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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

Scyphozoan life cycle and morphology of a scyphozoan rhopalium.A: Life cycle stages of the scyphozoan Aurelia. Scyphozoan ephyrae develop through transverse fission of polyps, a process known as strobilation (the “strobila” stage). Rhopalia (rh) begin development at the margin of each segment during strobilation. B: A schematic lateral view of the rhopalium in a juvenile medusa (“metephyra”). The distal end is to the left, the proximal end to the right. Oral is down, aboral up. Each rhopalium consists of terminal (te), intermediate (in) and basal (ba) regions, and has a gravity-sensitive organ consisting of the lithocyst (lc) and the touch plate (tp), a pigment-cup ocellus (co), and a pigment-spot ocellus (so). The boxed region is the cup-ocellus (co) shown in C. Morphological and behavioral evidence supports the photosensory function of the cup ocelli, but not of the spot ocelli [10–12], and thus this study focuses on analyzing gene expression in relation to the development of the former, but not the latter, structure. C: A confocal section of the cup-ocellus at the metephyra stage labeled with antibodies against FMRFamide-like neuropeptides (FMRF) and acetylated ∂-tubulin (acTub). Note basal cilia (ci) of photoreceptor cells (pr). The dark region surrounding the photoreceptor cells (pr) is the endodermal pigment layer (pi). Nuclei are labeled with the fluorescent dye TOTO. D: Schematics of developing rhopalia from late strobila (“Strobila”), through ephyra, into metephyra (“Juvenile”) stages. The top row shows the lateral view of the terminal (te) and intermediate (in) regions of a developing rhopalium; the distal end is to the left, the oral side down. The bottom row shows the oral view of a developing rhopalium; the distal end is to the top, the proximal end to the bottom. In the developing cup ocellus (co), the domain of ciliated ectodermal photoreceptor cells is shown in purple, while the domain of endodermal pigment cells is shown in grey. At strobilation, the gravity-sensitive organ—the lithocyst (lc) and the touch plate (tp)—begin development first, followed by the pacemaker neurons (pm) located in the proximal-most, basal region (ba) of the rhopalial ectoderm. Cup ocelli (co) start to differentiate in free-swimming ephyrae, while the pigment-spot ocelli (so) develop later at the metephyra stage. Note that the developing photosensory tissue of the cup ocellus is located in the oral-medial ectoderm of the intermediate region of the rhopalium. Abbreviations: en endoderm; ca rhopalar canal. Scale bars: 100 μm (A), 10 μm (B).
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pone.0132544.g001: Scyphozoan life cycle and morphology of a scyphozoan rhopalium.A: Life cycle stages of the scyphozoan Aurelia. Scyphozoan ephyrae develop through transverse fission of polyps, a process known as strobilation (the “strobila” stage). Rhopalia (rh) begin development at the margin of each segment during strobilation. B: A schematic lateral view of the rhopalium in a juvenile medusa (“metephyra”). The distal end is to the left, the proximal end to the right. Oral is down, aboral up. Each rhopalium consists of terminal (te), intermediate (in) and basal (ba) regions, and has a gravity-sensitive organ consisting of the lithocyst (lc) and the touch plate (tp), a pigment-cup ocellus (co), and a pigment-spot ocellus (so). The boxed region is the cup-ocellus (co) shown in C. Morphological and behavioral evidence supports the photosensory function of the cup ocelli, but not of the spot ocelli [10–12], and thus this study focuses on analyzing gene expression in relation to the development of the former, but not the latter, structure. C: A confocal section of the cup-ocellus at the metephyra stage labeled with antibodies against FMRFamide-like neuropeptides (FMRF) and acetylated ∂-tubulin (acTub). Note basal cilia (ci) of photoreceptor cells (pr). The dark region surrounding the photoreceptor cells (pr) is the endodermal pigment layer (pi). Nuclei are labeled with the fluorescent dye TOTO. D: Schematics of developing rhopalia from late strobila (“Strobila”), through ephyra, into metephyra (“Juvenile”) stages. The top row shows the lateral view of the terminal (te) and intermediate (in) regions of a developing rhopalium; the distal end is to the left, the oral side down. The bottom row shows the oral view of a developing rhopalium; the distal end is to the top, the proximal end to the bottom. In the developing cup ocellus (co), the domain of ciliated ectodermal photoreceptor cells is shown in purple, while the domain of endodermal pigment cells is shown in grey. At strobilation, the gravity-sensitive organ—the lithocyst (lc) and the touch plate (tp)—begin development first, followed by the pacemaker neurons (pm) located in the proximal-most, basal region (ba) of the rhopalial ectoderm. Cup ocelli (co) start to differentiate in free-swimming ephyrae, while the pigment-spot ocelli (so) develop later at the metephyra stage. Note that the developing photosensory tissue of the cup ocellus is located in the oral-medial ectoderm of the intermediate region of the rhopalium. Abbreviations: en endoderm; ca rhopalar canal. Scale bars: 100 μm (A), 10 μm (B).

Mentions: In the Cnidaria, Medusozoa (i.e. jellyfishes) have diverse photoreceptor types ranging from simple eye-spots to complex eyes with retinas (see [7] for a review). The medusozoan life history usually consists of a motile planula stage, a sessile polyp stage and a free-swimming, sexual medusa stage (e.g. Fig 1A). Distinct ocular structures are typically found at the bell margin of the medusa (but see [8, 9] for description of putative eye-like structures in a planula larva and a polyp, respectively), either at the base of the tentacles (in Hydrozoa), or in the club-shaped sensory structures called the rhopalium that usually occurs in multiples of four (at least eight in Scyphozoa, Fig 1A; four in Cubozoa).


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)

Scyphozoan life cycle and morphology of a scyphozoan rhopalium.A: Life cycle stages of the scyphozoan Aurelia. Scyphozoan ephyrae develop through transverse fission of polyps, a process known as strobilation (the “strobila” stage). Rhopalia (rh) begin development at the margin of each segment during strobilation. B: A schematic lateral view of the rhopalium in a juvenile medusa (“metephyra”). The distal end is to the left, the proximal end to the right. Oral is down, aboral up. Each rhopalium consists of terminal (te), intermediate (in) and basal (ba) regions, and has a gravity-sensitive organ consisting of the lithocyst (lc) and the touch plate (tp), a pigment-cup ocellus (co), and a pigment-spot ocellus (so). The boxed region is the cup-ocellus (co) shown in C. Morphological and behavioral evidence supports the photosensory function of the cup ocelli, but not of the spot ocelli [10–12], and thus this study focuses on analyzing gene expression in relation to the development of the former, but not the latter, structure. C: A confocal section of the cup-ocellus at the metephyra stage labeled with antibodies against FMRFamide-like neuropeptides (FMRF) and acetylated ∂-tubulin (acTub). Note basal cilia (ci) of photoreceptor cells (pr). The dark region surrounding the photoreceptor cells (pr) is the endodermal pigment layer (pi). Nuclei are labeled with the fluorescent dye TOTO. D: Schematics of developing rhopalia from late strobila (“Strobila”), through ephyra, into metephyra (“Juvenile”) stages. The top row shows the lateral view of the terminal (te) and intermediate (in) regions of a developing rhopalium; the distal end is to the left, the oral side down. The bottom row shows the oral view of a developing rhopalium; the distal end is to the top, the proximal end to the bottom. In the developing cup ocellus (co), the domain of ciliated ectodermal photoreceptor cells is shown in purple, while the domain of endodermal pigment cells is shown in grey. At strobilation, the gravity-sensitive organ—the lithocyst (lc) and the touch plate (tp)—begin development first, followed by the pacemaker neurons (pm) located in the proximal-most, basal region (ba) of the rhopalial ectoderm. Cup ocelli (co) start to differentiate in free-swimming ephyrae, while the pigment-spot ocelli (so) develop later at the metephyra stage. Note that the developing photosensory tissue of the cup ocellus is located in the oral-medial ectoderm of the intermediate region of the rhopalium. Abbreviations: en endoderm; ca rhopalar canal. Scale bars: 100 μm (A), 10 μm (B).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0132544.g001: Scyphozoan life cycle and morphology of a scyphozoan rhopalium.A: Life cycle stages of the scyphozoan Aurelia. Scyphozoan ephyrae develop through transverse fission of polyps, a process known as strobilation (the “strobila” stage). Rhopalia (rh) begin development at the margin of each segment during strobilation. B: A schematic lateral view of the rhopalium in a juvenile medusa (“metephyra”). The distal end is to the left, the proximal end to the right. Oral is down, aboral up. Each rhopalium consists of terminal (te), intermediate (in) and basal (ba) regions, and has a gravity-sensitive organ consisting of the lithocyst (lc) and the touch plate (tp), a pigment-cup ocellus (co), and a pigment-spot ocellus (so). The boxed region is the cup-ocellus (co) shown in C. Morphological and behavioral evidence supports the photosensory function of the cup ocelli, but not of the spot ocelli [10–12], and thus this study focuses on analyzing gene expression in relation to the development of the former, but not the latter, structure. C: A confocal section of the cup-ocellus at the metephyra stage labeled with antibodies against FMRFamide-like neuropeptides (FMRF) and acetylated ∂-tubulin (acTub). Note basal cilia (ci) of photoreceptor cells (pr). The dark region surrounding the photoreceptor cells (pr) is the endodermal pigment layer (pi). Nuclei are labeled with the fluorescent dye TOTO. D: Schematics of developing rhopalia from late strobila (“Strobila”), through ephyra, into metephyra (“Juvenile”) stages. The top row shows the lateral view of the terminal (te) and intermediate (in) regions of a developing rhopalium; the distal end is to the left, the oral side down. The bottom row shows the oral view of a developing rhopalium; the distal end is to the top, the proximal end to the bottom. In the developing cup ocellus (co), the domain of ciliated ectodermal photoreceptor cells is shown in purple, while the domain of endodermal pigment cells is shown in grey. At strobilation, the gravity-sensitive organ—the lithocyst (lc) and the touch plate (tp)—begin development first, followed by the pacemaker neurons (pm) located in the proximal-most, basal region (ba) of the rhopalial ectoderm. Cup ocelli (co) start to differentiate in free-swimming ephyrae, while the pigment-spot ocelli (so) develop later at the metephyra stage. Note that the developing photosensory tissue of the cup ocellus is located in the oral-medial ectoderm of the intermediate region of the rhopalium. Abbreviations: en endoderm; ca rhopalar canal. Scale bars: 100 μm (A), 10 μm (B).
Mentions: In the Cnidaria, Medusozoa (i.e. jellyfishes) have diverse photoreceptor types ranging from simple eye-spots to complex eyes with retinas (see [7] for a review). The medusozoan life history usually consists of a motile planula stage, a sessile polyp stage and a free-swimming, sexual medusa stage (e.g. Fig 1A). Distinct ocular structures are typically found at the bell margin of the medusa (but see [8, 9] for description of putative eye-like structures in a planula larva and a polyp, respectively), either at the base of the tentacles (in Hydrozoa), or in the club-shaped sensory structures called the rhopalium that usually occurs in multiples of four (at least eight in Scyphozoa, Fig 1A; four in Cubozoa).

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