http://dx.doi.org/10.3389/fmicb.2017.00171DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5293759PMC
February 2017

Involvement of FvSet1 in Fumonisin B1 Biosynthesis, Vegetative Growth, Fungal Virulence, and Environmental Stress Responses in Fusarium verticillioides.

Toxins (Basel) 2017 01 24;9(2). Epub 2017 Jan 24.

Key Laboratory of Monitoring and Management of Crop Diseases and Pest Insects, Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Ministry of Education, Nanjing 210095, China.

(teleomorph, ) is an important plant pathogen that causes seedling blight, stalk rot, and ear rot in maize (). During infection, produce fumonsins B1 (FB1) that pose a serious threat to human and animal health. Recent studies showed that Set1, a methyltransferase of H3K4, was responsible for toxin biosynthesis in filamentous fungi. However, to date, the regulation of FvSet1 on FB1 biosynthesis remains unclear. In the current study, we identified only one Set1 ortholog in (FvSet1) and found that the deletion of led to various defects in fungal growth and pathogenicity. More interestingly, the deletion mutant (ΔFvSet1) showed a significant defect in FB1 biosynthesis and lower expression levels of genes. FvSet1 was also found to play an important role in the responses of to multiple environmental stresses via regulating the phosphorylation of FvMgv1 and FvHog1. Taken together, these results indicate that FvSet1 plays essential roles in the regulation of FB1 biosynthesis, fungal growth and virulence, as well as various stress responses in
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http://dx.doi.org/10.3390/toxins9020043DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5331423PMC
January 2017

Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt.

Sci Rep 2017 01 16;7:40481. Epub 2017 Jan 16.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing 210095, PR China.

Volatile organic compounds (VOCs) produced by various bacteria have significant potential to enhance plant growth and to control phytopathogens. Six of the most effective antagonistic Bacillus spp. were used in this study against Ralstonia solanacearum (Rsc) TBBS1, the causal agent of bacterial wilt disease in tobacco. Bacillus amyloliquefaciens FZB42 and Bacillus artrophaeus LSSC22 had the strongest inhibitory effect against Rsc. Thirteen VOCs produced by FZB42 and 10 by LSSC22 were identified using gas chromatography-mass spectrometry analysis. Benzaldehyde, 1,2-benzisothiazol-3(2 H)-one and 1,3-butadiene significantly inhibited the colony size, cell viability, and motility of pathogens and negatively influenced chemotaxis. Transmission and scanning electron microscopy revealed severe morphological and ultra-structural changes in cells of Rsc. Furthermore, VOCs altered the transcriptional expression level of PhcA (a global virulence regulator), type III secretion system (T3SS), type IV secretion system (T4SS), extracellular polysaccharides and chemotaxis-related genes, which are major contributors to pathogenicity, resulting in decreased wilt disease. The VOCs significantly up-regulated the expression of genes related to wilt resistance and pathogen defense. Over-expression of EDS1 and NPR1 suggest the involvement of SA pathway in induction of systemic resistance. Our findings provide new insights regarding the potential of antibacterial VOCs as a biocontrol tool against bacterial wilt diseases.
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http://dx.doi.org/10.1038/srep40481DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5238454PMC
January 2017

Antibacterial effects of volatiles produced by Bacillus strain D13 against Xanthomonas oryzae pv. oryzae.

Mol Plant Pathol 2018 01 23;19(1):49-58. Epub 2016 Nov 23.

Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, 210095, China.

Recent investigations have demonstrated that bacteria employ the volatile compounds they produce during interactions with other organisms, such as plants, fungi, nematodes and bacteria. However, studies focused on the antibacterial activity of plant growth-promoting rhizobacteria (PGPR) volatiles against bacterial phytopathogens are still rare. In this study, Bacillus strain D13, which is antagonistic to Xanthomonas oryzae pv. oryzae (Xoo), was isolated and screened. Volatile compounds emitted from strain D13 reduced the colony diameter and cell motility of Xoo cultured in divided Petri plates. Transmission electron micrograph analysis showed concentration in cytoplasm and altered surface morphology in the majority of Xanthomonas cells after co-cultivation with strain D13. Transcriptional expression of virulence-associated genes in Xoo was repressed. Based on gas chromatography/mass spectrometry (GC/MS) analysis, 12 volatile compounds specifically produced by strain D13 were identified. Among them, decyl alcohol and 3,5,5-trimethylhexanol inhibited the growth of Xoo at minimum inhibitory amounts of 0.48 and 2.4 mg, respectively. Furthermore, transcriptional expression of virulence-associated genes was also repressed by decyl alcohol and 3,5,5-trimethylhexanol. These results are useful for a better understanding of the biocontrol mechanisms of Bacillus.
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http://dx.doi.org/10.1111/mpp.12494DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6637998PMC
January 2018

Acute toxicity assessment of explosive-contaminated soil extracting solution by luminescent bacteria assays.

Environ Sci Pollut Res Int 2016 Nov 26;23(22):22803-22809. Epub 2016 Aug 26.

Department of Environmental Engineering, Peking University, The Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing, 100871, China.

Explosive-contaminated soil is harmful to people's health and the local ecosystem. The acute toxicity of its extracting solution was tested by bacterial luminescence assay using three kinds of luminescent bacteria to characterize the toxicity of the soil. An orthogonal test L (4) was designed to optimize the soil extracting conditions. The optimum extracting conditions were obtained when the ultrasonic extraction time, ultrasonic extraction temperature, and the extraction repeat times were 6 h, 40 °C, and three, respectively. Fourier transform infrared spectroscopy (FTIR) results showed that the main components of the contaminated soil's extracting solution were 2,4-dinitrotoluene-3-sulfonate (2,4-DNT-3-SO); 2,4-dinitrotoluene-5-sulfonate (2,4-DNT-5-SO); and 2,6-dinitrotoluene (2,6-DNT). Compared with Photobacterium phosphoreum and Vibrio fischeri, Vibrio qinghaiensis sp. Nov. is more suitable for assessing the soil extracting solution's acute toxicity. Soil washing can remove most of the contaminants toxic to luminescent bacterium Vibrio qinghaiensis sp. Nov., suggesting that it may be a potential effective remediation method for explosive-contaminated soil.
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http://dx.doi.org/10.1007/s11356-016-7492-5DOI Listing
November 2016
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