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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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Distribution of T3E families in rhizobia.The T3E family names are listed across the top with strains of (A) S. fredii and (B) B. japonicum listed down the side. Boxes are color-coded as indicated in the key; white boxes = no detectable homolog. Conservation of T3Es is also color-coded (bars below each chart) as indicated.
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ppat-1003204-g003: Distribution of T3E families in rhizobia.The T3E family names are listed across the top with strains of (A) S. fredii and (B) B. japonicum listed down the side. Boxes are color-coded as indicated in the key; white boxes = no detectable homolog. Conservation of T3Es is also color-coded (bars below each chart) as indicated.

Mentions: The demonstration that members of a polymorphic T3E family behaved identically in the heterologous delivery assay allowed us to test just a subset of 127 genes that represent the diversity present in the 268 candidates. From these, 87 T3Es belonging to 47 families between the two rhizobial lineages were confirmed for T3SS-dependent translocation (Table 1; Figure 3). We also used the sequences of members of confirmed T3E families to re-survey all draft genome sequences and identified an additional 21 homologs that were interrupted by physical and sequence gaps. Nine CDSs were amplified using PCR and sequenced and all were classified as functional based on the absence of premature termination codons. The remaining 12 genes belonged to 10 families with four homologs having upstream sequences similar to a tts-box but with bit-scores below our threshold. Seven had no discernible upstream tts-box, and one (nopM2) potentially represents a subgroup of the nopM family since two copies are present in B. japonicum USDA123.


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)

Distribution of T3E families in rhizobia.The T3E family names are listed across the top with strains of (A) S. fredii and (B) B. japonicum listed down the side. Boxes are color-coded as indicated in the key; white boxes = no detectable homolog. Conservation of T3Es is also color-coded (bars below each chart) as indicated.
© Copyright Policy
Related In: Results  -  Collection

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

ppat-1003204-g003: Distribution of T3E families in rhizobia.The T3E family names are listed across the top with strains of (A) S. fredii and (B) B. japonicum listed down the side. Boxes are color-coded as indicated in the key; white boxes = no detectable homolog. Conservation of T3Es is also color-coded (bars below each chart) as indicated.
Mentions: The demonstration that members of a polymorphic T3E family behaved identically in the heterologous delivery assay allowed us to test just a subset of 127 genes that represent the diversity present in the 268 candidates. From these, 87 T3Es belonging to 47 families between the two rhizobial lineages were confirmed for T3SS-dependent translocation (Table 1; Figure 3). We also used the sequences of members of confirmed T3E families to re-survey all draft genome sequences and identified an additional 21 homologs that were interrupted by physical and sequence gaps. Nine CDSs were amplified using PCR and sequenced and all were classified as functional based on the absence of premature termination codons. The remaining 12 genes belonged to 10 families with four homologs having upstream sequences similar to a tts-box but with bit-scores below our threshold. Seven had no discernible upstream tts-box, and one (nopM2) potentially represents a subgroup of the nopM family since two copies are present in B. japonicum USDA123.

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