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Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

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T3E collections of S. fredii and B. japonicum are highly conserved in content.(A) Representation of T3Es in categories as percentage of total number of T3E families in S. fredii, B. japonicum, as well as group I and legume pathovars of P. syringae. Unconfirmed T3Es were not included. (B) Fisher's exact test for all pairwise comparisons (connected by lines) of the representation of T3Es in the four categories depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) Numbers of T3E genes and all genes binned as total, core, or accessory for each group of bacteria. Core genes are defined as those with orthologs present in all strains within each group. A Fisher's exact test was used to test for differences in distribution of core and accessory T3E genes relative to the distribution of all genes. All p-values are significant (Bonferonni adjusted α level = 0.0125).
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ppat-1003204-g004: T3E collections of S. fredii and B. japonicum are highly conserved in content.(A) Representation of T3Es in categories as percentage of total number of T3E families in S. fredii, B. japonicum, as well as group I and legume pathovars of P. syringae. Unconfirmed T3Es were not included. (B) Fisher's exact test for all pairwise comparisons (connected by lines) of the representation of T3Es in the four categories depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) Numbers of T3E genes and all genes binned as total, core, or accessory for each group of bacteria. Core genes are defined as those with orthologs present in all strains within each group. A Fisher's exact test was used to test for differences in distribution of core and accessory T3E genes relative to the distribution of all genes. All p-values are significant (Bonferonni adjusted α level = 0.0125).

Mentions: The T3Es of rhizobia were predominantly core, unlike the T3Es of the group I strains of P. syringae (Figure 4A). In fact, the representation of T3Es among the four categories of core, singletons (present in only a single strain of a group), pseudogenes (premature termination codon relative to a full-length family member), and other (polymorphic in regards to presence/absence), was significantly different (Figure 4B). Next, we compared the proportion of core and accessory T3E genes in the S. fredii, B. japonicum, and P. syringae group I strains to the proportion of genes that are core and accessory to each group (Figure 4C). Analysis indicated that the proportions of core T3E genes were significantly more than core genes for both groups of rhizobia. In contrast, the proportion of core T3E genes for the group I strains of P. syringae was significantly less. Thus, the collections of T3E genes of rhizobia are significantly more conserved than the collection of T3E genes of P. syringae and relative to their core genomes.


Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

T3E collections of S. fredii and B. japonicum are highly conserved in content.(A) Representation of T3Es in categories as percentage of total number of T3E families in S. fredii, B. japonicum, as well as group I and legume pathovars of P. syringae. Unconfirmed T3Es were not included. (B) Fisher's exact test for all pairwise comparisons (connected by lines) of the representation of T3Es in the four categories depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) Numbers of T3E genes and all genes binned as total, core, or accessory for each group of bacteria. Core genes are defined as those with orthologs present in all strains within each group. A Fisher's exact test was used to test for differences in distribution of core and accessory T3E genes relative to the distribution of all genes. All p-values are significant (Bonferonni adjusted α level = 0.0125).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585131&req=5

ppat-1003204-g004: T3E collections of S. fredii and B. japonicum are highly conserved in content.(A) Representation of T3Es in categories as percentage of total number of T3E families in S. fredii, B. japonicum, as well as group I and legume pathovars of P. syringae. Unconfirmed T3Es were not included. (B) Fisher's exact test for all pairwise comparisons (connected by lines) of the representation of T3Es in the four categories depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) Numbers of T3E genes and all genes binned as total, core, or accessory for each group of bacteria. Core genes are defined as those with orthologs present in all strains within each group. A Fisher's exact test was used to test for differences in distribution of core and accessory T3E genes relative to the distribution of all genes. All p-values are significant (Bonferonni adjusted α level = 0.0125).
Mentions: The T3Es of rhizobia were predominantly core, unlike the T3Es of the group I strains of P. syringae (Figure 4A). In fact, the representation of T3Es among the four categories of core, singletons (present in only a single strain of a group), pseudogenes (premature termination codon relative to a full-length family member), and other (polymorphic in regards to presence/absence), was significantly different (Figure 4B). Next, we compared the proportion of core and accessory T3E genes in the S. fredii, B. japonicum, and P. syringae group I strains to the proportion of genes that are core and accessory to each group (Figure 4C). Analysis indicated that the proportions of core T3E genes were significantly more than core genes for both groups of rhizobia. In contrast, the proportion of core T3E genes for the group I strains of P. syringae was significantly less. Thus, the collections of T3E genes of rhizobia are significantly more conserved than the collection of T3E genes of P. syringae and relative to their core genomes.

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

Show MeSH
Related in: MedlinePlus