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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.


Identification of Gr-like (Grl) genes(a) Summary of the GR/Grl repertoires identified in the genomes of selected arthropods (pink), non-arthropod Ecdysozoa (dark green), Lophotrochozoa (light green), Deuterostomia (blue) and non-Bilateria (yellow). An unscaled tree showing the phylogenetic relationships between these species is illustrated on the left; relationships among the different non-bilaterian phyla is unresolved, with the exception of the Cnidaria, which are the closest sister group to Bilateria62. Related genes were identified in multiple species of nematode worms but, for simplicity, only C. elegans is shown.(b) Computational predictions of the number of transmembrane domains found in D. melanogaster GRs and ORs (top) and Grls (bottom). Grl sequence fragments (lacking start/stop codons) were excluded from this analysis.(c) Alignment of the C-terminal regions of select insect GRs and ORs, C. elegans GURs and Grls. Predicted transmembrane (TM) domains are indicated with horizontal lines. The asterisk marks a conserved tyrosine residue important for ion conduction in insect ORs31. The arrowheads below the alignment indicate the positions of three phase 0 ancestral GR introns (inferred from analysis of D. melanogaster GRs and ORs1) that are conserved in Grls: intron I is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CeleGUR2, CeleGUR3, CtelGrl2, LgigGrl3; intron II is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CtelGrl2, and LgigGrl3. Intron III is conserved in all sequences.
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Figure 1: Identification of Gr-like (Grl) genes(a) Summary of the GR/Grl repertoires identified in the genomes of selected arthropods (pink), non-arthropod Ecdysozoa (dark green), Lophotrochozoa (light green), Deuterostomia (blue) and non-Bilateria (yellow). An unscaled tree showing the phylogenetic relationships between these species is illustrated on the left; relationships among the different non-bilaterian phyla is unresolved, with the exception of the Cnidaria, which are the closest sister group to Bilateria62. Related genes were identified in multiple species of nematode worms but, for simplicity, only C. elegans is shown.(b) Computational predictions of the number of transmembrane domains found in D. melanogaster GRs and ORs (top) and Grls (bottom). Grl sequence fragments (lacking start/stop codons) were excluded from this analysis.(c) Alignment of the C-terminal regions of select insect GRs and ORs, C. elegans GURs and Grls. Predicted transmembrane (TM) domains are indicated with horizontal lines. The asterisk marks a conserved tyrosine residue important for ion conduction in insect ORs31. The arrowheads below the alignment indicate the positions of three phase 0 ancestral GR introns (inferred from analysis of D. melanogaster GRs and ORs1) that are conserved in Grls: intron I is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CeleGUR2, CeleGUR3, CtelGrl2, LgigGrl3; intron II is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CtelGrl2, and LgigGrl3. Intron III is conserved in all sequences.

Mentions: We performed TBLASTN and PSI-BLAST searches using insect GRs and ORs as queries to identify putative homologous genes within non-insect genomes available at NCBI and other public genome and Expressed Sequence Tag (EST) databases (see Methods) (Figure 1a, Supplementary Table 1 and Supplementary Data 1). Within Protostomia, these searches recovered the previously described GRs of the crustacean Daphnia pulex (water flea)17 and the gustatory related (gur) and serpentine receptor class R (srr) genes of C. elegans1, 18, 19 and other nematodes. Beyond Ecdysozoa, we identified what we term GR-like (Grl) genes in Lophotrochozoa, including the annelids Capitella teleta (polychaete worm) and Helobdella robusta (freshwater leech)20, and the molluscs, Lottia gigantea (owl limpet)20, Crassostrea gigas (Pacific oyster)21 and Aplysia californica (sea slug). We also found homologous genes in Deuterostomia, including the hemichordate Saccoglossus kowalevskii (acorn worm) and several echinoderms, including the sea urchin Strongylocentrotus purpuratus22, but not in any chordate (Fig. 1a). Finally, we identified a small number of Grl genes in non-bilaterian species, including Cnidaria, such as the sea anemone Nematostella vectensis23 (independently noted in another study24) and the corals Acropora digitifera25 and Acropora millepora, and the placozoan Trichoplax adhaerens26. No sequences were recovered, however, from the genomes of another cnidarian, Hydra magnipapillata, the ctenophores Mnemiopsis leidyi27 and Pleurobrachia bachei28, or the sponges Amphimedon queenslandica29 and Oscarella carmela30. No fungal, unicellular eukaryotic or prokaryotic genomes contained identifiable Grls (Fig. 1a).


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)

Identification of Gr-like (Grl) genes(a) Summary of the GR/Grl repertoires identified in the genomes of selected arthropods (pink), non-arthropod Ecdysozoa (dark green), Lophotrochozoa (light green), Deuterostomia (blue) and non-Bilateria (yellow). An unscaled tree showing the phylogenetic relationships between these species is illustrated on the left; relationships among the different non-bilaterian phyla is unresolved, with the exception of the Cnidaria, which are the closest sister group to Bilateria62. Related genes were identified in multiple species of nematode worms but, for simplicity, only C. elegans is shown.(b) Computational predictions of the number of transmembrane domains found in D. melanogaster GRs and ORs (top) and Grls (bottom). Grl sequence fragments (lacking start/stop codons) were excluded from this analysis.(c) Alignment of the C-terminal regions of select insect GRs and ORs, C. elegans GURs and Grls. Predicted transmembrane (TM) domains are indicated with horizontal lines. The asterisk marks a conserved tyrosine residue important for ion conduction in insect ORs31. The arrowheads below the alignment indicate the positions of three phase 0 ancestral GR introns (inferred from analysis of D. melanogaster GRs and ORs1) that are conserved in Grls: intron I is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CeleGUR2, CeleGUR3, CtelGrl2, LgigGrl3; intron II is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CtelGrl2, and LgigGrl3. Intron III is conserved in all sequences.
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Figure 1: Identification of Gr-like (Grl) genes(a) Summary of the GR/Grl repertoires identified in the genomes of selected arthropods (pink), non-arthropod Ecdysozoa (dark green), Lophotrochozoa (light green), Deuterostomia (blue) and non-Bilateria (yellow). An unscaled tree showing the phylogenetic relationships between these species is illustrated on the left; relationships among the different non-bilaterian phyla is unresolved, with the exception of the Cnidaria, which are the closest sister group to Bilateria62. Related genes were identified in multiple species of nematode worms but, for simplicity, only C. elegans is shown.(b) Computational predictions of the number of transmembrane domains found in D. melanogaster GRs and ORs (top) and Grls (bottom). Grl sequence fragments (lacking start/stop codons) were excluded from this analysis.(c) Alignment of the C-terminal regions of select insect GRs and ORs, C. elegans GURs and Grls. Predicted transmembrane (TM) domains are indicated with horizontal lines. The asterisk marks a conserved tyrosine residue important for ion conduction in insect ORs31. The arrowheads below the alignment indicate the positions of three phase 0 ancestral GR introns (inferred from analysis of D. melanogaster GRs and ORs1) that are conserved in Grls: intron I is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CeleGUR2, CeleGUR3, CtelGrl2, LgigGrl3; intron II is conserved in phase and position in NvecGrl1, NvecGrl2, TadhGrl2, SpurGrl1, CtelGrl2, and LgigGrl3. Intron III is conserved in all sequences.
Mentions: We performed TBLASTN and PSI-BLAST searches using insect GRs and ORs as queries to identify putative homologous genes within non-insect genomes available at NCBI and other public genome and Expressed Sequence Tag (EST) databases (see Methods) (Figure 1a, Supplementary Table 1 and Supplementary Data 1). Within Protostomia, these searches recovered the previously described GRs of the crustacean Daphnia pulex (water flea)17 and the gustatory related (gur) and serpentine receptor class R (srr) genes of C. elegans1, 18, 19 and other nematodes. Beyond Ecdysozoa, we identified what we term GR-like (Grl) genes in Lophotrochozoa, including the annelids Capitella teleta (polychaete worm) and Helobdella robusta (freshwater leech)20, and the molluscs, Lottia gigantea (owl limpet)20, Crassostrea gigas (Pacific oyster)21 and Aplysia californica (sea slug). We also found homologous genes in Deuterostomia, including the hemichordate Saccoglossus kowalevskii (acorn worm) and several echinoderms, including the sea urchin Strongylocentrotus purpuratus22, but not in any chordate (Fig. 1a). Finally, we identified a small number of Grl genes in non-bilaterian species, including Cnidaria, such as the sea anemone Nematostella vectensis23 (independently noted in another study24) and the corals Acropora digitifera25 and Acropora millepora, and the placozoan Trichoplax adhaerens26. No sequences were recovered, however, from the genomes of another cnidarian, Hydra magnipapillata, the ctenophores Mnemiopsis leidyi27 and Pleurobrachia bachei28, or the sponges Amphimedon queenslandica29 and Oscarella carmela30. No fungal, unicellular eukaryotic or prokaryotic genomes contained identifiable Grls (Fig. 1a).

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.