Sustainable Strategies for Managing Bacterial Panicle Blight in Rice

Rice is an important source of food for more than half the world’s population. Bacterial panicle blight (BPB) is a disease of rice characterized by grain discoloration or sheath rot caused mainly by Burkholderia glumae . B. glumae synthesizes toxoflavin, an essential virulence factor, that is required for symptoms of the disease. The products of the tox operons, ToxABCDE and ToxFGHI, are responsible for the synthesis and the proton motive force (PMF)-dependent secretion of toxoflavin, respectively. The DedA family is a highly conserved membrane protein family found in most bacterial genomes that likely function as membrane transporters. Our previous work has demonstrated that absence of certain DedA family members results in pleiotropic effects, impacting multiple pathways that are energized by PMF. We have demonstrated that a member of the DedA family from Burkholderia thailandensis , named DbcA, is required for the extreme polymyxin resistance observed in this organism. B. glumae encodes a homolog of DbcA with 73% amino acid identity to Burkholderia thailandensis DbcA. Here, we created and characterized a B. glumae Δ dbcA strain. In addition to polymyxin sensitivity, B. glumae Δ dbcA is compromised for virulence in several BPB infection models and secretes only low amounts of toxoflavin (∼15% of wild type levels). Changes in membrane potential in B. glumae Δ dbcA were reproduced in the wild type strain by the addition of sub-inhibitory concentrations of sodium bicarbonate, previously demonstrated to cause disruption of PMF. Sodium bicarbonate inhibited B. glumae virulence in rice suggesting a possible non-toxic chemical intervention for bacterial panicle blight. IMPORTANCE Bacterial panicle blight (BPB) is a disease of rice characterized by grain discoloration or sheath rot caused mainly by Burkholderia glumae . The DedA family is a highly conserved membrane protein family found in most bacterial genomes that likely function as membrane transporters. Here, we constructed a B. glumae mutant with a deletion in a DedA family member named dbcA and report a loss of virulence in models of BPB. Physiological analysis of the mutant shows that the proton motive force is disrupted, leading to reduction of secretion of the essential virulence factor toxoflavin. The mutant phenotypes are reproduced in the virulent wild type strain without an effect on growth using sodium bicarbonate, a nontoxic buffer that has been reported to disrupt the PMF. The results presented here suggest that bicarbonate may be an effective antivirulence agent capable of controlling BPB without imposing an undue burden on the environment.

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Bacterial Panicle Blight Resistance QTLs in Rice and Their Association with Other Disease Resistance Loci and Heading Date

Crop Science ◽

10.2135/cropsci2008.07.0447 ◽

2010 ◽

Vol 50 (4) ◽

pp. 1287-1297 ◽

Cited By ~ 22

Author(s):

Shannon R. M. Pinson ◽

Abul K. M. Shahjahan ◽

M. Charles Rush ◽

Donald E. Groth

Keyword(s):

Disease Resistance ◽

Heading Date ◽

Blight Resistance ◽

Resistance Qtls ◽

Panicle Blight

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Association of Burkholderia glumae and B. gladioli with Panicle Blight Symptoms on Rice in Panama

Plant Disease ◽

10.1094/pdis-91-6-0767c ◽

2007 ◽

Vol 91 (6) ◽

pp. 767-767 ◽

Cited By ~ 26

Author(s):

R. Nandakumar ◽

M. C. Rush ◽

F. Correa

Keyword(s):

United States ◽

Fatty Acid ◽

16S Rdna ◽

Latin American ◽

The United States ◽

Unknown Etiology ◽

Rice Grain ◽

Burkholderia Glumae ◽

Specific Primers ◽

Panicle Blight

Panicle blight of rice, caused by Burkholderia glumae, has been a serious problem on rice in Japan since 1955. It has been reported from other rice-producing countries around the world and recently was reported on rice in the southern United States (2). A rice producer in Panama contacted us to verify the occurrence of bacterial panicle blight in rice fields where heavy losses were associated with a disease of unknown etiology, but with typical bacterial panicle blight symptoms (2). The observed grain discoloration, sterility, and abortion were thought to be due to the spinki mite, Steneotarsonemus spinki Smiley. After obtaining a USDA-APHIS import permit (73325), rice panicle samples from seven fields in Panama were sent to our laboratory in 2006. Bacteria were isolated from grains showing typical panicle blight symptoms on the semiselective S-Pg medium. Nonfluorescing colonies producing toxoflavin on King's B medium were selected for further identification. Initial PCR analyses, made with DNA isolated directly from grain crushed in sterile water, with B. glumae specific primers (BGF 5′ACACGG AACACCTGGGTA3′ and BGR 5′TCGCTCTCCCGAAGAGAT3′) gave a positive reaction for B. glumae in all seven samples. Biolog tests (Biolog Inc, Hayward, CA), fatty acid analysis, and PCR using species-specific primers for B. glumae and B. gladioli (BLF 5′CGAGCT AATACCGCGAAA3′ and BLR 5′AGACTCGA GTCAACTGA3′) identified 19 B. glumae and 6 B. gladioli strains among 35 bacterial strains isolated. Only the Biolog and fatty acid analyses identified B. gladioli strains. PCR analysis did not identify B. gladioli strains. To confirm B. gladioli, PCR amplification of the 16S rDNA gene from eight representative strains (four each for B. glumae and B. gladioli) using universal primers (16SF 5′AGAGTTTGATCCTGGCTCAG3′ and 16SR5′GGCTACCTTGTTACGACTT3′) and further sequencing of the PCR product was performed. A BLAST analysis of 16S rDNA sequences in the Genbank data base showed 99% sequence similarity for these two species with other published sequences. Our APHIS import permit did not allow us to perform pathogenicity tests with the strains isolated from Panama, but the B. glumae and B. gladioli strains obtained corresponded closely with pathogenic control cultures isolated from rice grown in the United States or with strains obtained from the ATCC. Other B. glumae strains recently isolated from rice in Panama, and identified by PCR, were tested for pathogenicity in tests conducted at CIAT in Colombia and were found to be pathogenic and highly virulent. These strains caused disease on seedlings when inoculated and typical bacterial panicle blight symptoms on panicles when spray inoculated. This disease has caused severe losses in Panama's rice crop for at least 3 years. Similar symptoms reported in Cuba, Haiti, and the Dominican Republic were attributed to damage from the spinki mite in association with Sarocladium oryzae (Sawada) W. Gams & D. Hawksw. (1). Zeigler and Alvarez (3) reported the occurrence of B. glumae in Columbia in 1987, but not in other Latin American countries. Pseudomonas fuscovaginae was reported in association with rice grain discoloration in Panama (4), but to our knowledge, this is the first report of these two Burkholderia species being associated with panicle blight symptoms on rice in Panama. References: (1) T. B. Bernal et al. Fitosanidad 6:15, 2002. (2). A. K. M. Shahjahan et al. Rice J. 103:26, 2000. (3). R. S. Zeigler and E. Alvarez. Plant Dis. 73:368, 1989. (4). R. S. Zeigler et al. Plant Dis. 71:896, 1987.

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Prevalence of Burkholderia glumae in rice crops in Ecuador

The Journal of Agriculture of the University of Puerto Rico ◽

10.46429/jaupr.v102i1-2.17532 ◽

2018 ◽

Vol 102 (1-2) ◽

pp. 65-78

Author(s):

Lenin Celiano Paz-Carrasco ◽

Luz Diana Intriago-Mendoza ◽

Marcos Fernando Basso ◽

Roberto E. Celi-Herán

Keyword(s):

Economic Importance ◽

23S Rrna ◽

Bacterial Isolates ◽

Severe Damage ◽

Burkholderia Glumae ◽

Genetic Studies ◽

Molecular Assays ◽

Blight Disease ◽

Panicle Blight

Burkholderia glumae is the agent responsible for bacterial panicle blight disease (BPBD) of rice that causes severe damage to this crop worldwide. During 2012 and 2013, symptoms of BPBD were observed in Palestina city, located in Guayas province, Ecuador. In 2014, the presence of B. glumae was confirmed at this location. In view of the socio-economic importance of rice in Ecuador, this research aimed to investigate the prevalence of B. glumae in other rice-producing regions. Eighteen bacterial isolates obtained from blighted kernels were characterized. Physiological, biochemical, serological, and molecular assays and the amplification of the 16S-23S rRNA ITS of the bacterial isolates collected confirmed the identity of the BPBD-associated bacterium. Pathogenicity assays verified the ability of these isolates to produce discoloration, spotting, and empty grains, symptoms associated with BPBD. Antibiotic assays showed that EC-EELS-01 isolate was sensitive to ciprofloxacin and tetracycline, and resistant to polymyxin. The dissemination and prevalence of B. glumae were confirmed in the rice-producing areas of El Oro, Cañar, Guayas, and Los Rios provinces. This research will serve to develop genetic studies to characterize the population in the B. glumae isolates in Ecuador.

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Warming increases Bacterial Panicle Blight (Burkholderia glumae) occurrences and impacts on USA rice production

PLoS ONE ◽

10.1371/journal.pone.0219199 ◽

2019 ◽

Vol 14 (7) ◽

pp. e0219199 ◽

Cited By ~ 3

Author(s):

Aaron M. Shew ◽

Alvaro Durand-Morat ◽

Lawton L. Nalley ◽

Xin-Gen Zhou ◽

Clemencia Rojas ◽

...

Keyword(s):

Rice Production ◽

Burkholderia Glumae ◽

Panicle Blight

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Bacterial Panicle Blight and Burkholderia glumae: from pathogen biology to disease control

Phytopathology ◽

10.1094/phyto-09-20-0401-rvw ◽

2020 ◽

Author(s):

Laura Ortega ◽

Clemencia Rojas

Keyword(s):

Biological Control ◽

Disease Resistance ◽

Disease Control ◽

Virulence Factors ◽

Plant Disease Resistance ◽

Plant Disease ◽

Rice Production ◽

Burkholderia Glumae ◽

Insight Into ◽

Panicle Blight

Bacterial Panicle Blight (BPB), caused by the bacterium Burkholderia glumae, has affected rice production worldwide. In spite of its importance, neither the disease nor its causal agent are well understood. Moreover, methods to manage BPB are still lacking. Nevertheless, the emerging importance of this pathogen has stimulated research to identify the mechanisms of pathogenicity, to gain insight into plant disease resistance, and to develop strategies to manage the disease. In this review, we consolidate current information regarding the virulence factors that have been identified in B. glumae and present a model of the disease and the pathogen. We also provide an update on the current research status to develop methods to control the disease especially through biological control approaches and through the development of resistant cultivars.

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IBUN2755 Bacillus strain controls seedling root and bacterial panicle blight caused by Burkholderia glumae

Biological Control ◽

10.1016/j.biocontrol.2020.104494 ◽

2021 ◽

Vol 153 ◽

pp. 104494

Author(s):

Luz Adriana Pedraza-Herrera ◽

Jessica Paola Bautista ◽

Carlos Alberto Cruz-Ramírez ◽

Daniel Uribe-Vélez

Keyword(s):

Burkholderia Glumae ◽

Bacillus Strain ◽

Seedling Root ◽

Panicle Blight

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Genome Sequence and Adaptation Analysis of the Human and Rice Pathogenic Strain Burkholderia glumae AU6208

Pathogens ◽

10.3390/pathogens10020087 ◽

2021 ◽

Vol 10 (2) ◽

pp. 87

Author(s):

Zhouqi Cui ◽

Sai Wang ◽

Kaleem Ullah Kakar ◽

Guanglin Xie ◽

Bin Li ◽

...

Keyword(s):

Genome Sequence ◽

Type Strain ◽

Antibiotic Biosynthesis ◽

Chronic Infections ◽

Burkholderia Glumae ◽

Niche Adaptation ◽

History Of ◽

Clinical Conditions ◽

Important Disease ◽

Panicle Blight

Burkholderia glumae causes rice (Oryza sativa) bacterial panicle blight, which is an increasingly economically important disease worldwide. As the first B. glumae strain isolated from patients with chronic infections, AU6208 has been reported as an opportunistic clinic pathogen. However, our understanding of the molecular mechanism underlying human pathogenesis by B. glumae remains rudimentary. In this study, we report the complete genome sequence of the human-isolated B. glumae strain AU6208 and compare this to the genome of the rice-pathogenic B. glumae type strain LMG 2196T. Analysis of the average nucleotide identity demonstrated 99.4% similarity between the human- and plant-pathogenic strains. However, the phenotypic results from this study suggest a history of niche adaptation and divergence. In particular, we found 44 genes were predicted to be horizontally transferred into AU6208, and most of these genes were upregulated in conditions that mimic clinical conditions. In these, the gene pair sbnAB encodes key enzymes in antibiotic biosynthesis. These results suggest that horizontal gene transfer in AU6208 may be responsible for selective advantages in its pathogenicity in humans. Our analysis of the AU6208 genome and comparison with that of LMG 2196T reveal the evolutionary signatures of B. glumae in the process of switching niches from plants to humans.

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Bioinspired Green Synthesis of Zinc Oxide Nanoparticles from a Native Bacillus cereus Strain RNT6: Characterization and Antibacterial Activity against Rice Panicle Blight Pathogens Burkholderia glumae and B. gladioli

Nanomaterials ◽

10.3390/nano11040884 ◽

2021 ◽

Vol 11 (4) ◽

pp. 884

Author(s):

Temoor Ahmed ◽

Zhifeng Wu ◽

Hubiao Jiang ◽

Jinyan Luo ◽

Muhammad Noman ◽

...

Keyword(s):

Zinc Oxide ◽

Antibacterial Activity ◽

Bacillus Cereus ◽

Zinc Oxide Nanoparticles ◽

Broth Culture ◽

Oxide Nanoparticles ◽

Rrna Gene ◽

Burkholderia Glumae ◽

Vis Spectroscopy ◽

Panicle Blight

Burkholderia glumae and B. gladioli are seed-borne rice pathogens that cause bacterial panicle blight (BPB) disease, resulting in huge rice yield losses worldwide. However, the excessive use of chemical pesticides in agriculture has led to an increase in environmental toxicity. Microbe-mediated nanoparticles (NPs) have recently gained significant attention owing to their promising application in plant disease control. In the current study, we biologically synthesize zinc oxide nanoparticles (ZnONPs) from a native Bacillus cereus RNT6 strain, which was taxonomically identified using 16S rRNA gene analysis. The biosynthesis of ZnONPs in the reaction mixture was confirmed by using UV–Vis spectroscopy. Moreover, XRD, FTIR, SEM-EDS, and TEM analysis revealed the functional groups, crystalline nature, and spherical shape of ZnONPs with sizes ranging from 21 to 35 nm, respectively. Biogenic ZnONPs showed significant antibacterial activity at 50 µg mL−1 against B. glumae and B. gladioli with a 2.83 cm and 2.18 cm zone of inhibition, respectively, while cell numbers (measured by OD600) of the two pathogens in broth culture were reduced by 71.2% and 68.1%, respectively. The ultrastructure studies revealed the morphological damage in ZnONPs-treated B. glumae and B. gladioli cells as compared to the corresponding control. The results of this study revealed that ZnONPs could be considered as promising nanopesticides to control BPB disease in rice.

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First Report of Bacterial Panicle Blight of Rice Caused by Burkholderia gladioli in Ecuador

Plant Disease ◽

10.1094/pdis-03-14-0222-pdn ◽

2014 ◽

Vol 98 (11) ◽

pp. 1577-1577 ◽

Cited By ~ 4

Author(s):

C. Riera-Ruiz ◽

J. Vargas ◽

J. M. Cevallos-Cevallos ◽

M. Ratti ◽

E. L. Peralta

Keyword(s):

Respiratory Infections ◽

Methyl Violet ◽

Clinical Importance ◽

Phenol Red ◽

Biochemical Tests ◽

First Report ◽

Burkholderia Gladioli ◽

A Cell ◽

O 24 ◽

Panicle Blight

Burkholderia gladioli is one of the causal agents of bacterial panicle blight of rice (BPB). Although B. glumae is considered the main pathogen responsible of BPB, B. gladioli can also cause this disease in rice (3). B. gladioli is also of clinical importance because of the ability of some strains to cause respiratory infections in humans (2). Symptoms in rice plantations of Palestina city, like upright panicles with grayish-straw color, grain rot, and vain grains were observed in July 2013, although similar symptoms were first noticed as early as 2012 in other regions of Ecuador. Since then, similar symptomatology has been reported by farmers in coastal provinces, possibly affecting 75% of the crops. One of the causal agents was recently identified as B. glumae but other bacteria were observed in infected rice (1). Plants showing BPB symptoms were collected from Palestina and bacteria were isolated from panicle twigs using the semi selective SPG agar (KH2PO4 1.3 g, Na2HPO4 1.2 g, (NH4)2SO4 5 g, MgSO4·7H2O 0.25 g, Na2MoO4·2H2O 24 mg, EDTA-Fe 10 mg, L-cystine 10 μg, D-sorbitol 10 g, pheneticillin potassium 50 mg, ampicillin sodium 10 mg, cetrimide 10 mg, methyl violet 1 mg, phenol red 20 mg, agar 15 g/liter distilled water). Colonies were then transferred to PDA. Presumptive B. gladioli colonies were classified into two groups according to their color on PDA. Colonies from group one (six strains) were dull yellow, whereas those from group two (two strains) were olive colored. Both groups produced fluorescent colonies with smooth, shiny surfaces on PDA. All cells were gram-negative rods with the following dimensions: 0.8 to 2.0 × 0.4 to 0.6 μm (group one) or 1.5 to 2.5 × 0.4 to 0.7 μm (group two). All colonies were subjected to biochemical tests (API 20NE) and shared a 99% or higher similarity (APIWEB) with B. gladioli. To confirm identity, genomic DNA was extracted (gDNA extraction kit from Invitrogen) and a portion of the 16s rDNA was amplified by PCR using the primers 536F: 5′-GTGCCAGCMGCCGCGGTAATAC-3′ and 1492R: 5′-GGTTACCTTGTTACGACTT-3′ followed by sequencing. Sequences of group one strains shared 100% similarity with B. gladioli strain OM1 (GenBank Accession No. EU678361) while the sequences from group two strains were 100% similar to B. gladioli strain BgHL-01 (JX566503). Sequences of the Ecuadorian strains were deposited into NCBI GenBank (group one: KF669879 to KF669882, KF669884, and KF669885; group two: KF669883 and KF669886). Pathogenicity was confirmed by submerging rice seeds in a cell suspension with 108 CFU of the pathogen for 24 h. Seeds were germinated at 28°C and about 70% RH on autoclaved peat. Inoculated seeds yielded plants with BPB symptoms 6 days after planting. Re-isolated strains shared a 99.9% similarity with B. gladioli by APIWEB. To the best of our knowledge, this is the first report of B. gladioli as a rice pathogen in Ecuador. References: (1) C. Riera-Ruiz et al. Plant Dis. 98:988, 2014. (2) C. Segonds et al. J. Clin. Microbiol. 47:1510, 2009. (3) H. Ura et al. J. Gen. Plant Pathol. 72:98, 2006.

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