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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 during trochophore larval stage. (A) SEM of a late trochophore larvae (18-24 hpf). (B-C) Gva-Gsx expression is first detected in early trochophore larva (12 hpf) in a pair of dorso-medial domains of episphere (red arrow heads). (D-K) In late trochophore larva (18-24 hpf) Gva-Gsx is expressed in the dorso-medial episphere (red arrow heads), in the apical sensory organ (grey arrow heads), and around the stomodeum (yellow arrow heads). (F) is higher magnification of Gva-Gsx expression in the apical sensory organ (the area marked by the black rectangle in E) and (H) is the higher magnification of Gva-Gsx expression around the stomodeum. (L-O) Gva-Xlox transcripts are detected in a pair of cell clusters in the ventral episphere (red arrow heads) and as a semicircle around the anal marker (black arrow heads). (P-S) Gva-Cdx is expressed in the left and right primary mesentoblasts (green arrows) and neuroectodermal cells in the hyposphere (black arrow heads). (O) and (S) are false colour images of the in situ hybridization stain, superimposed on fluorescent micrographs stained for nuclei. am anal marker, ao apical organ, f foot rudiment, n protonephridium, pt prototroch, s stomodeum, sf shell field.
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Figure 2: Expression of Gva-ParaHox during trochophore larval stage. (A) SEM of a late trochophore larvae (18-24 hpf). (B-C) Gva-Gsx expression is first detected in early trochophore larva (12 hpf) in a pair of dorso-medial domains of episphere (red arrow heads). (D-K) In late trochophore larva (18-24 hpf) Gva-Gsx is expressed in the dorso-medial episphere (red arrow heads), in the apical sensory organ (grey arrow heads), and around the stomodeum (yellow arrow heads). (F) is higher magnification of Gva-Gsx expression in the apical sensory organ (the area marked by the black rectangle in E) and (H) is the higher magnification of Gva-Gsx expression around the stomodeum. (L-O) Gva-Xlox transcripts are detected in a pair of cell clusters in the ventral episphere (red arrow heads) and as a semicircle around the anal marker (black arrow heads). (P-S) Gva-Cdx is expressed in the left and right primary mesentoblasts (green arrows) and neuroectodermal cells in the hyposphere (black arrow heads). (O) and (S) are false colour images of the in situ hybridization stain, superimposed on fluorescent micrographs stained for nuclei. am anal marker, ao apical organ, f foot rudiment, n protonephridium, pt prototroch, s stomodeum, sf shell field.

Mentions: We did not detect Gva-ParaHox transcripts by whole-mount in situ hybridization (WMISH) in developmental stages before the trochophore stage. A scanning electron micrograph (SEM) of a late trochophore larva (18-24 hpf) is shown in Figure 2A.


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 during trochophore larval stage. (A) SEM of a late trochophore larvae (18-24 hpf). (B-C) Gva-Gsx expression is first detected in early trochophore larva (12 hpf) in a pair of dorso-medial domains of episphere (red arrow heads). (D-K) In late trochophore larva (18-24 hpf) Gva-Gsx is expressed in the dorso-medial episphere (red arrow heads), in the apical sensory organ (grey arrow heads), and around the stomodeum (yellow arrow heads). (F) is higher magnification of Gva-Gsx expression in the apical sensory organ (the area marked by the black rectangle in E) and (H) is the higher magnification of Gva-Gsx expression around the stomodeum. (L-O) Gva-Xlox transcripts are detected in a pair of cell clusters in the ventral episphere (red arrow heads) and as a semicircle around the anal marker (black arrow heads). (P-S) Gva-Cdx is expressed in the left and right primary mesentoblasts (green arrows) and neuroectodermal cells in the hyposphere (black arrow heads). (O) and (S) are false colour images of the in situ hybridization stain, superimposed on fluorescent micrographs stained for nuclei. am anal marker, ao apical organ, f foot rudiment, n protonephridium, pt prototroch, s stomodeum, sf shell field.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Expression of Gva-ParaHox during trochophore larval stage. (A) SEM of a late trochophore larvae (18-24 hpf). (B-C) Gva-Gsx expression is first detected in early trochophore larva (12 hpf) in a pair of dorso-medial domains of episphere (red arrow heads). (D-K) In late trochophore larva (18-24 hpf) Gva-Gsx is expressed in the dorso-medial episphere (red arrow heads), in the apical sensory organ (grey arrow heads), and around the stomodeum (yellow arrow heads). (F) is higher magnification of Gva-Gsx expression in the apical sensory organ (the area marked by the black rectangle in E) and (H) is the higher magnification of Gva-Gsx expression around the stomodeum. (L-O) Gva-Xlox transcripts are detected in a pair of cell clusters in the ventral episphere (red arrow heads) and as a semicircle around the anal marker (black arrow heads). (P-S) Gva-Cdx is expressed in the left and right primary mesentoblasts (green arrows) and neuroectodermal cells in the hyposphere (black arrow heads). (O) and (S) are false colour images of the in situ hybridization stain, superimposed on fluorescent micrographs stained for nuclei. am anal marker, ao apical organ, f foot rudiment, n protonephridium, pt prototroch, s stomodeum, sf shell field.
Mentions: We did not detect Gva-ParaHox transcripts by whole-mount in situ hybridization (WMISH) in developmental stages before the trochophore stage. A scanning electron micrograph (SEM) of a late trochophore larva (18-24 hpf) is shown in Figure 2A.

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