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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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Summary of Gva-ParaHox expression during development of G. varia. Note that the colour codes on this figure correspond to the same colours as arrows on the Figure 2-4.
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Figure 6: Summary of Gva-ParaHox expression during development of G. varia. Note that the colour codes on this figure correspond to the same colours as arrows on the Figure 2-4.

Mentions: We were unable to detect clear colinear expression of ParaHox genes in Gibbula prior to torsion. If present, it is obscured by the permanent migration of cells from the digestive gland to their final positions in the gut, and by torsion processes. After torsion, however, a spatially colinear expression of ParaHox genes is obvious in the digestive system, with Gva-Gsx patterning the mouth opening and radula anlage, Gva-Xlox expressed in the midgut, and Gva-Cdx in the hindgut (Figure 4 and 6). Therefore, our results support Holland's hypothesis that ParaHox genes are involved in gut regionalization along the anterior-posterior body axis in protostomes [3].


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)

Summary of Gva-ParaHox expression during development of G. varia. Note that the colour codes on this figure correspond to the same colours as arrows on the Figure 2-4.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Summary of Gva-ParaHox expression during development of G. varia. Note that the colour codes on this figure correspond to the same colours as arrows on the Figure 2-4.
Mentions: We were unable to detect clear colinear expression of ParaHox genes in Gibbula prior to torsion. If present, it is obscured by the permanent migration of cells from the digestive gland to their final positions in the gut, and by torsion processes. After torsion, however, a spatially colinear expression of ParaHox genes is obvious in the digestive system, with Gva-Gsx patterning the mouth opening and radula anlage, Gva-Xlox expressed in the midgut, and Gva-Cdx in the hindgut (Figure 4 and 6). Therefore, our results support Holland's hypothesis that ParaHox genes are involved in gut regionalization along the anterior-posterior body axis in protostomes [3].

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