Involvement of Hox genes in shell morphogenesis in the encapsulated development of a top shell gastropod (Gibbula varia L.)

Molecular Phylogenetics, Department of Evolutionary Biology, Faculty of Life Sciences, University of Vienna, Althanstr. 14, 1090, Vienna, Austria.
Development Genes and Evolution (Impact Factor: 2.44). 12/2009; 219(9-10):523-30. DOI: 10.1007/s00427-009-0308-6
Source: PubMed


Regulatory gene expression during the patterning of molluscan shells has only recently drawn the attention of scientists. We show that several Hox genes are expressed in association with the shell gland and the mantle in the marine vetigastropod Gibbula varia (L.). The expression of Gva-Hox1, Gva-Post2, and Gva-Post1 is initially detected in the trochophore larval stage in the area of the shell field during formation of embryonic shell. Later, during development, these genes are expressed in the mantle demonstrating their continuous role in larval shell formation and differentiation of mantle edge that secretes the adult shell. Gva-Hox4 is expressed only late during the development of the veliger-like larva and may also be involved in the adult shell morphogenesis. Additionally, this gene also seems to be associated with secretion of another extracellular structure, the operculum. Our data provide further support for association of Hox genes with shell formation which suggest that the molecular mechanisms underlying shell synthesis may consist of numerous conserved pattern-formation genes. In cephalopods, the only other molluscan class in which Hox gene expression has been studied, no involvement of Hox genes in shell formation has been reported. Thus, our results suggest that Hox genes are coopted to various functions in molluscs.

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Available from: Leyli Samadi, Jan 19, 2015
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    • "While Raven’s model of shell gland induction [26] represents the canonical theory of molluscan shell field specification, the molecular mechanisms that initiate and underlie this process remain largely unknown. Molecular analyses that have previously identified transcription factors and signalling molecules in the shell gland and the evaginated and expanding shell field are expressed well after the specification of shell forming cells [19,21,24,31]. We are therefore developing L. stagnalis as a model for molecular investigations into the mechanisms that first specify shell forming cells, and through comparative studies, to enhance our understanding of how the variety of molluscan shells evolved. "
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    ABSTRACT: The morphological variety displayed by the molluscan shell underlies much of the evolutionary success of this phylum. However, the broad diversity of shell forms, sizes, ornamentations and functions contrasts with a deep conservation of early cell movements associated with the initiation of shell construction. This process begins during early embryogenesis with a thickening of an ectodermal, 'dorsal' (opposite the blastopore) population of cells, which then invaginates into the blastocoel to form the shell gland. The shell gland evaginates to form the shell field, which then expands and further differentiates to eventually become the adult shell-secreting organ commonly known as the mantle. Despite the deep conservation of the early shell forming developmental program across molluscan classes, little is known about the fine-scale cellular or molecular processes that underlie molluscan shell development. Using modern imaging techniques we provide here a description of the morphogenesis of a gastropod shell gland and shell field using the pulmonate gastropod Lymnaea stagnalis as a model. We find supporting evidence for a hypothesis of molluscan shell gland specification proposed over 60 years ago, and present histochemical assays that can be used to identify a variety of larval shell stages and distinct cell populations in whole mounts. By providing a detailed spatial and temporal map of cell movements and differentiation events during early shell development in L. stagnalis we have established a platform for future work aimed at elucidation of the molecular mechanisms and regulatory networks that underlie the evo-devo of the molluscan shell.
    Full-text · Article · Jul 2013 · BMC Developmental Biology
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    • "Hox1 has also been shown to be expressed in the shell-field margin of gastropods (Hinman et al., 2002; Samadi and Steiner, 2009). In gastropods, dpp is expressed in cells surrounding the engrailed-positive cells (Nederbragt et al., 2002; Iijima et al., 2008). "
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    ABSTRACT: The operculum is a novel structure in gastropod molluscs. Because the operculum shows notable similarities to the shell plate, we asked whether there were an evolutionary link between these two secretory organs. We found that some of the genes involved in shell-field development are expressed in the operculum, such as dpp and grainyhead, whereas engrailed and Hox1 are not. Specific knockdown of dpp by injection of double-stranded RNA (dsRNA) resulted in malformation of the shell plate. The shell plate was smaller due to failure of activation of cell proliferation in the shell-field margin. The expressions of grainyhead and chitin synthase 1 in the shell field margin were suppressed by dpp-dsRNA. However, matrix secretion was not completely abolished, and the expressions of ferritin, engrailed or Hox1 were not affected by dpp-dsRNA, indicating that dpp is partly involved in the developmental pathway for shell matrix secretion. We also present evidence that dpp performs a key role in operculum development. Indeed, dpp-dsRNA impaired matrix secretion in the operculum as well as expression of grainyhead. Based on these observations that dpp is important for development of both the shell plate and operculum, we conclude that co-option of dpp to the posterior part of the foot contributed to the innovation of the operculum in gastropods.
    Preview · Article · Apr 2012 · Developmental Biology
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    • "This gene is also similarly expressed in the veliger larvae of the two gastropods , where the transcripts are detected in the anterior margin of the mantle ( Hinman et al . 2003 ; Samadi and Steiner 2009 ) . Both Gva - Hox4 and Has - Hox4 genes are expressed in the anterior margin of the mantle at the posttorsional veliger stage , although Gva - Hox4 expression is restricted to the dorsal mantle edge . "
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    ABSTRACT: Hox transcription factors, a subfamily of homeobox genes, are expressed in distinct, often overlapping domains along the anterior-posterior body axis of animal embryos. Here, we report the sequence and expression pattern of Hox2, Hox3, Hox4, Hox5, Lox5, Hox7, Lox4, and Lox2 in different larval stages during the encapsulated development of the marine gastropod Gibbula varia. Our results show that all Gva-Hox genes are expressed in ectoderm-derived cells. Hox2, Hox3, Hox4, Hox5, and Hox7 are expressed in overlapping patterns in the pedal, pleural, oesophageal, and visceral ganglia, supporting the ancestral role of Hox genes in the neurogenesis processes in bilaterians. Gva-Hox1, Gva-Post2, and Gva-Post1 genes are involved in shell morphogenesis and have apparently lost their role in neurogangliogenesis. Lox5, Lox4, and Lox2 are expressed in different cells of the apical organ during the earlier larval stage (trochophore) and the cerebral ganglia during later larval stages (veliger). These results support the hypothesis that apical organ neurosensory cells contribute to the formation of cerebral ganglia commissures during metamorphosis. Gva-Hox7 and Gva-Lox4 are additionally expressed in the prototroch of the trochophore and in the velar area of the veliger larvae. This contradicts with the expression of these genes in the annelids, where most of Hox genes are expressed in the posttrochal area and are involved in segmental determination. Therefore, expression of Hox genes may serve as an example of co-option and plasticity of gene function during evolution of gastropods.
    Full-text · Article · Oct 2010 · Development Genes and Evolution
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