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

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.

SUBMITTER: Samadi L

PROVIDER: S-EPMC2913954 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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

Samadi Leyli L Steiner Gerhard G

BMC developmental biology 20100712

<h4>Background</h4>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 ...[more]

PMID: 20624311

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Project description:BackgroundThe homeobox genes Pdx and Cdx are widespread across the animal kingdom and part of the small ParaHox gene cluster. Gene expression patterns suggest ancient roles for Pdx and Cdx in patterning the through-gut of bilaterian animals although functional data are available for few lineages. To examine evolutionary conservation of Pdx and Cdx gene functions, we focus on amphioxus, small marine animals that occupy a pivotal position in chordate evolution and in which ParaHox gene clustering was first reported.ResultsUsing transcription activator-like effector nucleases (TALENs), we engineer frameshift mutations in the Pdx and Cdx genes of the amphioxus Branchiostoma floridae and establish mutant lines. Homozygous Pdx mutants have a defect in amphioxus endoderm, manifest as loss of a midgut region expressing endogenous GFP. The anus fails to open in homozygous Cdx mutants, which also have defects in posterior body extension and epidermal tail fin development. Treatment with an inverse agonist of retinoic acid (RA) signalling partially rescues the axial and tail fin phenotypes indicating they are caused by increased RA signalling. Gene expression analyses and luciferase assays suggest that posterior RA levels are kept low in wild type animals by a likely direct transcriptional regulation of a Cyp26 gene by Cdx. Transcriptome analysis reveals extensive gene expression changes in mutants, with a disproportionate effect of Pdx and Cdx on gut-enriched genes and a colinear-like effect of Cdx on Hox genes.ConclusionsThese data reveal that amphioxus Pdx and Cdx have roles in specifying middle and posterior cell fates in the endoderm of the gut, roles that likely date to the origin of Bilateria. This conclusion is consistent with these two ParaHox genes playing a role in the origin of the bilaterian through-gut with a distinct anus, morphological innovations that contributed to ecological change in the Cambrian. In addition, we find that amphioxus Cdx promotes body axis extension through a molecular mechanism conserved with vertebrates. The axial extension role for Cdx dates back at least to the origin of Chordata and may have facilitated the evolution of the post-anal tail and active locomotion in chordates.

Project description:Adaptation to a hypertonic marine environment is one of the major topics in animal physiology research. Marine teleosts lose water osmotically from the gills and compensate for this loss by drinking surrounding seawater and absorbing water from the intestine. This situation is in contrast to that in mammals, which experience a net osmotic loss of water after drinking seawater. Water absorption in fishes is made possible by (1) removal of monovalent ions (desalinization) by the esophagus, (2) removal of divalent ions as carbonate (Mg/CaCO3) precipitates promoted by HCO3- secretion, and (3) facilitation of NaCl and water absorption from diluted seawater by the intestine using a suite of unique transporters. As a result, 70-85% of ingested seawater is absorbed during its passage through the digestive tract. Thus, the digestive tract is an essential organ for marine teleost survival in the hypertonic seawater environment. The eel is a species that has been frequently used for osmoregulation research in laboratories worldwide. The eel possesses many advantages as an experimental animal for osmoregulation studies, one of which is its outstanding euryhalinity, which enables researchers to examine changes in the structure and function of the digestive tract after direct transfer from freshwater to seawater. In recent years, the molecular mechanisms of ion and water transport across epithelial cells (the transcellular route) and through tight junctions (the paracellular route) have been elucidated for the esophagus and intestine. Thanks to the rapid progress in analytical methods for genome databases on teleosts, including the eel, the molecular identities of transporters, channels, pumps and junctional proteins have been clarified at the isoform level. As 10 y have passed since the previous reviews on this subject, it seems relevant and timely to summarize recent progress in research on the molecular mechanisms of water and ion transport in the digestive tract in eels and to compare the mechanisms with those of other teleosts and mammals from comparative and evolutionary viewpoints. We also propose future directions for this research field to achieve integrative understanding of the role of the digestive tract in adaptation to seawater with regard to pathways/mechanisms including the paracellular route, divalent ion absorption, metabolon formation and cellular trafficking of transporters. Notably, some of these have already attracted practical attention in laboratories.

Dataset Information

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

Publications

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

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