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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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Structural model of GALA-LRR.(A) Cα-trace superposition of a modeled GALA-LRR and the known CC-LRR from human Skp2 protein [10] and RI-LRR from porcine ribonuclease inhibitor [46]. GALA-LRR model is shown in a ball-and-stick representation, CC-LRR is shown by a blue trace and RI-LRR by a magenta trace. Numbering of the conserved GALA-LRR residues is taken from Figure 1. Numbers in red point to positions inferred to be under positive selection. The carbon atoms are in green, oxygen in red, nitrogen in blue. (B) A ribbon diagram of a structural model of the C-terminal LRR domain of GALA4 type III effector protein from R. solanacearum (strain MolK2, region 170 to 460, accession code ZP_00946474). The figure was generated with Pymol [47]. The atomic coordinates of the model are available on request.
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pone-0001694-g002: Structural model of GALA-LRR.(A) Cα-trace superposition of a modeled GALA-LRR and the known CC-LRR from human Skp2 protein [10] and RI-LRR from porcine ribonuclease inhibitor [46]. GALA-LRR model is shown in a ball-and-stick representation, CC-LRR is shown by a blue trace and RI-LRR by a magenta trace. Numbering of the conserved GALA-LRR residues is taken from Figure 1. Numbers in red point to positions inferred to be under positive selection. The carbon atoms are in green, oxygen in red, nitrogen in blue. (B) A ribbon diagram of a structural model of the C-terminal LRR domain of GALA4 type III effector protein from R. solanacearum (strain MolK2, region 170 to 460, accession code ZP_00946474). The figure was generated with Pymol [47]. The atomic coordinates of the model are available on request.

Mentions: (A) An arrangement of LRRs (rhombs), F-boxes (rectangles) and BTB domain (ellipse) within new representative proteins of CC-LRR subfamily. The following proteins are shown: GALA4 from R. Solanacearum, strain GMI1000 GenBank accession number CAD15502; GALA protein from Legionella pneumophila subsp.pneumophila str. Philadelphia 1, AAU27032; hypothetical protein from Arabidopsis thaliana, AAF82144; putative regulatory subunit from Gemmata sp. Wa1-1, AAX07517; hypothetical protein from Parachlamydia sp. UWE25, CAF23996; hypothetical protein from Parachlamydia sp. UWE25, CAF24006. (B) Alignment of some known (indicated by *) and newly identified LRR consensus sequences. (C) A consensus sequences of an updated CC-LRR. The boxes over the alignment outline known or putative α-helical and β-structural regions. Bold uppercase and lowercase letters indicate more than 60% and 20% identity, correspondingly. “O” denotes an apolar residue, “x” denotes any residue, “-“ is a position of a gap. Numbers below the GALA-LRR consensus sequence show the positions of conserved residues (see also Figure 2A).


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)

Structural model of GALA-LRR.(A) Cα-trace superposition of a modeled GALA-LRR and the known CC-LRR from human Skp2 protein [10] and RI-LRR from porcine ribonuclease inhibitor [46]. GALA-LRR model is shown in a ball-and-stick representation, CC-LRR is shown by a blue trace and RI-LRR by a magenta trace. Numbering of the conserved GALA-LRR residues is taken from Figure 1. Numbers in red point to positions inferred to be under positive selection. The carbon atoms are in green, oxygen in red, nitrogen in blue. (B) A ribbon diagram of a structural model of the C-terminal LRR domain of GALA4 type III effector protein from R. solanacearum (strain MolK2, region 170 to 460, accession code ZP_00946474). The figure was generated with Pymol [47]. The atomic coordinates of the model are available on request.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001694-g002: Structural model of GALA-LRR.(A) Cα-trace superposition of a modeled GALA-LRR and the known CC-LRR from human Skp2 protein [10] and RI-LRR from porcine ribonuclease inhibitor [46]. GALA-LRR model is shown in a ball-and-stick representation, CC-LRR is shown by a blue trace and RI-LRR by a magenta trace. Numbering of the conserved GALA-LRR residues is taken from Figure 1. Numbers in red point to positions inferred to be under positive selection. The carbon atoms are in green, oxygen in red, nitrogen in blue. (B) A ribbon diagram of a structural model of the C-terminal LRR domain of GALA4 type III effector protein from R. solanacearum (strain MolK2, region 170 to 460, accession code ZP_00946474). The figure was generated with Pymol [47]. The atomic coordinates of the model are available on request.
Mentions: (A) An arrangement of LRRs (rhombs), F-boxes (rectangles) and BTB domain (ellipse) within new representative proteins of CC-LRR subfamily. The following proteins are shown: GALA4 from R. Solanacearum, strain GMI1000 GenBank accession number CAD15502; GALA protein from Legionella pneumophila subsp.pneumophila str. Philadelphia 1, AAU27032; hypothetical protein from Arabidopsis thaliana, AAF82144; putative regulatory subunit from Gemmata sp. Wa1-1, AAX07517; hypothetical protein from Parachlamydia sp. UWE25, CAF23996; hypothetical protein from Parachlamydia sp. UWE25, CAF24006. (B) Alignment of some known (indicated by *) and newly identified LRR consensus sequences. (C) A consensus sequences of an updated CC-LRR. The boxes over the alignment outline known or putative α-helical and β-structural regions. Bold uppercase and lowercase letters indicate more than 60% and 20% identity, correspondingly. “O” denotes an apolar residue, “x” denotes any residue, “-“ is a position of a gap. Numbers below the GALA-LRR consensus sequence show the positions of conserved residues (see also Figure 2A).

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