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Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment

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ABSTRACT

Understanding the processes that shaped contemporary pathogen populations in agricultural landscapes is quite important to define appropriate management strategies and to support crop improvement efforts. Here, we took advantage of an historical record to examine the adaptation pathway of the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo) in a semi-isolated environment represented in the Philippine archipelago. By comparing genomes of key Xoo groups we showed that modern populations derived from three Asian lineages. We also showed that diversification of virulence factors occurred within each lineage, most likely driven by host adaptation, and it was essential to shape contemporary pathogen races. This finding is particularly important because it expands our understanding of pathogen adaptation to modern agriculture.

No MeSH data available.


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Clustering of ten Xanthomonas oryzae pv. oryzae strains from the Philippines by the predicted TALE targets in the rice genome (Nipponbare MSU7).Targets were predicted as described in Perez-Quintero et al.35. Clustering of strains in the top follows lineage classification (green = PX-A, blue = PX-B, and red = PX-C). Clustering on the left represents rice target distribution for each TALE repertoire. Intensity of the histogram indicates normalized prediction score (1 being highest score for one TALE in the genome). Multiple prediction scores for the same gene for one strain were summed, so values higher than 1 indicate targeting by multiple TALE from the same strain. Examples of known TALE targets in the rice genome are shown on the right.
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f4: Clustering of ten Xanthomonas oryzae pv. oryzae strains from the Philippines by the predicted TALE targets in the rice genome (Nipponbare MSU7).Targets were predicted as described in Perez-Quintero et al.35. Clustering of strains in the top follows lineage classification (green = PX-A, blue = PX-B, and red = PX-C). Clustering on the left represents rice target distribution for each TALE repertoire. Intensity of the histogram indicates normalized prediction score (1 being highest score for one TALE in the genome). Multiple prediction scores for the same gene for one strain were summed, so values higher than 1 indicate targeting by multiple TALE from the same strain. Examples of known TALE targets in the rice genome are shown on the right.

Mentions: The activation of target genes by TALEs is guided by cognate effector binding elements (EBEs) in the host genome6. Based on DNA-binding specificities, TEF clustering followed the same pattern of classification as described using RVD distances (Supplementary Fig. S7). This indicates that alleles within each TEF are likely to have similar host targets. To investigate if members from the same lineage have functionally equivalent TEFs, we analyzed predicted target genes in the rice genome using the program Talvez35 and found that lineage members share more predicted targets that non-members (Fig. 4). For instance, lineage PX-A and PX-B members share 73% and 66% of the hits, respectively (Supplementary Table S6). This observation is consistent with effector diversification within genetically related groups due to environmental adaptation as observed in other plant pathogens53. In addition, the reduced number of core TEFs indicates some level of functional redundancy, a strategy that has been proposed for other pathogens with type III effectors54. For instance, Xanthomonas pathogens achieve functional redundancy by having TALEs bound to overlapping EBEs on the same promoter. The most notorious example in Xoo is the case of the SWEET14 susceptibility gene, which contains three known EBEs in its promoter12. In our data, several genes were predicted to be targets of multiple strains or have more than one putative EBE in the promoter region (Fig. 4), suggesting that functional redundancy could occur frequently. Overall, our observations reveal a unique evolutionary pathway of this pathogen in the agricultural landscape of the Philippine archipelago, in which different lineages diverged into modern Xoo races. This process was likely to be driven by diversification of effector repertoires during host adaptation.


Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment
Clustering of ten Xanthomonas oryzae pv. oryzae strains from the Philippines by the predicted TALE targets in the rice genome (Nipponbare MSU7).Targets were predicted as described in Perez-Quintero et al.35. Clustering of strains in the top follows lineage classification (green = PX-A, blue = PX-B, and red = PX-C). Clustering on the left represents rice target distribution for each TALE repertoire. Intensity of the histogram indicates normalized prediction score (1 being highest score for one TALE in the genome). Multiple prediction scores for the same gene for one strain were summed, so values higher than 1 indicate targeting by multiple TALE from the same strain. Examples of known TALE targets in the rice genome are shown on the right.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5035989&req=5

f4: Clustering of ten Xanthomonas oryzae pv. oryzae strains from the Philippines by the predicted TALE targets in the rice genome (Nipponbare MSU7).Targets were predicted as described in Perez-Quintero et al.35. Clustering of strains in the top follows lineage classification (green = PX-A, blue = PX-B, and red = PX-C). Clustering on the left represents rice target distribution for each TALE repertoire. Intensity of the histogram indicates normalized prediction score (1 being highest score for one TALE in the genome). Multiple prediction scores for the same gene for one strain were summed, so values higher than 1 indicate targeting by multiple TALE from the same strain. Examples of known TALE targets in the rice genome are shown on the right.
Mentions: The activation of target genes by TALEs is guided by cognate effector binding elements (EBEs) in the host genome6. Based on DNA-binding specificities, TEF clustering followed the same pattern of classification as described using RVD distances (Supplementary Fig. S7). This indicates that alleles within each TEF are likely to have similar host targets. To investigate if members from the same lineage have functionally equivalent TEFs, we analyzed predicted target genes in the rice genome using the program Talvez35 and found that lineage members share more predicted targets that non-members (Fig. 4). For instance, lineage PX-A and PX-B members share 73% and 66% of the hits, respectively (Supplementary Table S6). This observation is consistent with effector diversification within genetically related groups due to environmental adaptation as observed in other plant pathogens53. In addition, the reduced number of core TEFs indicates some level of functional redundancy, a strategy that has been proposed for other pathogens with type III effectors54. For instance, Xanthomonas pathogens achieve functional redundancy by having TALEs bound to overlapping EBEs on the same promoter. The most notorious example in Xoo is the case of the SWEET14 susceptibility gene, which contains three known EBEs in its promoter12. In our data, several genes were predicted to be targets of multiple strains or have more than one putative EBE in the promoter region (Fig. 4), suggesting that functional redundancy could occur frequently. Overall, our observations reveal a unique evolutionary pathway of this pathogen in the agricultural landscape of the Philippine archipelago, in which different lineages diverged into modern Xoo races. This process was likely to be driven by diversification of effector repertoires during host adaptation.

View Article: PubMed Central - PubMed

ABSTRACT

Understanding the processes that shaped contemporary pathogen populations in agricultural landscapes is quite important to define appropriate management strategies and to support crop improvement efforts. Here, we took advantage of an historical record to examine the adaptation pathway of the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo) in a semi-isolated environment represented in the Philippine archipelago. By comparing genomes of key Xoo groups we showed that modern populations derived from three Asian lineages. We also showed that diversification of virulence factors occurred within each lineage, most likely driven by host adaptation, and it was essential to shape contemporary pathogen races. This finding is particularly important because it expands our understanding of pathogen adaptation to modern agriculture.

No MeSH data available.


Related in: MedlinePlus