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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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Post-larval expression of Gva-Gsx. (A) Medial longitudinal section through the radula of a hatched juvenile stained with Toluidine Blue. (B) Paired odontoblastic cushions at the base of the radula sac where radula teeth are formed. The staining is Toluidine Blue. (C-E) Gva-Gsx expression is observed in odontoblastic cushions of the hatchling. The black rectangular area marked on (C) is demonstrated in higher magnification in (D). The gradient of Gva-Gsx expression in odontophores and odontoblast is shown in (E). bc buccal cavity, cf ctenidial filaments, eso esophagus, frt forming radula teeth, ie inferior epithelium, j jaw, mf mantle fold, mo mouth opening, oc odontoblastic cushions, od odontoblasts, odc odontoblastic cartilage, op odontophores, op operculum, pf pedal folds, rm radula membrane, rn radula nerve, rt radula teeth, sc separating cells, sm shell matrix, tsm tensor muscle.
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Figure 5: Post-larval expression of Gva-Gsx. (A) Medial longitudinal section through the radula of a hatched juvenile stained with Toluidine Blue. (B) Paired odontoblastic cushions at the base of the radula sac where radula teeth are formed. The staining is Toluidine Blue. (C-E) Gva-Gsx expression is observed in odontoblastic cushions of the hatchling. The black rectangular area marked on (C) is demonstrated in higher magnification in (D). The gradient of Gva-Gsx expression in odontophores and odontoblast is shown in (E). bc buccal cavity, cf ctenidial filaments, eso esophagus, frt forming radula teeth, ie inferior epithelium, j jaw, mf mantle fold, mo mouth opening, oc odontoblastic cushions, od odontoblasts, odc odontoblastic cartilage, op odontophores, op operculum, pf pedal folds, rm radula membrane, rn radula nerve, rt radula teeth, sc separating cells, sm shell matrix, tsm tensor muscle.

Mentions: Serial section in situ hybridizations were used to trace the expression pattern of all three Gva-ParaHox in the hatchling (about four days after fertilization). No positive signals for Gva-Xlox and Gva-Cad transcripts are detected at this stage. Gva-Gsx is the only ParaHox gene that is expressed in the most posterior part of the radula sac during postlarval development (Figure 5). The juvenile hatchling has a complete radula with the radula sheath, buccal musculature, and radula bolsters (also called odontoblastic cartilages, Figure 5A). The posterior end of the radula sac forms the odontoblastic cushion which consists of a single-layered epithelium arranged in a semicircle and protruding into the sac's lumen. The epithelial cells are produced by two separated dorsolateral mitotic centres at the end of the sac (Figure 5B). Mitotic activity is scattered over the posterior area of odontoblastic cushions where the cells are small and undifferentiated. Towards the anterior of the cushions, the cells gradually elongate and form the tall odontoblastic epithelial cells (Figure 5B). Gva-Gsx transcripts are mainly detected in the paired odontoblastic cushions at the base of the radula (Figure 5C; the weak signal observed in the pedal area seems to be unspecific). Gva-Gsx is expressed both in undifferentiated cells located at the back of the cushions and in odontoblastic epithelial cells. No transcripts were detected in the cells separating the two halves of the odontoblastic cushion (Figure 5D and 5E). The intensity of expression of Gva-Gsx diminishes gradually from posterior to anterior, i.e. from the undifferentiated cells to fully differentiated epithelial odontoblasts (Figure 5E).


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)

Post-larval expression of Gva-Gsx. (A) Medial longitudinal section through the radula of a hatched juvenile stained with Toluidine Blue. (B) Paired odontoblastic cushions at the base of the radula sac where radula teeth are formed. The staining is Toluidine Blue. (C-E) Gva-Gsx expression is observed in odontoblastic cushions of the hatchling. The black rectangular area marked on (C) is demonstrated in higher magnification in (D). The gradient of Gva-Gsx expression in odontophores and odontoblast is shown in (E). bc buccal cavity, cf ctenidial filaments, eso esophagus, frt forming radula teeth, ie inferior epithelium, j jaw, mf mantle fold, mo mouth opening, oc odontoblastic cushions, od odontoblasts, odc odontoblastic cartilage, op odontophores, op operculum, pf pedal folds, rm radula membrane, rn radula nerve, rt radula teeth, sc separating cells, sm shell matrix, tsm tensor muscle.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2913954&req=5

Figure 5: Post-larval expression of Gva-Gsx. (A) Medial longitudinal section through the radula of a hatched juvenile stained with Toluidine Blue. (B) Paired odontoblastic cushions at the base of the radula sac where radula teeth are formed. The staining is Toluidine Blue. (C-E) Gva-Gsx expression is observed in odontoblastic cushions of the hatchling. The black rectangular area marked on (C) is demonstrated in higher magnification in (D). The gradient of Gva-Gsx expression in odontophores and odontoblast is shown in (E). bc buccal cavity, cf ctenidial filaments, eso esophagus, frt forming radula teeth, ie inferior epithelium, j jaw, mf mantle fold, mo mouth opening, oc odontoblastic cushions, od odontoblasts, odc odontoblastic cartilage, op odontophores, op operculum, pf pedal folds, rm radula membrane, rn radula nerve, rt radula teeth, sc separating cells, sm shell matrix, tsm tensor muscle.
Mentions: Serial section in situ hybridizations were used to trace the expression pattern of all three Gva-ParaHox in the hatchling (about four days after fertilization). No positive signals for Gva-Xlox and Gva-Cad transcripts are detected at this stage. Gva-Gsx is the only ParaHox gene that is expressed in the most posterior part of the radula sac during postlarval development (Figure 5). The juvenile hatchling has a complete radula with the radula sheath, buccal musculature, and radula bolsters (also called odontoblastic cartilages, Figure 5A). The posterior end of the radula sac forms the odontoblastic cushion which consists of a single-layered epithelium arranged in a semicircle and protruding into the sac's lumen. The epithelial cells are produced by two separated dorsolateral mitotic centres at the end of the sac (Figure 5B). Mitotic activity is scattered over the posterior area of odontoblastic cushions where the cells are small and undifferentiated. Towards the anterior of the cushions, the cells gradually elongate and form the tall odontoblastic epithelial cells (Figure 5B). Gva-Gsx transcripts are mainly detected in the paired odontoblastic cushions at the base of the radula (Figure 5C; the weak signal observed in the pedal area seems to be unspecific). Gva-Gsx is expressed both in undifferentiated cells located at the back of the cushions and in odontoblastic epithelial cells. No transcripts were detected in the cells separating the two halves of the odontoblastic cushion (Figure 5D and 5E). The intensity of expression of Gva-Gsx diminishes gradually from posterior to anterior, i.e. from the undifferentiated cells to fully differentiated epithelial odontoblasts (Figure 5E).

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