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Dynamic evolution of toll-like receptor multigene families in echinoderms.

Buckley KM, Rast JP - Front Immunol (2012)

Bottom Line: Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences).The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level.These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Department of Immunology, Sunnybrook Research Institute, University of Toronto Toronto, ON, Canada.

ABSTRACT
The genome sequence of the purple sea urchin, Strongylocentrotus purpuratus, a large and long-lived invertebrate, provides a new perspective on animal immunity. Analysis of this genome uncovered a highly complex immune system in which the gene families that encode homologs of the pattern recognition receptors that form the core of vertebrate innate immunity are encoded in large multigene families. The sea urchin genome contains 253 Toll-like receptor (TLR) sequences, more than 200 Nod-like receptors and 1095 scavenger receptor cysteine-rich domains, a 10-fold expansion relative to vertebrates. Given their stereotypic protein structure and simple intron-exon architecture, the TLRs are the most tractable of these families for more detailed analysis. A role for these receptors in immune defense is suggested by their similarity to TLRs in other organisms, sequence diversity, and expression in immunologically active tissues, including phagocytes. The complexity of the sea urchin TLR multigene families is largely derived from expansions independent of those in vertebrates and protostomes, although a small family of TLRs with structure similar to that of Drosophila Toll can be traced to an ancient eumetazoan ancestor. Several other echinoderm sequences are now available, including Lytechinus variegatus, as well as partial sequences from two other sea urchin species. Here, we present an analysis of the invertebrate deuterostome TLRs with emphasis on the echinoderms. Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences). The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level. These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

No MeSH data available.


Complete phylogeny of the sea urchin TLR sequences. The TIR domains of the TLR sequences from S. purpuratus and L. variegatus were used to construct the tree shown, which is a more detailed version of the tree in Figure 2. Bootstrap values greater than 50 are shown. Red indicates clades that are specific to S. purpuratus, blue clades contain only sequences from L. variegatus, and black clades contain sequences from both species. Each of the boxes (1–4) is shown in greater detail as indicated. The sequences are labeled by scaffold number and the position of the open reading frame (scaffold_start_stop). More information about the sequences can be found in Tables S1 and S2 in Supplementary Material. Subfamily designations are indicated on the right of each tree and correspond to those shown in Figure 2.
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FA1: Complete phylogeny of the sea urchin TLR sequences. The TIR domains of the TLR sequences from S. purpuratus and L. variegatus were used to construct the tree shown, which is a more detailed version of the tree in Figure 2. Bootstrap values greater than 50 are shown. Red indicates clades that are specific to S. purpuratus, blue clades contain only sequences from L. variegatus, and black clades contain sequences from both species. Each of the boxes (1–4) is shown in greater detail as indicated. The sequences are labeled by scaffold number and the position of the open reading frame (scaffold_start_stop). More information about the sequences can be found in Tables S1 and S2 in Supplementary Material. Subfamily designations are indicated on the right of each tree and correspond to those shown in Figure 2.

Mentions: Phylogeny of sea urchin TLR sequences. The TIR domains from the S. purpuratus (red branches) and L. variegatus (blue branches) TLRs were used to construct a neighbor-joining tree in MEGA 5.0 (Tamura et al., 2011) using Poisson corrected distances. Alignment positions containing gaps were eliminated completely from the analysis. Bootstrap values are shown and are based on 1000 replicates. Each of these clades is also reconstructed using other methods (maximum likelihood and maximum parsimony; data not shown). The subfamily for each clade is designated on the right. A more detailed version of this tree is shown in Figure A1 in Appendix.


Dynamic evolution of toll-like receptor multigene families in echinoderms.

Buckley KM, Rast JP - Front Immunol (2012)

Complete phylogeny of the sea urchin TLR sequences. The TIR domains of the TLR sequences from S. purpuratus and L. variegatus were used to construct the tree shown, which is a more detailed version of the tree in Figure 2. Bootstrap values greater than 50 are shown. Red indicates clades that are specific to S. purpuratus, blue clades contain only sequences from L. variegatus, and black clades contain sequences from both species. Each of the boxes (1–4) is shown in greater detail as indicated. The sequences are labeled by scaffold number and the position of the open reading frame (scaffold_start_stop). More information about the sequences can be found in Tables S1 and S2 in Supplementary Material. Subfamily designations are indicated on the right of each tree and correspond to those shown in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3367398&req=5

FA1: Complete phylogeny of the sea urchin TLR sequences. The TIR domains of the TLR sequences from S. purpuratus and L. variegatus were used to construct the tree shown, which is a more detailed version of the tree in Figure 2. Bootstrap values greater than 50 are shown. Red indicates clades that are specific to S. purpuratus, blue clades contain only sequences from L. variegatus, and black clades contain sequences from both species. Each of the boxes (1–4) is shown in greater detail as indicated. The sequences are labeled by scaffold number and the position of the open reading frame (scaffold_start_stop). More information about the sequences can be found in Tables S1 and S2 in Supplementary Material. Subfamily designations are indicated on the right of each tree and correspond to those shown in Figure 2.
Mentions: Phylogeny of sea urchin TLR sequences. The TIR domains from the S. purpuratus (red branches) and L. variegatus (blue branches) TLRs were used to construct a neighbor-joining tree in MEGA 5.0 (Tamura et al., 2011) using Poisson corrected distances. Alignment positions containing gaps were eliminated completely from the analysis. Bootstrap values are shown and are based on 1000 replicates. Each of these clades is also reconstructed using other methods (maximum likelihood and maximum parsimony; data not shown). The subfamily for each clade is designated on the right. A more detailed version of this tree is shown in Figure A1 in Appendix.

Bottom Line: Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences).The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level.These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Department of Immunology, Sunnybrook Research Institute, University of Toronto Toronto, ON, Canada.

ABSTRACT
The genome sequence of the purple sea urchin, Strongylocentrotus purpuratus, a large and long-lived invertebrate, provides a new perspective on animal immunity. Analysis of this genome uncovered a highly complex immune system in which the gene families that encode homologs of the pattern recognition receptors that form the core of vertebrate innate immunity are encoded in large multigene families. The sea urchin genome contains 253 Toll-like receptor (TLR) sequences, more than 200 Nod-like receptors and 1095 scavenger receptor cysteine-rich domains, a 10-fold expansion relative to vertebrates. Given their stereotypic protein structure and simple intron-exon architecture, the TLRs are the most tractable of these families for more detailed analysis. A role for these receptors in immune defense is suggested by their similarity to TLRs in other organisms, sequence diversity, and expression in immunologically active tissues, including phagocytes. The complexity of the sea urchin TLR multigene families is largely derived from expansions independent of those in vertebrates and protostomes, although a small family of TLRs with structure similar to that of Drosophila Toll can be traced to an ancient eumetazoan ancestor. Several other echinoderm sequences are now available, including Lytechinus variegatus, as well as partial sequences from two other sea urchin species. Here, we present an analysis of the invertebrate deuterostome TLRs with emphasis on the echinoderms. Representatives of most of the S. purpuratus TLR subfamilies and homologs of the mccTLR sequences are found in L. variegatus, although the L. variegatus TLR gene family is notably smaller (68 TLR sequences). The phylogeny of these genes within sea urchins highlights lineage-specific expansions at higher resolution than is evident at the phylum level. These analyses identify quickly evolving TLR subfamilies that are likely to have novel immune recognition functions and other, more stable, subfamilies that may function more similarly to those of vertebrates.

No MeSH data available.