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Origin and evolution of GALA-LRR, a new member of the CC-LRR subfamily: from plants to bacteria?

Kajava AV, Anisimova M, Peeters N - PLoS ONE (2008)

Bottom Line: The GALA LRRs do not perfectly fit any of the previously described LRR subfamilies.The examination of the selective evolutionary pressure acting on GALA proteins suggests that the convex side of their horse-shoe shaped LRR domains is more prone to positive selection than the concave side, and we therefore hypothesize that the convex surface might be the site of protein binding relevant to the adaptor function of the F-box GALA proteins.This conclusion provides a strong background for further functional studies aimed at determining the role of these type III effectors in the virulence of R. solanacearum.

View Article: PubMed Central - PubMed

Affiliation: Centre de Recherches de Biochimie Macromoléculaire, CNRS, University of Montpellier 1 and 2, Montpellier, France. andrey.kajava@crbm.cnrs.fr

ABSTRACT
The phytopathogenic bacterium Ralstonia solanacearum encodes type III effectors, called GALA proteins, which contain F-box and LRR domains. The GALA LRRs do not perfectly fit any of the previously described LRR subfamilies. By applying protein sequence analysis and structural prediction, we clarify this ambiguous case of LRR classification and assign GALA-LRRs to CC-LRR subfamily. We demonstrate that side-by-side packing of LRRs in the 3D structures may control the limits of repeat variability within the LRR subfamilies during evolution. The LRR packing can be used as a criterion, complementing the repeat sequences, to classify newly identified LRR domains. Our phylogenetic analysis of F-box domains proposes the lateral gene transfer of bacterial GALA proteins from host plants. We also present an evolutionary scenario which can explain the transformation of the original plant LRRs into slightly different bacterial LRRs. The examination of the selective evolutionary pressure acting on GALA proteins suggests that the convex side of their horse-shoe shaped LRR domains is more prone to positive selection than the concave side, and we therefore hypothesize that the convex surface might be the site of protein binding relevant to the adaptor function of the F-box GALA proteins. This conclusion provides a strong background for further functional studies aimed at determining the role of these type III effectors in the virulence of R. solanacearum.

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Side-by-side packing of LRRs having different consensus sequence motifs.“Knobs-into-holes” packing of GALA-LRRs against CC LRRs (contoured by a thin line box) and “knobs-into-knobs” packing of PS-LRRs, RI-LRRs, SDS22-LRRs, typical LRRs, bacterial LRRs against CC-LRRs. The CC-LRR-domain is in blue color. The side-chains that are involved in the inter-domain packing are shown by ball-and-stick representation. Arrows point at the clash sites where Cα and (or) Cβ atoms have distances between of 2.1–2.7 Å.
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pone-0001694-g003: Side-by-side packing of LRRs having different consensus sequence motifs.“Knobs-into-holes” packing of GALA-LRRs against CC LRRs (contoured by a thin line box) and “knobs-into-knobs” packing of PS-LRRs, RI-LRRs, SDS22-LRRs, typical LRRs, bacterial LRRs against CC-LRRs. The CC-LRR-domain is in blue color. The side-chains that are involved in the inter-domain packing are shown by ball-and-stick representation. Arrows point at the clash sites where Cα and (or) Cβ atoms have distances between of 2.1–2.7 Å.

Mentions: The modeling also shows that GALA-, GL-, and CC-LRRs can be packed well together and therefore, in contrast to the other LRR subfamilies, do not have mutually exclusive relationships with CC-LRRs in terms of inter-LRR packing (Figure 3). This conclusion is based on the following analysis. The conserved β-structural parts of the known crystal structures of LRR domains from different subfamilies and the model of GALA-LRRs were superimposed with the CC-LRR domain and the side-by-side packing of variable LRR fragments was analyzed (see Methods for details). The analysis shows that only the α-helices of GALA-LRR and CC-LRR have an energetically favorable “knobs-into-holes” interface while the superposition of LRRs from the other analyzed subfamilies with the CC-LRR results in “knobs-into-knobs” packing with steric tensions and voids (Figure 3). For example, the RI-LRR and CC-LRR, PS-LRR and CC-LRR, and SDS22-LRR and CC-LRR interfaces have distances between Cα and (or) Cβ atoms of 2.1-2.7 Å that are 0.5–1.1 Å closer than normally allowed limits for such distances [11]. This steric tension could be alleviated by a deformation of the LRR β-structure, but the distortion of the β-structural H-bonds would eventually also lead to the loss in the structure stability. The superposition of the typical LRR and CC-LRR domains does not lead to such close contacts, however, it results in an energetically unfavorable “knobs-into-knobs” packing with voids (Figure 3). Thus, our analysis suggests that some LRRs with different sequence motifs have an energetically favorable (“permissive”) packing, while simultaneous occurrence of the other ones in the same structure results in unfavorable (“mutually exclusive”) packing. The permissive packing of repeats with different consensus sequences may serve as a criterion for their membership in the same subfamily, at the same time as the mutually exclusive packing defines the boundaries between the LRR subfamilies.


Origin and evolution of GALA-LRR, a new member of the CC-LRR subfamily: from plants to bacteria?

Kajava AV, Anisimova M, Peeters N - PLoS ONE (2008)

Side-by-side packing of LRRs having different consensus sequence motifs.“Knobs-into-holes” packing of GALA-LRRs against CC LRRs (contoured by a thin line box) and “knobs-into-knobs” packing of PS-LRRs, RI-LRRs, SDS22-LRRs, typical LRRs, bacterial LRRs against CC-LRRs. The CC-LRR-domain is in blue color. The side-chains that are involved in the inter-domain packing are shown by ball-and-stick representation. Arrows point at the clash sites where Cα and (or) Cβ atoms have distances between of 2.1–2.7 Å.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2244805&req=5

pone-0001694-g003: Side-by-side packing of LRRs having different consensus sequence motifs.“Knobs-into-holes” packing of GALA-LRRs against CC LRRs (contoured by a thin line box) and “knobs-into-knobs” packing of PS-LRRs, RI-LRRs, SDS22-LRRs, typical LRRs, bacterial LRRs against CC-LRRs. The CC-LRR-domain is in blue color. The side-chains that are involved in the inter-domain packing are shown by ball-and-stick representation. Arrows point at the clash sites where Cα and (or) Cβ atoms have distances between of 2.1–2.7 Å.
Mentions: The modeling also shows that GALA-, GL-, and CC-LRRs can be packed well together and therefore, in contrast to the other LRR subfamilies, do not have mutually exclusive relationships with CC-LRRs in terms of inter-LRR packing (Figure 3). This conclusion is based on the following analysis. The conserved β-structural parts of the known crystal structures of LRR domains from different subfamilies and the model of GALA-LRRs were superimposed with the CC-LRR domain and the side-by-side packing of variable LRR fragments was analyzed (see Methods for details). The analysis shows that only the α-helices of GALA-LRR and CC-LRR have an energetically favorable “knobs-into-holes” interface while the superposition of LRRs from the other analyzed subfamilies with the CC-LRR results in “knobs-into-knobs” packing with steric tensions and voids (Figure 3). For example, the RI-LRR and CC-LRR, PS-LRR and CC-LRR, and SDS22-LRR and CC-LRR interfaces have distances between Cα and (or) Cβ atoms of 2.1-2.7 Å that are 0.5–1.1 Å closer than normally allowed limits for such distances [11]. This steric tension could be alleviated by a deformation of the LRR β-structure, but the distortion of the β-structural H-bonds would eventually also lead to the loss in the structure stability. The superposition of the typical LRR and CC-LRR domains does not lead to such close contacts, however, it results in an energetically unfavorable “knobs-into-knobs” packing with voids (Figure 3). Thus, our analysis suggests that some LRRs with different sequence motifs have an energetically favorable (“permissive”) packing, while simultaneous occurrence of the other ones in the same structure results in unfavorable (“mutually exclusive”) packing. The permissive packing of repeats with different consensus sequences may serve as a criterion for their membership in the same subfamily, at the same time as the mutually exclusive packing defines the boundaries between the LRR subfamilies.

Bottom Line: The GALA LRRs do not perfectly fit any of the previously described LRR subfamilies.The examination of the selective evolutionary pressure acting on GALA proteins suggests that the convex side of their horse-shoe shaped LRR domains is more prone to positive selection than the concave side, and we therefore hypothesize that the convex surface might be the site of protein binding relevant to the adaptor function of the F-box GALA proteins.This conclusion provides a strong background for further functional studies aimed at determining the role of these type III effectors in the virulence of R. solanacearum.

View Article: PubMed Central - PubMed

Affiliation: Centre de Recherches de Biochimie Macromoléculaire, CNRS, University of Montpellier 1 and 2, Montpellier, France. andrey.kajava@crbm.cnrs.fr

ABSTRACT
The phytopathogenic bacterium Ralstonia solanacearum encodes type III effectors, called GALA proteins, which contain F-box and LRR domains. The GALA LRRs do not perfectly fit any of the previously described LRR subfamilies. By applying protein sequence analysis and structural prediction, we clarify this ambiguous case of LRR classification and assign GALA-LRRs to CC-LRR subfamily. We demonstrate that side-by-side packing of LRRs in the 3D structures may control the limits of repeat variability within the LRR subfamilies during evolution. The LRR packing can be used as a criterion, complementing the repeat sequences, to classify newly identified LRR domains. Our phylogenetic analysis of F-box domains proposes the lateral gene transfer of bacterial GALA proteins from host plants. We also present an evolutionary scenario which can explain the transformation of the original plant LRRs into slightly different bacterial LRRs. The examination of the selective evolutionary pressure acting on GALA proteins suggests that the convex side of their horse-shoe shaped LRR domains is more prone to positive selection than the concave side, and we therefore hypothesize that the convex surface might be the site of protein binding relevant to the adaptor function of the F-box GALA proteins. This conclusion provides a strong background for further functional studies aimed at determining the role of these type III effectors in the virulence of R. solanacearum.

Show MeSH
Related in: MedlinePlus