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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.


Early developmental expression of an S. purpuratus Grl(a) Schematic of the life cycle of the sea urchin S. purpuratus.(b) Quantitative RT-PCR analysis of the temporal expression of the five SpurGrl genes during nine developmental time points. Data are represented as number of transcripts per embryo and represent the average of four technical replicates in each of two independent biological replicate samples (see Supplementary Table 3).(c) RNA in situ hybridisation using a riboprobe against SpurGrl1 on whole mount S. purpuratus of five developmental stages. All the embryos represent lateral views: as indicated in the schematic, the oral ectoderm is on the left and the apical domain on the top in gastrula and pluteus specimens. The arrows mark the expression of SpurGrl1 in the apical domain (where the apical organ will form), while the arrowheads mark a pair of presumptive neurosecretory cells in the oral ectoderm. Scale bars = 20 μm.
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Figure 6: Early developmental expression of an S. purpuratus Grl(a) Schematic of the life cycle of the sea urchin S. purpuratus.(b) Quantitative RT-PCR analysis of the temporal expression of the five SpurGrl genes during nine developmental time points. Data are represented as number of transcripts per embryo and represent the average of four technical replicates in each of two independent biological replicate samples (see Supplementary Table 3).(c) RNA in situ hybridisation using a riboprobe against SpurGrl1 on whole mount S. purpuratus of five developmental stages. All the embryos represent lateral views: as indicated in the schematic, the oral ectoderm is on the left and the apical domain on the top in gastrula and pluteus specimens. The arrows mark the expression of SpurGrl1 in the apical domain (where the apical organ will form), while the arrowheads mark a pair of presumptive neurosecretory cells in the oral ectoderm. Scale bars = 20 μm.

Mentions: To determine whether the early developmental expression of Grl genes is conserved in Deuterostomia, we used qPCR to analyse transcript levels of the five Grls of the echinoderm S. purpuratus during embryonic stages (Fig. 6a). Notably, SpurGrl1, which is the most similar sea urchin Grl to NvecGrl1 (Fig. 2), was detected during early development (Fig. 6b and Supplementary Table 3): the highest expression of SpurGrl1 was at the blastula stage, but it remained at elevated levels in the gastrula and later embryonic developmental stages. These qPCR data are in agreement with quantitative developmental transcriptome data (Supplementary Fig. 3a)40. The other four SpurGrls were expressed at only very low levels during developmental stages (Fig. 6b), but transcripts could be readily amplified for all SpurGrls, except SpurGrl3, from adult neural tissue (Supplementary Fig. 3b). These observations suggest that SpurGrl1 has a unique function during embryonic development.


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)

Early developmental expression of an S. purpuratus Grl(a) Schematic of the life cycle of the sea urchin S. purpuratus.(b) Quantitative RT-PCR analysis of the temporal expression of the five SpurGrl genes during nine developmental time points. Data are represented as number of transcripts per embryo and represent the average of four technical replicates in each of two independent biological replicate samples (see Supplementary Table 3).(c) RNA in situ hybridisation using a riboprobe against SpurGrl1 on whole mount S. purpuratus of five developmental stages. All the embryos represent lateral views: as indicated in the schematic, the oral ectoderm is on the left and the apical domain on the top in gastrula and pluteus specimens. The arrows mark the expression of SpurGrl1 in the apical domain (where the apical organ will form), while the arrowheads mark a pair of presumptive neurosecretory cells in the oral ectoderm. Scale bars = 20 μm.
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Related In: Results  -  Collection

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Figure 6: Early developmental expression of an S. purpuratus Grl(a) Schematic of the life cycle of the sea urchin S. purpuratus.(b) Quantitative RT-PCR analysis of the temporal expression of the five SpurGrl genes during nine developmental time points. Data are represented as number of transcripts per embryo and represent the average of four technical replicates in each of two independent biological replicate samples (see Supplementary Table 3).(c) RNA in situ hybridisation using a riboprobe against SpurGrl1 on whole mount S. purpuratus of five developmental stages. All the embryos represent lateral views: as indicated in the schematic, the oral ectoderm is on the left and the apical domain on the top in gastrula and pluteus specimens. The arrows mark the expression of SpurGrl1 in the apical domain (where the apical organ will form), while the arrowheads mark a pair of presumptive neurosecretory cells in the oral ectoderm. Scale bars = 20 μm.
Mentions: To determine whether the early developmental expression of Grl genes is conserved in Deuterostomia, we used qPCR to analyse transcript levels of the five Grls of the echinoderm S. purpuratus during embryonic stages (Fig. 6a). Notably, SpurGrl1, which is the most similar sea urchin Grl to NvecGrl1 (Fig. 2), was detected during early development (Fig. 6b and Supplementary Table 3): the highest expression of SpurGrl1 was at the blastula stage, but it remained at elevated levels in the gastrula and later embryonic developmental stages. These qPCR data are in agreement with quantitative developmental transcriptome data (Supplementary Fig. 3a)40. The other four SpurGrls were expressed at only very low levels during developmental stages (Fig. 6b), but transcripts could be readily amplified for all SpurGrls, except SpurGrl3, from adult neural tissue (Supplementary Fig. 3b). These observations suggest that SpurGrl1 has a unique function during embryonic development.

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.