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Conservation of ParaHox genes' function in patterning of the digestive tract of the marine gastropod Gibbula varia.

Samadi L, Steiner G - BMC Dev. Biol. (2010)

Bottom Line: Gva-Gsx patterns potential neural precursors of cerebral ganglia as well as of the apical sensory organ.ParaHox genes of Gibbula are also expressed during specification of cerebral and ventral neuroectodermal cells.Our results provide additional support for the ancestral complexity of Gsx expression and its ancestral role in mouth patterning in protostomes, which was secondarily lost or simplified in some species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria. leili.samadi@univie.ac.at

ABSTRACT

Background: Presence of all three ParaHox genes has been described in deuterostomes and lophotrochozoans, but to date one of these three genes, Xlox has not been reported from any ecdysozoan taxa and both Xlox and Gsx are absent in nematodes. There is evidence that the ParaHox genes were ancestrally a single chromosomal cluster. Colinear expression of the ParaHox genes in anterior, middle, and posterior tissues of several species studied so far suggest that these genes may be responsible for axial patterning of the digestive tract. So far, there are no data on expression of these genes in molluscs.

Results: We isolated the complete coding sequences of the three Gibbula varia ParaHox genes, and then tested their expression in larval and postlarval development. In Gibbula varia, the ParaHox genes participate in patterning of the digestive tract and are expressed in some cells of the neuroectoderm. The expression of these genes coincides with the gradual formation of the gut in the larva. Gva-Gsx patterns potential neural precursors of cerebral ganglia as well as of the apical sensory organ. During larval development this gene is involved in the formation of the mouth and during postlarval development it is expressed in the precursor cells involved in secretion of the radula, the odontoblasts. Gva-Xolx and Gva-Cdx are involved in gut patterning in the middle and posterior parts of digestive tract, respectively. Both genes are expressed in some ventral neuroectodermal cells; however the expression of Gva-Cdx fades in later larval stages while the expression of Gva-Xolx in these cells persists.

Conclusions: In Gibbula varia the ParaHox genes are expressed during anterior-posterior patterning of the digestive system. This colinearity is not easy to spot during early larval stages because the differentiated endothelial cells within the yolk permanently migrate to their destinations in the gut. After torsion, Gsx patterns the mouth and foregut, Xlox the midgut gland or digestive gland, and Cdx the hindgut. ParaHox genes of Gibbula are also expressed during specification of cerebral and ventral neuroectodermal cells. Our results provide additional support for the ancestral complexity of Gsx expression and its ancestral role in mouth patterning in protostomes, which was secondarily lost or simplified in some species.

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Expression of Gva-ParaHox in the posttorsional larval stage. (A) SEM of pretorsional veliger larva. (B-D) Gva-Gsx is expressed in the area of the mouth opening (yellow arrow heads), apical ganglion (grey arrow heads), and ventral part of the digestive gland (blue arrow heads). (E-F) Gva-Gsx expression is detected in the buccal cavity in the forming radula anlage at onset of competence (yellow arrow heads). The gene is also expressed in the forming cerebral ganglia (red arrow heads). (G-J) Gva-Xlox is expressed in the digestive gland (blue arrow heads) and 6-7 cells of the ventral neuroectoderm (black arrow heads). The area marked by black rectangles in (G) and (H) is shown in higher magnification in (I). A section through the digestive gland is shown in (J). Note that the section is not medial since the digestive gland is located on the left side of the larva. (K-L) Gva-Cdx is expressed in the hindgut (blue asterisk) and weaker in the digestive gland (blue arrow heads). ag apical ganglion, at apical tuft, cg cerebral ganglion, e eye, f foot, m mantle edge, mc mantle cavity, mo mouth, o operculum, pv prevelar area, sc sensory cups, v velum, y yolk.
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Figure 4: Expression of Gva-ParaHox in the posttorsional larval stage. (A) SEM of pretorsional veliger larva. (B-D) Gva-Gsx is expressed in the area of the mouth opening (yellow arrow heads), apical ganglion (grey arrow heads), and ventral part of the digestive gland (blue arrow heads). (E-F) Gva-Gsx expression is detected in the buccal cavity in the forming radula anlage at onset of competence (yellow arrow heads). The gene is also expressed in the forming cerebral ganglia (red arrow heads). (G-J) Gva-Xlox is expressed in the digestive gland (blue arrow heads) and 6-7 cells of the ventral neuroectoderm (black arrow heads). The area marked by black rectangles in (G) and (H) is shown in higher magnification in (I). A section through the digestive gland is shown in (J). Note that the section is not medial since the digestive gland is located on the left side of the larva. (K-L) Gva-Cdx is expressed in the hindgut (blue asterisk) and weaker in the digestive gland (blue arrow heads). ag apical ganglion, at apical tuft, cg cerebral ganglion, e eye, f foot, m mantle edge, mc mantle cavity, mo mouth, o operculum, pv prevelar area, sc sensory cups, v velum, y yolk.

Mentions: After torsion (60 hpf), the velum reduces in size with a ventral split, and the mantle expands over the back of the head (Figure 4A). As the digestive tract continues to develop in the posttorsional veliger larva, expression patterns of Gva-ParaHox become more elaborated. At this stage, Gva-Gsx expression in the ventral part of the digestive gland and in the area of the mouth opening persists (Figure 4B and 4C). Sections reveal Gva-Gsx-positive cells at the ventral border of the area of yolk-filled cells (Figure 4D). Gva-Gsx transcripts are further apparent as paired domains beneath the apical organ where the formation of the cerebral ganglia commences (Figures 4C and 4D). At about three days post fertilization, expression of Gva-Gsx fades in the digestive gland. Instead, the gene is now expressed in the foregut around the area of the radula anlage (Figure 4E and 4F). At metamorphosis, when the apical sensory organ starts to dissociate, Gva-Gsx continues to be expressed in the area of the cerebral ganglia (Figure 4F). Gva-Xlox expression persists on the left side of the visceral mass from the pretorsional to the posttorsional stages (Figure 4G and 4H). Sections through the left side of the larva reveal that these Gva-Xlox-positive cells are part of the developing digestive gland (Figure 4J). Six or seven ectodermally-derived Gva-Xlox-positive cells are located in the ventral part of the visceral mass (Figure 4G, H, and 4I). Gva-Cdx is mainly expressed in the newly formed hindgut and rectum, and weakly in the digestive gland (Figures 4K and 4L).


Conservation of ParaHox genes' function in patterning of the digestive tract of the marine gastropod Gibbula varia.

Samadi L, Steiner G - BMC Dev. Biol. (2010)

Expression of Gva-ParaHox in the posttorsional larval stage. (A) SEM of pretorsional veliger larva. (B-D) Gva-Gsx is expressed in the area of the mouth opening (yellow arrow heads), apical ganglion (grey arrow heads), and ventral part of the digestive gland (blue arrow heads). (E-F) Gva-Gsx expression is detected in the buccal cavity in the forming radula anlage at onset of competence (yellow arrow heads). The gene is also expressed in the forming cerebral ganglia (red arrow heads). (G-J) Gva-Xlox is expressed in the digestive gland (blue arrow heads) and 6-7 cells of the ventral neuroectoderm (black arrow heads). The area marked by black rectangles in (G) and (H) is shown in higher magnification in (I). A section through the digestive gland is shown in (J). Note that the section is not medial since the digestive gland is located on the left side of the larva. (K-L) Gva-Cdx is expressed in the hindgut (blue asterisk) and weaker in the digestive gland (blue arrow heads). ag apical ganglion, at apical tuft, cg cerebral ganglion, e eye, f foot, m mantle edge, mc mantle cavity, mo mouth, o operculum, pv prevelar area, sc sensory cups, v velum, y yolk.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2913954&req=5

Figure 4: Expression of Gva-ParaHox in the posttorsional larval stage. (A) SEM of pretorsional veliger larva. (B-D) Gva-Gsx is expressed in the area of the mouth opening (yellow arrow heads), apical ganglion (grey arrow heads), and ventral part of the digestive gland (blue arrow heads). (E-F) Gva-Gsx expression is detected in the buccal cavity in the forming radula anlage at onset of competence (yellow arrow heads). The gene is also expressed in the forming cerebral ganglia (red arrow heads). (G-J) Gva-Xlox is expressed in the digestive gland (blue arrow heads) and 6-7 cells of the ventral neuroectoderm (black arrow heads). The area marked by black rectangles in (G) and (H) is shown in higher magnification in (I). A section through the digestive gland is shown in (J). Note that the section is not medial since the digestive gland is located on the left side of the larva. (K-L) Gva-Cdx is expressed in the hindgut (blue asterisk) and weaker in the digestive gland (blue arrow heads). ag apical ganglion, at apical tuft, cg cerebral ganglion, e eye, f foot, m mantle edge, mc mantle cavity, mo mouth, o operculum, pv prevelar area, sc sensory cups, v velum, y yolk.
Mentions: After torsion (60 hpf), the velum reduces in size with a ventral split, and the mantle expands over the back of the head (Figure 4A). As the digestive tract continues to develop in the posttorsional veliger larva, expression patterns of Gva-ParaHox become more elaborated. At this stage, Gva-Gsx expression in the ventral part of the digestive gland and in the area of the mouth opening persists (Figure 4B and 4C). Sections reveal Gva-Gsx-positive cells at the ventral border of the area of yolk-filled cells (Figure 4D). Gva-Gsx transcripts are further apparent as paired domains beneath the apical organ where the formation of the cerebral ganglia commences (Figures 4C and 4D). At about three days post fertilization, expression of Gva-Gsx fades in the digestive gland. Instead, the gene is now expressed in the foregut around the area of the radula anlage (Figure 4E and 4F). At metamorphosis, when the apical sensory organ starts to dissociate, Gva-Gsx continues to be expressed in the area of the cerebral ganglia (Figure 4F). Gva-Xlox expression persists on the left side of the visceral mass from the pretorsional to the posttorsional stages (Figure 4G and 4H). Sections through the left side of the larva reveal that these Gva-Xlox-positive cells are part of the developing digestive gland (Figure 4J). Six or seven ectodermally-derived Gva-Xlox-positive cells are located in the ventral part of the visceral mass (Figure 4G, H, and 4I). Gva-Cdx is mainly expressed in the newly formed hindgut and rectum, and weakly in the digestive gland (Figures 4K and 4L).

Bottom Line: Gva-Gsx patterns potential neural precursors of cerebral ganglia as well as of the apical sensory organ.ParaHox genes of Gibbula are also expressed during specification of cerebral and ventral neuroectodermal cells.Our results provide additional support for the ancestral complexity of Gsx expression and its ancestral role in mouth patterning in protostomes, which was secondarily lost or simplified in some species.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Evolutionary Biology, Faculty of Life Sciences, University of Vienna, Vienna, Austria. leili.samadi@univie.ac.at

ABSTRACT

Background: Presence of all three ParaHox genes has been described in deuterostomes and lophotrochozoans, but to date one of these three genes, Xlox has not been reported from any ecdysozoan taxa and both Xlox and Gsx are absent in nematodes. There is evidence that the ParaHox genes were ancestrally a single chromosomal cluster. Colinear expression of the ParaHox genes in anterior, middle, and posterior tissues of several species studied so far suggest that these genes may be responsible for axial patterning of the digestive tract. So far, there are no data on expression of these genes in molluscs.

Results: We isolated the complete coding sequences of the three Gibbula varia ParaHox genes, and then tested their expression in larval and postlarval development. In Gibbula varia, the ParaHox genes participate in patterning of the digestive tract and are expressed in some cells of the neuroectoderm. The expression of these genes coincides with the gradual formation of the gut in the larva. Gva-Gsx patterns potential neural precursors of cerebral ganglia as well as of the apical sensory organ. During larval development this gene is involved in the formation of the mouth and during postlarval development it is expressed in the precursor cells involved in secretion of the radula, the odontoblasts. Gva-Xolx and Gva-Cdx are involved in gut patterning in the middle and posterior parts of digestive tract, respectively. Both genes are expressed in some ventral neuroectodermal cells; however the expression of Gva-Cdx fades in later larval stages while the expression of Gva-Xolx in these cells persists.

Conclusions: In Gibbula varia the ParaHox genes are expressed during anterior-posterior patterning of the digestive system. This colinearity is not easy to spot during early larval stages because the differentiated endothelial cells within the yolk permanently migrate to their destinations in the gut. After torsion, Gsx patterns the mouth and foregut, Xlox the midgut gland or digestive gland, and Cdx the hindgut. ParaHox genes of Gibbula are also expressed during specification of cerebral and ventral neuroectodermal cells. Our results provide additional support for the ancestral complexity of Gsx expression and its ancestral role in mouth patterning in protostomes, which was secondarily lost or simplified in some species.

Show MeSH
Related in: MedlinePlus