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Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development.

Nakanishi N, Camara AC, Yuan DC, Gold DA, Jacobs DK - PLoS ONE (2015)

Bottom Line: Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia.Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa.The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, UCLA, Los Angeles, California, United States of America.

ABSTRACT
In Bilateria, Pax6, Six, Eya and Dach families of transcription factors underlie the development and evolution of morphologically and phyletically distinct eyes, including the compound eyes in Drosophila and the camera-type eyes in vertebrates, indicating that bilaterian eyes evolved under the strong influence of ancestral developmental gene regulation. However the conservation in eye developmental genetics deeper in the Eumetazoa, and the origin of the conserved gene regulatory apparatus controlling eye development remain unclear due to limited comparative developmental data from Cnidaria. Here we show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis (so)/six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B). In addition, the so and eya co-expression domain encompasses the region of active cell proliferation, neurogenesis, and mechanoreceptor development in rhopalia. Consistent with the role of so and eya in rhopalial development, developmental transcriptome data across Aurelia life cycle stages show upregulation of so and eya, but not optix or pax (A&B), during medusa formation. Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia. Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa. The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

No MeSH data available.


Related in: MedlinePlus

AurOptix, AurPaxA and AurPaxB mRNAs are differentially expressed outside the domain of eye development.Aurelia sp.1 free-swimming ephyrae were labeled with antisense riboprobes against AurOptix (A-C), AurPaxA (D-F), and AurPaxB (G-I). A is a lateral view of an ephyra with the mouth/manubrium facing upwards. Black arrowheads show rhopalia. Note strong localization of AurOptix transcripts in the endoderm of the arms (en). In C and F, the rhopalia were also labeled with antibodies against acetylated ∂-tubulin (acTub) and FMRFamide-like neuropeptides (FMRF; in F). B, C, E, G and H, and an inset in A, are oral views with the rhopalial distal ends pointed upwards. D is an aboral view with the rhopalial distal end pointed upwards. F and I are lateral views with the rhopalial distal ends pointed to the left. B: a medial optical section of a rhopalium, showing endodermal AurOptix expression. An inset shows AurOptix-expressing endodermal pigment cells (arrowheads) in the gastrovascular canal (gc). C: a medial confocal section of a rhopalium showing AurOptix-expressing cells morphologically identifiable as a sensory cell (upper arrowhead) and ganglion cells (lower arrowhead) (cf. [18]). An inset is the section at the plane of the developing photosensory domain (boxed), showing little AurOptix expression. D: an optical section through the exumbrellar (aboral) ectoderm, showing strong AurPaxA expression in individual cells (arrowheads). E: a medial optical section of a rhopalium, showing no detectable levels of AurPaxA expression. F: a sagital confocal section of a rhopalium and the overlying exumbrellar ectoderm showing that AurPaxA-expressing cells are located at the base of the aboral ectoderm (arrowhead) in close association with the FMRFamide-immunoreactive neuronal network (FMRF). G: an oral view of a rhopalar arm. AurPaxB transcript localization in the basal region of a rhopalium is detectable at low levels (arrowhead). H: a medial optical section of a rhopalium, showing AurPaxB expression in the ectoderm (ec) of the proximal region of the rhopalium (arrowhead in an inset). I: a sagittal optical section through the pigment-cup ocellus of a rhopalium, showing little AurPaxB expression in the developing photosensory domain (arrowhead). Abbreviations: lc lithocyst. Scale bars: 1 mm (A) 50 μm (B-I).
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pone.0132544.g004: AurOptix, AurPaxA and AurPaxB mRNAs are differentially expressed outside the domain of eye development.Aurelia sp.1 free-swimming ephyrae were labeled with antisense riboprobes against AurOptix (A-C), AurPaxA (D-F), and AurPaxB (G-I). A is a lateral view of an ephyra with the mouth/manubrium facing upwards. Black arrowheads show rhopalia. Note strong localization of AurOptix transcripts in the endoderm of the arms (en). In C and F, the rhopalia were also labeled with antibodies against acetylated ∂-tubulin (acTub) and FMRFamide-like neuropeptides (FMRF; in F). B, C, E, G and H, and an inset in A, are oral views with the rhopalial distal ends pointed upwards. D is an aboral view with the rhopalial distal end pointed upwards. F and I are lateral views with the rhopalial distal ends pointed to the left. B: a medial optical section of a rhopalium, showing endodermal AurOptix expression. An inset shows AurOptix-expressing endodermal pigment cells (arrowheads) in the gastrovascular canal (gc). C: a medial confocal section of a rhopalium showing AurOptix-expressing cells morphologically identifiable as a sensory cell (upper arrowhead) and ganglion cells (lower arrowhead) (cf. [18]). An inset is the section at the plane of the developing photosensory domain (boxed), showing little AurOptix expression. D: an optical section through the exumbrellar (aboral) ectoderm, showing strong AurPaxA expression in individual cells (arrowheads). E: a medial optical section of a rhopalium, showing no detectable levels of AurPaxA expression. F: a sagital confocal section of a rhopalium and the overlying exumbrellar ectoderm showing that AurPaxA-expressing cells are located at the base of the aboral ectoderm (arrowhead) in close association with the FMRFamide-immunoreactive neuronal network (FMRF). G: an oral view of a rhopalar arm. AurPaxB transcript localization in the basal region of a rhopalium is detectable at low levels (arrowhead). H: a medial optical section of a rhopalium, showing AurPaxB expression in the ectoderm (ec) of the proximal region of the rhopalium (arrowhead in an inset). I: a sagittal optical section through the pigment-cup ocellus of a rhopalium, showing little AurPaxB expression in the developing photosensory domain (arrowhead). Abbreviations: lc lithocyst. Scale bars: 1 mm (A) 50 μm (B-I).

Mentions: In contrast to so and eya, optix, paxA and paxB mRNAs are differentially expressed outside the domain of Aurelia cup-ocellus development (Fig 4A–4I). Thus they do not appear to be directly involved in eye development in Aurelia. We found that AurOptix mRNA was expressed in a few neuronal cells in the ectoderm in rhopalia (arrowheads in Fig 4C), as well as in non-ocular pigment cells in the endoderm (Fig 4B). At the late strobila stage, AurOptix expression appeared confined to the endoderm (E and F in S6 Fig). This suggests that that AurOptix functions in the development and/or maintenance of a subset of rhopalial non-photoreceptor neurons as well as non-ocular pigment cells in the endoderm. AurPaxA-expressing cells rarely occurred in rhopalia (Fig 4D–4F). However, high levels of AurPaxA mRNA expression were detected in individual cells that were located at the base of the exumbrellar ectoderm in a close association with the FMRFamide-immunoreactive neuronal network (Fig 4F), suggesting that AurPaxA may be involved in the development of the exumbrellar nerve net. AurPaxB mRNA expression occurs in the ectoderm of the basal portion of the rhopalium (Fig 4G–4I), where a number of neurons, likely including the pacemaker neurons that receive input from photosensory cells, develop [18]. At the late strobila stage, the expression pattern of AurPaxA did not differ from that at the free-swimming ephyra stage with few cells expressing AurPaxA transcripts in developing rhopalia (G and H in S6 Fig), while we failed to detect AurPaxB transcripts at the late strobila stage (data not shown). Thus, AurPaxA and AurPaxB may function in non-ocular neural development, though AurPaxB may be important for the maintenance and/or post-strobilation development of pacemaker neurons that communicate with the photoreceptor cells in the pigment-cup eye. It is also possible that AurPaxA and B have roles in the development of non-ocular photoreceptor cells; identification of non-ocular photoreceptor cells (e.g. by localizing the expression of photosenstive molecules such as opsin in non-ocular cells) is necessary to address this possibility.


Gene Expression Data from the Moon Jelly, Aurelia, Provide Insights into the Evolution of the Combinatorial Code Controlling Animal Sense Organ Development.

Nakanishi N, Camara AC, Yuan DC, Gold DA, Jacobs DK - PLoS ONE (2015)

AurOptix, AurPaxA and AurPaxB mRNAs are differentially expressed outside the domain of eye development.Aurelia sp.1 free-swimming ephyrae were labeled with antisense riboprobes against AurOptix (A-C), AurPaxA (D-F), and AurPaxB (G-I). A is a lateral view of an ephyra with the mouth/manubrium facing upwards. Black arrowheads show rhopalia. Note strong localization of AurOptix transcripts in the endoderm of the arms (en). In C and F, the rhopalia were also labeled with antibodies against acetylated ∂-tubulin (acTub) and FMRFamide-like neuropeptides (FMRF; in F). B, C, E, G and H, and an inset in A, are oral views with the rhopalial distal ends pointed upwards. D is an aboral view with the rhopalial distal end pointed upwards. F and I are lateral views with the rhopalial distal ends pointed to the left. B: a medial optical section of a rhopalium, showing endodermal AurOptix expression. An inset shows AurOptix-expressing endodermal pigment cells (arrowheads) in the gastrovascular canal (gc). C: a medial confocal section of a rhopalium showing AurOptix-expressing cells morphologically identifiable as a sensory cell (upper arrowhead) and ganglion cells (lower arrowhead) (cf. [18]). An inset is the section at the plane of the developing photosensory domain (boxed), showing little AurOptix expression. D: an optical section through the exumbrellar (aboral) ectoderm, showing strong AurPaxA expression in individual cells (arrowheads). E: a medial optical section of a rhopalium, showing no detectable levels of AurPaxA expression. F: a sagital confocal section of a rhopalium and the overlying exumbrellar ectoderm showing that AurPaxA-expressing cells are located at the base of the aboral ectoderm (arrowhead) in close association with the FMRFamide-immunoreactive neuronal network (FMRF). G: an oral view of a rhopalar arm. AurPaxB transcript localization in the basal region of a rhopalium is detectable at low levels (arrowhead). H: a medial optical section of a rhopalium, showing AurPaxB expression in the ectoderm (ec) of the proximal region of the rhopalium (arrowhead in an inset). I: a sagittal optical section through the pigment-cup ocellus of a rhopalium, showing little AurPaxB expression in the developing photosensory domain (arrowhead). Abbreviations: lc lithocyst. Scale bars: 1 mm (A) 50 μm (B-I).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4520661&req=5

pone.0132544.g004: AurOptix, AurPaxA and AurPaxB mRNAs are differentially expressed outside the domain of eye development.Aurelia sp.1 free-swimming ephyrae were labeled with antisense riboprobes against AurOptix (A-C), AurPaxA (D-F), and AurPaxB (G-I). A is a lateral view of an ephyra with the mouth/manubrium facing upwards. Black arrowheads show rhopalia. Note strong localization of AurOptix transcripts in the endoderm of the arms (en). In C and F, the rhopalia were also labeled with antibodies against acetylated ∂-tubulin (acTub) and FMRFamide-like neuropeptides (FMRF; in F). B, C, E, G and H, and an inset in A, are oral views with the rhopalial distal ends pointed upwards. D is an aboral view with the rhopalial distal end pointed upwards. F and I are lateral views with the rhopalial distal ends pointed to the left. B: a medial optical section of a rhopalium, showing endodermal AurOptix expression. An inset shows AurOptix-expressing endodermal pigment cells (arrowheads) in the gastrovascular canal (gc). C: a medial confocal section of a rhopalium showing AurOptix-expressing cells morphologically identifiable as a sensory cell (upper arrowhead) and ganglion cells (lower arrowhead) (cf. [18]). An inset is the section at the plane of the developing photosensory domain (boxed), showing little AurOptix expression. D: an optical section through the exumbrellar (aboral) ectoderm, showing strong AurPaxA expression in individual cells (arrowheads). E: a medial optical section of a rhopalium, showing no detectable levels of AurPaxA expression. F: a sagital confocal section of a rhopalium and the overlying exumbrellar ectoderm showing that AurPaxA-expressing cells are located at the base of the aboral ectoderm (arrowhead) in close association with the FMRFamide-immunoreactive neuronal network (FMRF). G: an oral view of a rhopalar arm. AurPaxB transcript localization in the basal region of a rhopalium is detectable at low levels (arrowhead). H: a medial optical section of a rhopalium, showing AurPaxB expression in the ectoderm (ec) of the proximal region of the rhopalium (arrowhead in an inset). I: a sagittal optical section through the pigment-cup ocellus of a rhopalium, showing little AurPaxB expression in the developing photosensory domain (arrowhead). Abbreviations: lc lithocyst. Scale bars: 1 mm (A) 50 μm (B-I).
Mentions: In contrast to so and eya, optix, paxA and paxB mRNAs are differentially expressed outside the domain of Aurelia cup-ocellus development (Fig 4A–4I). Thus they do not appear to be directly involved in eye development in Aurelia. We found that AurOptix mRNA was expressed in a few neuronal cells in the ectoderm in rhopalia (arrowheads in Fig 4C), as well as in non-ocular pigment cells in the endoderm (Fig 4B). At the late strobila stage, AurOptix expression appeared confined to the endoderm (E and F in S6 Fig). This suggests that that AurOptix functions in the development and/or maintenance of a subset of rhopalial non-photoreceptor neurons as well as non-ocular pigment cells in the endoderm. AurPaxA-expressing cells rarely occurred in rhopalia (Fig 4D–4F). However, high levels of AurPaxA mRNA expression were detected in individual cells that were located at the base of the exumbrellar ectoderm in a close association with the FMRFamide-immunoreactive neuronal network (Fig 4F), suggesting that AurPaxA may be involved in the development of the exumbrellar nerve net. AurPaxB mRNA expression occurs in the ectoderm of the basal portion of the rhopalium (Fig 4G–4I), where a number of neurons, likely including the pacemaker neurons that receive input from photosensory cells, develop [18]. At the late strobila stage, the expression pattern of AurPaxA did not differ from that at the free-swimming ephyra stage with few cells expressing AurPaxA transcripts in developing rhopalia (G and H in S6 Fig), while we failed to detect AurPaxB transcripts at the late strobila stage (data not shown). Thus, AurPaxA and AurPaxB may function in non-ocular neural development, though AurPaxB may be important for the maintenance and/or post-strobilation development of pacemaker neurons that communicate with the photoreceptor cells in the pigment-cup eye. It is also possible that AurPaxA and B have roles in the development of non-ocular photoreceptor cells; identification of non-ocular photoreceptor cells (e.g. by localizing the expression of photosenstive molecules such as opsin in non-ocular cells) is necessary to address this possibility.

Bottom Line: Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia.Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa.The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, UCLA, Los Angeles, California, United States of America.

ABSTRACT
In Bilateria, Pax6, Six, Eya and Dach families of transcription factors underlie the development and evolution of morphologically and phyletically distinct eyes, including the compound eyes in Drosophila and the camera-type eyes in vertebrates, indicating that bilaterian eyes evolved under the strong influence of ancestral developmental gene regulation. However the conservation in eye developmental genetics deeper in the Eumetazoa, and the origin of the conserved gene regulatory apparatus controlling eye development remain unclear due to limited comparative developmental data from Cnidaria. Here we show in the eye-bearing scyphozoan cnidarian Aurelia that the ectodermal photosensory domain of the developing medusa sensory structure known as the rhopalium expresses sine oculis (so)/six1/2 and eyes absent/eya, but not optix/six3/6 or pax (A&B). In addition, the so and eya co-expression domain encompasses the region of active cell proliferation, neurogenesis, and mechanoreceptor development in rhopalia. Consistent with the role of so and eya in rhopalial development, developmental transcriptome data across Aurelia life cycle stages show upregulation of so and eya, but not optix or pax (A&B), during medusa formation. Moreover, pax6 and dach are absent in the Aurelia genome, and thus are not required for eye development in Aurelia. Our data are consistent with so and eya, but not optix, pax or dach, having conserved functions in sensory structure specification across Eumetazoa. The lability of developmental components including Pax genes relative to so-eya is consistent with a model of sense organ development and evolution that involved the lineage specific modification of a combinatorial code that specifies animal sense organs.

No MeSH data available.


Related in: MedlinePlus