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Rice-Infecting Pseudomonas Genomes Are Highly Accessorized and Harbor Multiple Putative Virulence Mechanisms to Cause Sheath Brown Rot.

Quibod IL, Grande G, Oreiro EG, Borja FN, Dossa GS, Mauleon R, Cruz CV, Oliva R - PLoS ONE (2015)

Bottom Line: Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world.Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism.The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

View Article: PubMed Central - PubMed

Affiliation: Plant Breeding, Genetics, and Biotechnology Division, International Rice Research Institute, Los Baños, Philippines.

ABSTRACT
Sheath rot complex and seed discoloration in rice involve a number of pathogenic bacteria that cannot be associated with distinctive symptoms. These pathogens can easily travel on asymptomatic seeds and therefore represent a threat to rice cropping systems. Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world. The appearance of a similar Pseudomonas population, which here we named P. fuscovaginae-like, represents a perfect opportunity to understand common genomic features that can explain the infection mechanism in rice. We showed that the novel population is indeed closely related to P. fuscovaginae. A comparative genomics approach on eight rice-infecting Pseudomonas revealed heterogeneous genomes and a high number of strain-specific genes. The genomes of P. fuscovaginae-like harbor four secretion systems (Type I, II, III, and VI) and other important pathogenicity machinery that could probably facilitate rice colonization. We identified 123 core secreted proteins, most of which have strong signatures of positive selection suggesting functional adaptation. Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism. The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

No MeSH data available.


Related in: MedlinePlus

P. fuscovaginae-like (Pfv-like) strains are closely related to P. fuscovaginae (Pfv).A) Average nucleotide identity (ANI) and average amino acid identity (AAI) clustering analysis of the eight rice-infecting Pseudomonas draft genomes. Clustering analysis identified two separated groups involving Pfv-like strains (orange) collected in the Philippines and Pfv strains (blue) collected elsewhere. Values scale is depicted in red, orange, yellow, and white colors in ANI (horizontal) and AAI (vertical) pairwise comparison. Value cut-offs with >95% reflect the possibility of same species grouping. The heatmap was generated in the R package gplots using the heatmap.2 function. B) Phylogenetic reconstruction of rice-infecting Pseudomonas and closely related Pseudomonas species using the concatenated housekeeping rpoB and rpoD. Maximum likelihood was used to infer the phylogenetic relationship with bootstrap of 1000 using the RAxML software [61]. Pfv and Pfv-like are highlighted in blue and orange, respectively.
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pone.0139256.g002: P. fuscovaginae-like (Pfv-like) strains are closely related to P. fuscovaginae (Pfv).A) Average nucleotide identity (ANI) and average amino acid identity (AAI) clustering analysis of the eight rice-infecting Pseudomonas draft genomes. Clustering analysis identified two separated groups involving Pfv-like strains (orange) collected in the Philippines and Pfv strains (blue) collected elsewhere. Values scale is depicted in red, orange, yellow, and white colors in ANI (horizontal) and AAI (vertical) pairwise comparison. Value cut-offs with >95% reflect the possibility of same species grouping. The heatmap was generated in the R package gplots using the heatmap.2 function. B) Phylogenetic reconstruction of rice-infecting Pseudomonas and closely related Pseudomonas species using the concatenated housekeeping rpoB and rpoD. Maximum likelihood was used to infer the phylogenetic relationship with bootstrap of 1000 using the RAxML software [61]. Pfv and Pfv-like are highlighted in blue and orange, respectively.

Mentions: To get insight into the overall homology levels and to evaluate genetic relatedness among Pfv and Pfv-like genomes, we calculated both ANI and AAI values for the eight genomes [44, 63]. We found levels of homology that were inconsistent with a single monophyletic group. In our analysis, the ANI values ranged from 87.95% to 98.65% while the AAI values varied from 87.95% to 99.35% (Fig 2A). We built a distance matrix based on pair-wise ANI-AAI values which identified at least two subgroups within rice-infecting Pseudomonas (Fig 2A). The dendrogram topology clustered the Pfv strains from Madagascar, Japan, China, and Australia separately from those Pfv-like strains from the Philippines. Similar to previous reports [22], IRRI 6609, IRRI7007, and S-E1 appear to be more related to each other. Values that separate Pfv and Pfv-like groups were below the species boundary cut-off of 95% (Fig 2A). This result also correlates with the TETRA analysis that had a species delineation cut-off of ≥ 99% (S1 Fig). Using a one-way comparison approach, we also explored the distribution of homology between IRRI 6609 and 78 closely related Pseudomonas genomes (S1 Table). Results were more consistent with a continuous distribution rather than a clearly defined cluster, with average ANI values ranging from 82.57% for P. stutzeri (n = 6) genomes to 96.13% for Pfv-like (n = 2) genomes (S2 Fig). The data suggest that Pfv-like genomes were more related to Pfv than to any of the other 71 closely related Pseudomonas genomes. We also characterized genome ancestry using a phylogenetic analysis involving 34 Pseudomonas accessions. Using rpoB and rpoD, we found two separated clusters (Fig 2B) that correlated with the homology status of ANI and AAI, in which Pfv and Pfv-like populations share a common ancestor. To further support the phylogenetic relationship of Pfv and Pfv-like strains (Fig 2B), we constructed a robust evolutionary tree using 10 housekeeping genes and observed similar results (S3 Fig). It is clear that species definition in the genus Pseudomonas can be particularly problematic for some of the groups due to the intrinsic diversity in their genomic content [17, 21]. For instance, the P. fluorescens group actually involved multiple species [20, 21] occupying quite diverse ecological niches. Based on the whole genome comparison or phylogenetic inference, we did not find any evidence suggesting that Pfv-like strains may be considered as Pfv sensu stricto. Moreover, Pfv may be part of a species complex composed of different groups including the Pfv-like organisms analyzed in this study. Whether these strains can be considered a novel species or not will need further research efforts.


Rice-Infecting Pseudomonas Genomes Are Highly Accessorized and Harbor Multiple Putative Virulence Mechanisms to Cause Sheath Brown Rot.

Quibod IL, Grande G, Oreiro EG, Borja FN, Dossa GS, Mauleon R, Cruz CV, Oliva R - PLoS ONE (2015)

P. fuscovaginae-like (Pfv-like) strains are closely related to P. fuscovaginae (Pfv).A) Average nucleotide identity (ANI) and average amino acid identity (AAI) clustering analysis of the eight rice-infecting Pseudomonas draft genomes. Clustering analysis identified two separated groups involving Pfv-like strains (orange) collected in the Philippines and Pfv strains (blue) collected elsewhere. Values scale is depicted in red, orange, yellow, and white colors in ANI (horizontal) and AAI (vertical) pairwise comparison. Value cut-offs with >95% reflect the possibility of same species grouping. The heatmap was generated in the R package gplots using the heatmap.2 function. B) Phylogenetic reconstruction of rice-infecting Pseudomonas and closely related Pseudomonas species using the concatenated housekeeping rpoB and rpoD. Maximum likelihood was used to infer the phylogenetic relationship with bootstrap of 1000 using the RAxML software [61]. Pfv and Pfv-like are highlighted in blue and orange, respectively.
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getmorefigures.php?uid=PMC4589537&req=5

pone.0139256.g002: P. fuscovaginae-like (Pfv-like) strains are closely related to P. fuscovaginae (Pfv).A) Average nucleotide identity (ANI) and average amino acid identity (AAI) clustering analysis of the eight rice-infecting Pseudomonas draft genomes. Clustering analysis identified two separated groups involving Pfv-like strains (orange) collected in the Philippines and Pfv strains (blue) collected elsewhere. Values scale is depicted in red, orange, yellow, and white colors in ANI (horizontal) and AAI (vertical) pairwise comparison. Value cut-offs with >95% reflect the possibility of same species grouping. The heatmap was generated in the R package gplots using the heatmap.2 function. B) Phylogenetic reconstruction of rice-infecting Pseudomonas and closely related Pseudomonas species using the concatenated housekeeping rpoB and rpoD. Maximum likelihood was used to infer the phylogenetic relationship with bootstrap of 1000 using the RAxML software [61]. Pfv and Pfv-like are highlighted in blue and orange, respectively.
Mentions: To get insight into the overall homology levels and to evaluate genetic relatedness among Pfv and Pfv-like genomes, we calculated both ANI and AAI values for the eight genomes [44, 63]. We found levels of homology that were inconsistent with a single monophyletic group. In our analysis, the ANI values ranged from 87.95% to 98.65% while the AAI values varied from 87.95% to 99.35% (Fig 2A). We built a distance matrix based on pair-wise ANI-AAI values which identified at least two subgroups within rice-infecting Pseudomonas (Fig 2A). The dendrogram topology clustered the Pfv strains from Madagascar, Japan, China, and Australia separately from those Pfv-like strains from the Philippines. Similar to previous reports [22], IRRI 6609, IRRI7007, and S-E1 appear to be more related to each other. Values that separate Pfv and Pfv-like groups were below the species boundary cut-off of 95% (Fig 2A). This result also correlates with the TETRA analysis that had a species delineation cut-off of ≥ 99% (S1 Fig). Using a one-way comparison approach, we also explored the distribution of homology between IRRI 6609 and 78 closely related Pseudomonas genomes (S1 Table). Results were more consistent with a continuous distribution rather than a clearly defined cluster, with average ANI values ranging from 82.57% for P. stutzeri (n = 6) genomes to 96.13% for Pfv-like (n = 2) genomes (S2 Fig). The data suggest that Pfv-like genomes were more related to Pfv than to any of the other 71 closely related Pseudomonas genomes. We also characterized genome ancestry using a phylogenetic analysis involving 34 Pseudomonas accessions. Using rpoB and rpoD, we found two separated clusters (Fig 2B) that correlated with the homology status of ANI and AAI, in which Pfv and Pfv-like populations share a common ancestor. To further support the phylogenetic relationship of Pfv and Pfv-like strains (Fig 2B), we constructed a robust evolutionary tree using 10 housekeeping genes and observed similar results (S3 Fig). It is clear that species definition in the genus Pseudomonas can be particularly problematic for some of the groups due to the intrinsic diversity in their genomic content [17, 21]. For instance, the P. fluorescens group actually involved multiple species [20, 21] occupying quite diverse ecological niches. Based on the whole genome comparison or phylogenetic inference, we did not find any evidence suggesting that Pfv-like strains may be considered as Pfv sensu stricto. Moreover, Pfv may be part of a species complex composed of different groups including the Pfv-like organisms analyzed in this study. Whether these strains can be considered a novel species or not will need further research efforts.

Bottom Line: Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world.Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism.The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

View Article: PubMed Central - PubMed

Affiliation: Plant Breeding, Genetics, and Biotechnology Division, International Rice Research Institute, Los Baños, Philippines.

ABSTRACT
Sheath rot complex and seed discoloration in rice involve a number of pathogenic bacteria that cannot be associated with distinctive symptoms. These pathogens can easily travel on asymptomatic seeds and therefore represent a threat to rice cropping systems. Among the rice-infecting Pseudomonas, P. fuscovaginae has been associated with sheath brown rot disease in several rice growing areas around the world. The appearance of a similar Pseudomonas population, which here we named P. fuscovaginae-like, represents a perfect opportunity to understand common genomic features that can explain the infection mechanism in rice. We showed that the novel population is indeed closely related to P. fuscovaginae. A comparative genomics approach on eight rice-infecting Pseudomonas revealed heterogeneous genomes and a high number of strain-specific genes. The genomes of P. fuscovaginae-like harbor four secretion systems (Type I, II, III, and VI) and other important pathogenicity machinery that could probably facilitate rice colonization. We identified 123 core secreted proteins, most of which have strong signatures of positive selection suggesting functional adaptation. Transcript accumulation of putative pathogenicity-related genes during rice colonization revealed a concerted virulence mechanism. The study suggests that rice-infecting Pseudomonas causing sheath brown rot are intrinsically diverse and maintain a variable set of metabolic capabilities as a potential strategy to occupy a range of environments.

No MeSH data available.


Related in: MedlinePlus