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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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Phylogenetic reconstruction of ParaHox genes. The tree is from Bayesian likelihood analysis using MrBayes: half compatibility consensus from five million replicates, burn-in of 5,000 replicates. The tree is built with the amino-acid sequences of the homeodomain and the flanking region. Support values of branches are posterior probabilities of Bayesian likelihood. Hox1 sequences of several bilaterians are used as outgroup (black). Groupings of the ParaHox genes are strongly supported. Gsx/Gsh sequences are shown in red, Xlox sequences in blue, and Cad/Cdx in green. Yellow rectangles highlight ParaHox sequences of G. varia. Amphioxus: Branchiostoma floridae, Branchiopode: Artemia franciscana, Frog: Xenopus tropicalis, Fruit fly: Drosophila melanogaster, Human: Homo sapiens, Hydrozoa: Podocoryne carnea, Leech: Hirudo medicinalis, Limpet: Patella vulgata, Mouse: Mus musculus, Mosquito: Anopheles gambiae, Nematode: Caenorhabditis elegans, Polychaete 1: Platynereis dumerilii, Polychaete 2: Capitella teleta, Sea Anemone: Nematostella vectensis, Sea Urchin: Strongylocentrotus purpuratus, Top Shell: Gibbula varia.
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Figure 1: Phylogenetic reconstruction of ParaHox genes. The tree is from Bayesian likelihood analysis using MrBayes: half compatibility consensus from five million replicates, burn-in of 5,000 replicates. The tree is built with the amino-acid sequences of the homeodomain and the flanking region. Support values of branches are posterior probabilities of Bayesian likelihood. Hox1 sequences of several bilaterians are used as outgroup (black). Groupings of the ParaHox genes are strongly supported. Gsx/Gsh sequences are shown in red, Xlox sequences in blue, and Cad/Cdx in green. Yellow rectangles highlight ParaHox sequences of G. varia. Amphioxus: Branchiostoma floridae, Branchiopode: Artemia franciscana, Frog: Xenopus tropicalis, Fruit fly: Drosophila melanogaster, Human: Homo sapiens, Hydrozoa: Podocoryne carnea, Leech: Hirudo medicinalis, Limpet: Patella vulgata, Mouse: Mus musculus, Mosquito: Anopheles gambiae, Nematode: Caenorhabditis elegans, Polychaete 1: Platynereis dumerilii, Polychaete 2: Capitella teleta, Sea Anemone: Nematostella vectensis, Sea Urchin: Strongylocentrotus purpuratus, Top Shell: Gibbula varia.

Mentions: The entire coding sequences for all three G. varia ParaHox genes were isolated by a combination of 3' and 5' rapid amplification of cDNA ends (RACE, see Methods). 3' and 5' RACE together yielded a complete cDNA of 885 bp with the complete open reading frame (ORF) of 519 bp (172 amino acids) for Gva-Gsx, a complete cDNA of 1739 bp with complete ORF of 1002 bp (333 amino acids) for Gva-Xlox, and a complete cDNA of 1466 bp with complete ORF of 976 bp (325 amino acids) for Gva-Cdx. Alignments of each G. varia ParaHox amino acid sequence to orthologs of other species are shown in additional file 2, Figure S3, S4, and S5. Beside the homeobox which is the main region of conservation between ParaHox genes, further conserved domains are the N-terminal domain in Gsx, and the hexapeptide motifs just upstream of the homeodomains in both Xlox and Cdx (Additional file 2, Figure S3, S4, and S5). The classification of the G. varia ParaHox genes into their orthology groups is apparent from phylogenetic analyses (Figure 1). The species names and accession number of the genes used in phylogenetic analysis are provided in additional file 2. Although the phylogenetic analysis clearly assigns the Gibbula paraHox genes to the Gsx, Xlox and Cdx classes with high support values, the internal grouping remains unclear.


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)

Phylogenetic reconstruction of ParaHox genes. The tree is from Bayesian likelihood analysis using MrBayes: half compatibility consensus from five million replicates, burn-in of 5,000 replicates. The tree is built with the amino-acid sequences of the homeodomain and the flanking region. Support values of branches are posterior probabilities of Bayesian likelihood. Hox1 sequences of several bilaterians are used as outgroup (black). Groupings of the ParaHox genes are strongly supported. Gsx/Gsh sequences are shown in red, Xlox sequences in blue, and Cad/Cdx in green. Yellow rectangles highlight ParaHox sequences of G. varia. Amphioxus: Branchiostoma floridae, Branchiopode: Artemia franciscana, Frog: Xenopus tropicalis, Fruit fly: Drosophila melanogaster, Human: Homo sapiens, Hydrozoa: Podocoryne carnea, Leech: Hirudo medicinalis, Limpet: Patella vulgata, Mouse: Mus musculus, Mosquito: Anopheles gambiae, Nematode: Caenorhabditis elegans, Polychaete 1: Platynereis dumerilii, Polychaete 2: Capitella teleta, Sea Anemone: Nematostella vectensis, Sea Urchin: Strongylocentrotus purpuratus, Top Shell: Gibbula varia.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Phylogenetic reconstruction of ParaHox genes. The tree is from Bayesian likelihood analysis using MrBayes: half compatibility consensus from five million replicates, burn-in of 5,000 replicates. The tree is built with the amino-acid sequences of the homeodomain and the flanking region. Support values of branches are posterior probabilities of Bayesian likelihood. Hox1 sequences of several bilaterians are used as outgroup (black). Groupings of the ParaHox genes are strongly supported. Gsx/Gsh sequences are shown in red, Xlox sequences in blue, and Cad/Cdx in green. Yellow rectangles highlight ParaHox sequences of G. varia. Amphioxus: Branchiostoma floridae, Branchiopode: Artemia franciscana, Frog: Xenopus tropicalis, Fruit fly: Drosophila melanogaster, Human: Homo sapiens, Hydrozoa: Podocoryne carnea, Leech: Hirudo medicinalis, Limpet: Patella vulgata, Mouse: Mus musculus, Mosquito: Anopheles gambiae, Nematode: Caenorhabditis elegans, Polychaete 1: Platynereis dumerilii, Polychaete 2: Capitella teleta, Sea Anemone: Nematostella vectensis, Sea Urchin: Strongylocentrotus purpuratus, Top Shell: Gibbula varia.
Mentions: The entire coding sequences for all three G. varia ParaHox genes were isolated by a combination of 3' and 5' rapid amplification of cDNA ends (RACE, see Methods). 3' and 5' RACE together yielded a complete cDNA of 885 bp with the complete open reading frame (ORF) of 519 bp (172 amino acids) for Gva-Gsx, a complete cDNA of 1739 bp with complete ORF of 1002 bp (333 amino acids) for Gva-Xlox, and a complete cDNA of 1466 bp with complete ORF of 976 bp (325 amino acids) for Gva-Cdx. Alignments of each G. varia ParaHox amino acid sequence to orthologs of other species are shown in additional file 2, Figure S3, S4, and S5. Beside the homeobox which is the main region of conservation between ParaHox genes, further conserved domains are the N-terminal domain in Gsx, and the hexapeptide motifs just upstream of the homeodomains in both Xlox and Cdx (Additional file 2, Figure S3, S4, and S5). The classification of the G. varia ParaHox genes into their orthology groups is apparent from phylogenetic analyses (Figure 1). The species names and accession number of the genes used in phylogenetic analysis are provided in additional file 2. Although the phylogenetic analysis clearly assigns the Gibbula paraHox genes to the Gsx, Xlox and Cdx classes with high support values, the internal grouping remains unclear.

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