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The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis.

Kamesh N, Aradhyam GK, Manoj N - BMC Evol. Biol. (2008)

Bottom Line: Our studies suggest that the ascidians contain the basic ancestral complement of vertebrate GPCR genes.This is evident at the subfamily level comparisons since Ciona GPCR sequences are significantly analogous to vertebrate GPCR subfamilies even while exhibiting Ciona specific genes.Our analysis provides a framework to perform future experimental and comparative studies to understand the roles of the ancestral chordate versions of GPCRs that predated the divergence of the urochordates and the vertebrates.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Bhupat and Jyothi Mehta School of Biosciences Building, Indian Institute of Technology Madras, Chennai 600036, India. kamesh@smail.iitm.ac.in

ABSTRACT

Background: G protein-coupled receptors (GPCRs) constitute a large family of integral transmembrane receptor proteins that play a central role in signal transduction in eukaryotes. The genome of the protochordate Ciona intestinalis has a compact size with an ancestral complement of many diversified gene families of vertebrates and is a good model system for studying protochordate to vertebrate diversification. An analysis of the Ciona repertoire of GPCRs from a comparative genomic perspective provides insight into the evolutionary origins of the GPCR signalling system in vertebrates.

Results: We have identified 169 gene products in the Ciona genome that code for putative GPCRs. Phylogenetic analyses reveal that Ciona GPCRs have homologous representatives from the five major GRAFS (Glutamate, Rhodopsin, Adhesion, Frizzled and Secretin) families concomitant with other vertebrate GPCR repertoires. Nearly 39% of Ciona GPCRs have unambiguous orthologs of vertebrate GPCR families, as defined for the human, mouse, puffer fish and chicken genomes. The Rhodopsin family accounts for ~68% of the Ciona GPCR repertoire wherein the LGR-like subfamily exhibits a lineage specific gene expansion of a group of receptors that possess a novel domain organisation hitherto unobserved in metazoan genomes.

Conclusion: Comparison of GPCRs in Ciona to that in human reveals a high level of orthology of a protochordate repertoire with that of vertebrate GPCRs. Our studies suggest that the ascidians contain the basic ancestral complement of vertebrate GPCR genes. This is evident at the subfamily level comparisons since Ciona GPCR sequences are significantly analogous to vertebrate GPCR subfamilies even while exhibiting Ciona specific genes. Our analysis provides a framework to perform future experimental and comparative studies to understand the roles of the ancestral chordate versions of GPCRs that predated the divergence of the urochordates and the vertebrates.

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Phylogenetic relationship between GPCRs in Ciona and other genomes. The figure illustrates the presence of representatives of Glutamate, Rhodopsin, Adhesion, Frizzled, and Secretin family members in Ciona. Two sequences that are homologous to cAMP and Methuselah GPCRs are also represented. The position of the Rhodopsin family was established by including 15 receptors from the Rhodopsin family. The divergent, "Other/Unclassified" GPCRs known to lack reliable homologs from other species or which are fast evolving, are excluded from the final representation. For display reasons bootstrap values are not represented in the figure. Instead, the corresponding tree file in standard Newick format is provided [Additional data file 5]. For Figure 2, and Figures 3, 5 and 6, the multiple sequence alignment was built taking into account terminally truncated TM spanning regions, while the consensus phylogenetic tree was calculated using NJ method on 1000 replicas of the dataset. Ciona GPCR taxons are represented in numerals as per numbering in Additional data file 2. Abbreviations for known GPCRs are as described in [5, 6, 8, 9] and based on Swiss-prot IDs. Ciona GPCRs that deviate from the predicted 7TM structure are marked using a '#' symbol.
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Figure 2: Phylogenetic relationship between GPCRs in Ciona and other genomes. The figure illustrates the presence of representatives of Glutamate, Rhodopsin, Adhesion, Frizzled, and Secretin family members in Ciona. Two sequences that are homologous to cAMP and Methuselah GPCRs are also represented. The position of the Rhodopsin family was established by including 15 receptors from the Rhodopsin family. The divergent, "Other/Unclassified" GPCRs known to lack reliable homologs from other species or which are fast evolving, are excluded from the final representation. For display reasons bootstrap values are not represented in the figure. Instead, the corresponding tree file in standard Newick format is provided [Additional data file 5]. For Figure 2, and Figures 3, 5 and 6, the multiple sequence alignment was built taking into account terminally truncated TM spanning regions, while the consensus phylogenetic tree was calculated using NJ method on 1000 replicas of the dataset. Ciona GPCR taxons are represented in numerals as per numbering in Additional data file 2. Abbreviations for known GPCRs are as described in [5, 6, 8, 9] and based on Swiss-prot IDs. Ciona GPCRs that deviate from the predicted 7TM structure are marked using a '#' symbol.

Mentions: HMM based genome-wide GPCR surveys have been previously carried out in 13 genomes, including that of Ciona [13]. While this HMM based study provided a broad overview of the repertoire of GPCRs in the Ciona genome, an independent large-scale molecular phylogenetic treatment with respect to the tunicate GPCRs has not emerged and awaits investigation. GPCR features reflecting highly specialized ascidian specific biology are usually evident from such phylogenetic analysis. Of particular interest are whole-genome orthology and paralogy comparisons that are not evident from the previous HMM based search approach [13]. A table describing orthology and paralogy observations identified in Ciona GPCRs through our comparative genomic studies is provided [Additional data file 2: sheet 1]. Our phylogenetic study also provides the first ever insight into Ciona specific protochordate GPCR repertoire apart from vindicating the presence of the five major GRAFS families (Figure 2). Homologs of the chemosensory GPCRs from nematodes, plant GPCRs, Yeast Pheromone receptors, gustatory and olfactory receptors from insects were not identified. 66 clear orthologs of human GPCRs could be identified in Ciona based on phylogenetic analysis.


The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis.

Kamesh N, Aradhyam GK, Manoj N - BMC Evol. Biol. (2008)

Phylogenetic relationship between GPCRs in Ciona and other genomes. The figure illustrates the presence of representatives of Glutamate, Rhodopsin, Adhesion, Frizzled, and Secretin family members in Ciona. Two sequences that are homologous to cAMP and Methuselah GPCRs are also represented. The position of the Rhodopsin family was established by including 15 receptors from the Rhodopsin family. The divergent, "Other/Unclassified" GPCRs known to lack reliable homologs from other species or which are fast evolving, are excluded from the final representation. For display reasons bootstrap values are not represented in the figure. Instead, the corresponding tree file in standard Newick format is provided [Additional data file 5]. For Figure 2, and Figures 3, 5 and 6, the multiple sequence alignment was built taking into account terminally truncated TM spanning regions, while the consensus phylogenetic tree was calculated using NJ method on 1000 replicas of the dataset. Ciona GPCR taxons are represented in numerals as per numbering in Additional data file 2. Abbreviations for known GPCRs are as described in [5, 6, 8, 9] and based on Swiss-prot IDs. Ciona GPCRs that deviate from the predicted 7TM structure are marked using a '#' symbol.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2396169&req=5

Figure 2: Phylogenetic relationship between GPCRs in Ciona and other genomes. The figure illustrates the presence of representatives of Glutamate, Rhodopsin, Adhesion, Frizzled, and Secretin family members in Ciona. Two sequences that are homologous to cAMP and Methuselah GPCRs are also represented. The position of the Rhodopsin family was established by including 15 receptors from the Rhodopsin family. The divergent, "Other/Unclassified" GPCRs known to lack reliable homologs from other species or which are fast evolving, are excluded from the final representation. For display reasons bootstrap values are not represented in the figure. Instead, the corresponding tree file in standard Newick format is provided [Additional data file 5]. For Figure 2, and Figures 3, 5 and 6, the multiple sequence alignment was built taking into account terminally truncated TM spanning regions, while the consensus phylogenetic tree was calculated using NJ method on 1000 replicas of the dataset. Ciona GPCR taxons are represented in numerals as per numbering in Additional data file 2. Abbreviations for known GPCRs are as described in [5, 6, 8, 9] and based on Swiss-prot IDs. Ciona GPCRs that deviate from the predicted 7TM structure are marked using a '#' symbol.
Mentions: HMM based genome-wide GPCR surveys have been previously carried out in 13 genomes, including that of Ciona [13]. While this HMM based study provided a broad overview of the repertoire of GPCRs in the Ciona genome, an independent large-scale molecular phylogenetic treatment with respect to the tunicate GPCRs has not emerged and awaits investigation. GPCR features reflecting highly specialized ascidian specific biology are usually evident from such phylogenetic analysis. Of particular interest are whole-genome orthology and paralogy comparisons that are not evident from the previous HMM based search approach [13]. A table describing orthology and paralogy observations identified in Ciona GPCRs through our comparative genomic studies is provided [Additional data file 2: sheet 1]. Our phylogenetic study also provides the first ever insight into Ciona specific protochordate GPCR repertoire apart from vindicating the presence of the five major GRAFS families (Figure 2). Homologs of the chemosensory GPCRs from nematodes, plant GPCRs, Yeast Pheromone receptors, gustatory and olfactory receptors from insects were not identified. 66 clear orthologs of human GPCRs could be identified in Ciona based on phylogenetic analysis.

Bottom Line: Our studies suggest that the ascidians contain the basic ancestral complement of vertebrate GPCR genes.This is evident at the subfamily level comparisons since Ciona GPCR sequences are significantly analogous to vertebrate GPCR subfamilies even while exhibiting Ciona specific genes.Our analysis provides a framework to perform future experimental and comparative studies to understand the roles of the ancestral chordate versions of GPCRs that predated the divergence of the urochordates and the vertebrates.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biotechnology, Bhupat and Jyothi Mehta School of Biosciences Building, Indian Institute of Technology Madras, Chennai 600036, India. kamesh@smail.iitm.ac.in

ABSTRACT

Background: G protein-coupled receptors (GPCRs) constitute a large family of integral transmembrane receptor proteins that play a central role in signal transduction in eukaryotes. The genome of the protochordate Ciona intestinalis has a compact size with an ancestral complement of many diversified gene families of vertebrates and is a good model system for studying protochordate to vertebrate diversification. An analysis of the Ciona repertoire of GPCRs from a comparative genomic perspective provides insight into the evolutionary origins of the GPCR signalling system in vertebrates.

Results: We have identified 169 gene products in the Ciona genome that code for putative GPCRs. Phylogenetic analyses reveal that Ciona GPCRs have homologous representatives from the five major GRAFS (Glutamate, Rhodopsin, Adhesion, Frizzled and Secretin) families concomitant with other vertebrate GPCR repertoires. Nearly 39% of Ciona GPCRs have unambiguous orthologs of vertebrate GPCR families, as defined for the human, mouse, puffer fish and chicken genomes. The Rhodopsin family accounts for ~68% of the Ciona GPCR repertoire wherein the LGR-like subfamily exhibits a lineage specific gene expansion of a group of receptors that possess a novel domain organisation hitherto unobserved in metazoan genomes.

Conclusion: Comparison of GPCRs in Ciona to that in human reveals a high level of orthology of a protochordate repertoire with that of vertebrate GPCRs. Our studies suggest that the ascidians contain the basic ancestral complement of vertebrate GPCR genes. This is evident at the subfamily level comparisons since Ciona GPCR sequences are significantly analogous to vertebrate GPCR subfamilies even while exhibiting Ciona specific genes. Our analysis provides a framework to perform future experimental and comparative studies to understand the roles of the ancestral chordate versions of GPCRs that predated the divergence of the urochordates and the vertebrates.

Show MeSH
Related in: MedlinePlus