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

Leyli Samadi,Gerhard Steiner

doi:10.1186/1471-213x-10-74

Abstract

BackgroundPresence 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.ResultsWe 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.ConclusionsIn 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.

Highlights

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
In order to elucidate the function of the ParaHox genes in molluscs and to gain broader insights into the evolution of the ParaHox genes in the Lophotrochozoa, we describe the sequences as well as expression patterns for all three ParaHox orthologues by whole mount in situ hybridization from embryonic through juvenile stages in the top shell Gibbula varia
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)

Summary

Introduction

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. Gsx is expressed more anteriorly and only in the nervous system, while Xlox and Cdx are expressed within the gut primordium with Xlox anterior to Cdx [25,26,27,28]. The Aty-Xlox expression is found in the archenteron as well as in ectodermal cells near the vegetal region of early and mid-gastrula stages [29]. This expression pattern is very different from those of Xlox homologues in other deuterostomes

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