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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.


N. vectensis Grls are expressed during early development(a) Schematic of the life cycle of the sea anemone N. vectensis. Dark grey shading in blastula, gastrula and early planula stages indicates the endoderm.(b) Quantitative RT-PCR analysis of the temporal expression of NvecGrl1 and NvecGrl2 during nine developmental time-points. Data from three biological replicate samples (mean ± s.e.m.) are shown.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at three developmental stages. Lateral views, with the arboral side on the left, are shown for all specimens in this and subsequent figures, unless otherwise noted.(d) Two-colour RNA in situ hybridisation using riboprobes against NvecGrl1 (light blue) and NvecFgfa1 (dark blue) on whole mount N. vectensis embryos.(e) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at two developmental stages showing an apical view, which reveal the formation of a ring-like distribution of transcripts at the planula stage. The apical organ forms from the unstained cells inside the ring (white arrow). Scale bars in (c-e) = 100 μm.
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Figure 3: N. vectensis Grls are expressed during early development(a) Schematic of the life cycle of the sea anemone N. vectensis. Dark grey shading in blastula, gastrula and early planula stages indicates the endoderm.(b) Quantitative RT-PCR analysis of the temporal expression of NvecGrl1 and NvecGrl2 during nine developmental time-points. Data from three biological replicate samples (mean ± s.e.m.) are shown.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at three developmental stages. Lateral views, with the arboral side on the left, are shown for all specimens in this and subsequent figures, unless otherwise noted.(d) Two-colour RNA in situ hybridisation using riboprobes against NvecGrl1 (light blue) and NvecFgfa1 (dark blue) on whole mount N. vectensis embryos.(e) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at two developmental stages showing an apical view, which reveal the formation of a ring-like distribution of transcripts at the planula stage. The apical organ forms from the unstained cells inside the ring (white arrow). Scale bars in (c-e) = 100 μm.

Mentions: To investigate the role of Grls in non-Arthropoda, we focused in this study on the cnidarian N. vectensis (here abbreviated Nvec), which is amenable to gene expression and functional analyses. Moreover, the development and anatomy of this organism are relatively well-described, and a presumed chemosensory structure, the apical organ, has been identified (Fig. 3a)32, 33. N. vectensis development proceeds through a coeloblastula stage to gastrulation, which occurs mainly by invagination34, 35. After gastrulation, the embryo emerges from the egg jelly as a free-swimming planula, which moves by ciliary beating with the apical sense organ pointing forward. Subsequently, the planula transforms (“metamorphoses”) into a sessile polyp, which starts feeding after formation of the tentacles that surround the single opening of the animal (Fig. 3a).


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)

N. vectensis Grls are expressed during early development(a) Schematic of the life cycle of the sea anemone N. vectensis. Dark grey shading in blastula, gastrula and early planula stages indicates the endoderm.(b) Quantitative RT-PCR analysis of the temporal expression of NvecGrl1 and NvecGrl2 during nine developmental time-points. Data from three biological replicate samples (mean ± s.e.m.) are shown.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at three developmental stages. Lateral views, with the arboral side on the left, are shown for all specimens in this and subsequent figures, unless otherwise noted.(d) Two-colour RNA in situ hybridisation using riboprobes against NvecGrl1 (light blue) and NvecFgfa1 (dark blue) on whole mount N. vectensis embryos.(e) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at two developmental stages showing an apical view, which reveal the formation of a ring-like distribution of transcripts at the planula stage. The apical organ forms from the unstained cells inside the ring (white arrow). Scale bars in (c-e) = 100 μm.
© Copyright Policy
Related In: Results  -  Collection

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Figure 3: N. vectensis Grls are expressed during early development(a) Schematic of the life cycle of the sea anemone N. vectensis. Dark grey shading in blastula, gastrula and early planula stages indicates the endoderm.(b) Quantitative RT-PCR analysis of the temporal expression of NvecGrl1 and NvecGrl2 during nine developmental time-points. Data from three biological replicate samples (mean ± s.e.m.) are shown.(c) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at three developmental stages. Lateral views, with the arboral side on the left, are shown for all specimens in this and subsequent figures, unless otherwise noted.(d) Two-colour RNA in situ hybridisation using riboprobes against NvecGrl1 (light blue) and NvecFgfa1 (dark blue) on whole mount N. vectensis embryos.(e) RNA in situ hybridisation using a riboprobe against NvecGrl1 on whole mount N. vectensis at two developmental stages showing an apical view, which reveal the formation of a ring-like distribution of transcripts at the planula stage. The apical organ forms from the unstained cells inside the ring (white arrow). Scale bars in (c-e) = 100 μm.
Mentions: To investigate the role of Grls in non-Arthropoda, we focused in this study on the cnidarian N. vectensis (here abbreviated Nvec), which is amenable to gene expression and functional analyses. Moreover, the development and anatomy of this organism are relatively well-described, and a presumed chemosensory structure, the apical organ, has been identified (Fig. 3a)32, 33. N. vectensis development proceeds through a coeloblastula stage to gastrulation, which occurs mainly by invagination34, 35. After gastrulation, the embryo emerges from the egg jelly as a free-swimming planula, which moves by ciliary beating with the apical sense organ pointing forward. Subsequently, the planula transforms (“metamorphoses”) into a sessile polyp, which starts feeding after formation of the tentacles that surround the single opening of the animal (Fig. 3a).

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.