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A cnidarian homologue of an insect gustatory receptor functions in developmental body patterning.

Saina M, Busengdal H, Sinigaglia C, Petrone L, Oliveri P, Rentzsch F, Benton R - Nat Commun (2015)

Bottom Line: Morpholino-mediated knockdown of NvecGrl1 causes developmental patterning defects of this region, leading to animals lacking the apical sensory organ.A deuterostome Grl from the sea urchin Strongylocentrotus purpuratus displays similar patterns of developmental expression.These results reveal an early evolutionary origin of the insect chemosensory receptor family and raise the possibility that their ancestral role was in embryonic development.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biology and Medicine, Center for Integrative Genomics, University of Lausanne, Genopode Building, CH-1015 Lausanne, Switzerland.

ABSTRACT
Insect gustatory and odorant receptors (GRs and ORs) form a superfamily of novel transmembrane proteins, which are expressed in chemosensory neurons that detect environmental stimuli. Here we identify homologues of GRs (Gustatory receptor-like (Grl) genes) in genomes across Protostomia, Deuterostomia and non-Bilateria. Surprisingly, two Grls in the cnidarian Nematostella vectensis, NvecGrl1 and NvecGrl2, are expressed early in development, in the blastula and gastrula, but not at later stages when a putative chemosensory organ forms. NvecGrl1 transcripts are detected around the aboral pole, considered the equivalent to the head-forming region of Bilateria. Morpholino-mediated knockdown of NvecGrl1 causes developmental patterning defects of this region, leading to animals lacking the apical sensory organ. A deuterostome Grl from the sea urchin Strongylocentrotus purpuratus displays similar patterns of developmental expression. These results reveal an early evolutionary origin of the insect chemosensory receptor family and raise the possibility that their ancestral role was in embryonic development.

No MeSH data available.


Phylogenetic analysis of Grl, GR and OR genesMaximum likelihood tree showing the relationships between select arthropod GRs/ORs, C. elegans GURs and all Grls (except the short sequence fragments predicted in P. miniata and A. millepora), colour-coded as in Fig. 1a. Drosophila Rhodopsins are included as an outgroup; although it remains unclear whether these two different families of heptahelical membrane proteins share a common ancestor, they clearly belong to a separate clade. For clarity, branches for large clades of D. melanogaster GRs/ORs or D. pulex GRs have been collapsed. The scale bar represents the number of amino acid substitutions per site.
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Figure 2: Phylogenetic analysis of Grl, GR and OR genesMaximum likelihood tree showing the relationships between select arthropod GRs/ORs, C. elegans GURs and all Grls (except the short sequence fragments predicted in P. miniata and A. millepora), colour-coded as in Fig. 1a. Drosophila Rhodopsins are included as an outgroup; although it remains unclear whether these two different families of heptahelical membrane proteins share a common ancestor, they clearly belong to a separate clade. For clarity, branches for large clades of D. melanogaster GRs/ORs or D. pulex GRs have been collapsed. The scale bar represents the number of amino acid substitutions per site.

Mentions: The overall sequence similarity of Grls and insect GRs (or ORs) is very low (~15-20% amino acid identity, similar to the minimum identity within the GR and OR families themselves1), with the highest similarity to the GR64a-f/GR61a clade of sugar-sensing receptors14. Phylogenetic analysis revealed no unambiguous orthologous relationships of Grls with any insect GR, or between Grls of different lophotrochozoan, deuterostome or non-bilaterian species (Fig. 2). Although the high divergence of these sequences precludes accurate reconstruction of their ancestry, many members of these repertoires appear to have formed by species-specific expansions (Fig. 2).


A cnidarian homologue of an insect gustatory receptor functions in developmental body patterning.

Saina M, Busengdal H, Sinigaglia C, Petrone L, Oliveri P, Rentzsch F, Benton R - Nat Commun (2015)

Phylogenetic analysis of Grl, GR and OR genesMaximum likelihood tree showing the relationships between select arthropod GRs/ORs, C. elegans GURs and all Grls (except the short sequence fragments predicted in P. miniata and A. millepora), colour-coded as in Fig. 1a. Drosophila Rhodopsins are included as an outgroup; although it remains unclear whether these two different families of heptahelical membrane proteins share a common ancestor, they clearly belong to a separate clade. For clarity, branches for large clades of D. melanogaster GRs/ORs or D. pulex GRs have been collapsed. The scale bar represents the number of amino acid substitutions per site.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4374167&req=5

Figure 2: Phylogenetic analysis of Grl, GR and OR genesMaximum likelihood tree showing the relationships between select arthropod GRs/ORs, C. elegans GURs and all Grls (except the short sequence fragments predicted in P. miniata and A. millepora), colour-coded as in Fig. 1a. Drosophila Rhodopsins are included as an outgroup; although it remains unclear whether these two different families of heptahelical membrane proteins share a common ancestor, they clearly belong to a separate clade. For clarity, branches for large clades of D. melanogaster GRs/ORs or D. pulex GRs have been collapsed. The scale bar represents the number of amino acid substitutions per site.
Mentions: The overall sequence similarity of Grls and insect GRs (or ORs) is very low (~15-20% amino acid identity, similar to the minimum identity within the GR and OR families themselves1), with the highest similarity to the GR64a-f/GR61a clade of sugar-sensing receptors14. Phylogenetic analysis revealed no unambiguous orthologous relationships of Grls with any insect GR, or between Grls of different lophotrochozoan, deuterostome or non-bilaterian species (Fig. 2). Although the high divergence of these sequences precludes accurate reconstruction of their ancestry, many members of these repertoires appear to have formed by species-specific expansions (Fig. 2).

Bottom Line: Morpholino-mediated knockdown of NvecGrl1 causes developmental patterning defects of this region, leading to animals lacking the apical sensory organ.A deuterostome Grl from the sea urchin Strongylocentrotus purpuratus displays similar patterns of developmental expression.These results reveal an early evolutionary origin of the insect chemosensory receptor family and raise the possibility that their ancestral role was in embryonic development.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biology and Medicine, Center for Integrative Genomics, University of Lausanne, Genopode Building, CH-1015 Lausanne, Switzerland.

ABSTRACT
Insect gustatory and odorant receptors (GRs and ORs) form a superfamily of novel transmembrane proteins, which are expressed in chemosensory neurons that detect environmental stimuli. Here we identify homologues of GRs (Gustatory receptor-like (Grl) genes) in genomes across Protostomia, Deuterostomia and non-Bilateria. Surprisingly, two Grls in the cnidarian Nematostella vectensis, NvecGrl1 and NvecGrl2, are expressed early in development, in the blastula and gastrula, but not at later stages when a putative chemosensory organ forms. NvecGrl1 transcripts are detected around the aboral pole, considered the equivalent to the head-forming region of Bilateria. Morpholino-mediated knockdown of NvecGrl1 causes developmental patterning defects of this region, leading to animals lacking the apical sensory organ. A deuterostome Grl from the sea urchin Strongylocentrotus purpuratus displays similar patterns of developmental expression. These results reveal an early evolutionary origin of the insect chemosensory receptor family and raise the possibility that their ancestral role was in embryonic development.

No MeSH data available.