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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.


Regulation of N. vectensis Grl1 expression by the apical patterning network(a) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecSix3/6 morpholino oligonucleotides. Quantification of the phenotypes is shown below. Note that NvecGrl1 transcripts are relatively weakly detected and a fraction of control morpholino injected animals did not exhibit staining. The n is shown in white within each bar in this and all equivalent graphs.(b) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa1 morpholino oligonucleotides. Quantification of the phenotypes is shown below.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa2 morpholino oligonucleotides. In NvecFgf2 morphants, note the precocious formation and larger size of the ring of NvecGrl1 transcripts around the aboral pole (compare with Fig. 3e). Quantification of the phenotypes is shown below. Scale bars in (a c) = 100 μm.
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Figure 4: Regulation of N. vectensis Grl1 expression by the apical patterning network(a) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecSix3/6 morpholino oligonucleotides. Quantification of the phenotypes is shown below. Note that NvecGrl1 transcripts are relatively weakly detected and a fraction of control morpholino injected animals did not exhibit staining. The n is shown in white within each bar in this and all equivalent graphs.(b) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa1 morpholino oligonucleotides. Quantification of the phenotypes is shown below.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa2 morpholino oligonucleotides. In NvecFgf2 morphants, note the precocious formation and larger size of the ring of NvecGrl1 transcripts around the aboral pole (compare with Fig. 3e). Quantification of the phenotypes is shown below. Scale bars in (a c) = 100 μm.

Mentions: Several transcription factors and signalling molecules that are expressed in the aboral region and required for apical organ formation in N. vectensis have been identified36. For example, the homeodomain transcription factor NvecSix3/6 is an important determinant of the aboral territory, where it initiates an autoregulatory loop of Fibroblast Growth Factor (FGF) signalling to pattern this domain36. To determine if NvecGrl1 aboral expression is regulated by these factors, we performed RNA in situ hybridisation on zygotes injected with morpholino oligonucleotides (morphants) designed to block translation of these genes. In NvecSix3/6 morphants, NvecGrl1 aboral expression is reduced or absent in gastrula embryos compared to control morphants, similar to other markers of this domain36 (Fig. 4a), suggesting that NvecGrl1 functions downstream of this transcription factor.


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)

Regulation of N. vectensis Grl1 expression by the apical patterning network(a) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecSix3/6 morpholino oligonucleotides. Quantification of the phenotypes is shown below. Note that NvecGrl1 transcripts are relatively weakly detected and a fraction of control morpholino injected animals did not exhibit staining. The n is shown in white within each bar in this and all equivalent graphs.(b) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa1 morpholino oligonucleotides. Quantification of the phenotypes is shown below.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa2 morpholino oligonucleotides. In NvecFgf2 morphants, note the precocious formation and larger size of the ring of NvecGrl1 transcripts around the aboral pole (compare with Fig. 3e). Quantification of the phenotypes is shown below. Scale bars in (a c) = 100 μm.
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Related In: Results  -  Collection

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Figure 4: Regulation of N. vectensis Grl1 expression by the apical patterning network(a) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecSix3/6 morpholino oligonucleotides. Quantification of the phenotypes is shown below. Note that NvecGrl1 transcripts are relatively weakly detected and a fraction of control morpholino injected animals did not exhibit staining. The n is shown in white within each bar in this and all equivalent graphs.(b) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa1 morpholino oligonucleotides. Quantification of the phenotypes is shown below.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis embryos injected with either control or NvecFgfa2 morpholino oligonucleotides. In NvecFgf2 morphants, note the precocious formation and larger size of the ring of NvecGrl1 transcripts around the aboral pole (compare with Fig. 3e). Quantification of the phenotypes is shown below. Scale bars in (a c) = 100 μm.
Mentions: Several transcription factors and signalling molecules that are expressed in the aboral region and required for apical organ formation in N. vectensis have been identified36. For example, the homeodomain transcription factor NvecSix3/6 is an important determinant of the aboral territory, where it initiates an autoregulatory loop of Fibroblast Growth Factor (FGF) signalling to pattern this domain36. To determine if NvecGrl1 aboral expression is regulated by these factors, we performed RNA in situ hybridisation on zygotes injected with morpholino oligonucleotides (morphants) designed to block translation of these genes. In NvecSix3/6 morphants, NvecGrl1 aboral expression is reduced or absent in gastrula embryos compared to control morphants, similar to other markers of this domain36 (Fig. 4a), suggesting that NvecGrl1 functions downstream of this transcription factor.

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.