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

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.


Clustering of 10 Xanthomonas oryzae pv. oryzae strains from the Philippines based on lesion lengths 14 days after leaf clip inoculation to 14 near-isogenic lines (NILs) carrying single Xa genes. Circles proportionally represent the length of the lesion averaged across 6 replicates. NILs are distinguished by color. Lineages are color-coded in the tree.
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f5: Clustering of 10 Xanthomonas oryzae pv. oryzae strains from the Philippines based on lesion lengths 14 days after leaf clip inoculation to 14 near-isogenic lines (NILs) carrying single Xa genes. Circles proportionally represent the length of the lesion averaged across 6 replicates. NILs are distinguished by color. Lineages are color-coded in the tree.

Mentions: To assess the contribution of effector repertoires to the virulence spectrum, we measured disease symptoms on rice NILs carrying 14 known resistance genes. Interestingly, we found that members of the same lineage are more likely to have similar virulence spectra (Fig. 5). Even though the composition of TEF will not explain all the symptoms observed, phenotypic differences may be due to single major genes in some cases. We then analyzed possible correlations between the phenotypes and the effector composition of each strain. While the presence of several TEFs seemed to be associated with major effects (Fig. 6), smaller effects were observed for some Xops (Supplementary Fig. S8). A strong negative correlation between lesion length and presence of a TEF was found for known TALE/executor gene pairs, particularly evident in the case of AvrXa10/IRBB1055 and AvrXa27/IRBB2756 (Fig. 6). Curiously, the presence of TEF11b, very similar in RVD sequence to AvrXa27 (Supplementary Table S5), did not correlate with lesion length, suggesting that this variant might escape the Xa27 executor gene activation trap. No correlation was found for IRBB23/AvrXa2315 due to the absence of variation (all strains tested contained AvrXa23 and caused short lesions). This analysis also showed that AvrXa7 correlates negatively with Xa7-mediated resistance and positively to xa13-resistance (AvrXa7 can overcome xa13 resistance)57. The opposite was true for PthXo1, which highlights the importance of redundant targeting of SWEET families for Xoo pathogenicity. Both PXO99A and PXO71 appear to overcome xa5 resistance genes using PthXo1, a TALE that activates OsSWEET1158. Interestingly, members of TEF19 have a similar pattern to AvrXa7 (TEF24) for reaction on xa13, Xa7, and xa5. Since these members have different sequence specificities (Supplementary Table S5), TEF19 represents an opportunity to study targeting redundancy in the Xoo–rice interaction. Additional correlations, such as a correlation between xa8 and TEF12/TEF27, are currently being investigated. Overall, the associations of TEF with phenotype underscore the critical importance and utility of including TALE sequence analysis in any genotype-based approach to phenotyping20.


Effector Diversification Contributes to Xanthomonas oryzae pv. oryzae Phenotypic Adaptation in a Semi-Isolated Environment
Clustering of 10 Xanthomonas oryzae pv. oryzae strains from the Philippines based on lesion lengths 14 days after leaf clip inoculation to 14 near-isogenic lines (NILs) carrying single Xa genes. Circles proportionally represent the length of the lesion averaged across 6 replicates. NILs are distinguished by color. Lineages are color-coded in the tree.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Clustering of 10 Xanthomonas oryzae pv. oryzae strains from the Philippines based on lesion lengths 14 days after leaf clip inoculation to 14 near-isogenic lines (NILs) carrying single Xa genes. Circles proportionally represent the length of the lesion averaged across 6 replicates. NILs are distinguished by color. Lineages are color-coded in the tree.
Mentions: To assess the contribution of effector repertoires to the virulence spectrum, we measured disease symptoms on rice NILs carrying 14 known resistance genes. Interestingly, we found that members of the same lineage are more likely to have similar virulence spectra (Fig. 5). Even though the composition of TEF will not explain all the symptoms observed, phenotypic differences may be due to single major genes in some cases. We then analyzed possible correlations between the phenotypes and the effector composition of each strain. While the presence of several TEFs seemed to be associated with major effects (Fig. 6), smaller effects were observed for some Xops (Supplementary Fig. S8). A strong negative correlation between lesion length and presence of a TEF was found for known TALE/executor gene pairs, particularly evident in the case of AvrXa10/IRBB1055 and AvrXa27/IRBB2756 (Fig. 6). Curiously, the presence of TEF11b, very similar in RVD sequence to AvrXa27 (Supplementary Table S5), did not correlate with lesion length, suggesting that this variant might escape the Xa27 executor gene activation trap. No correlation was found for IRBB23/AvrXa2315 due to the absence of variation (all strains tested contained AvrXa23 and caused short lesions). This analysis also showed that AvrXa7 correlates negatively with Xa7-mediated resistance and positively to xa13-resistance (AvrXa7 can overcome xa13 resistance)57. The opposite was true for PthXo1, which highlights the importance of redundant targeting of SWEET families for Xoo pathogenicity. Both PXO99A and PXO71 appear to overcome xa5 resistance genes using PthXo1, a TALE that activates OsSWEET1158. Interestingly, members of TEF19 have a similar pattern to AvrXa7 (TEF24) for reaction on xa13, Xa7, and xa5. Since these members have different sequence specificities (Supplementary Table S5), TEF19 represents an opportunity to study targeting redundancy in the Xoo–rice interaction. Additional correlations, such as a correlation between xa8 and TEF12/TEF27, are currently being investigated. Overall, the associations of TEF with phenotype underscore the critical importance and utility of including TALE sequence analysis in any genotype-based approach to phenotyping20.

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.