Conserved Anterior Boundaries of Hox Gene Expression in the Central Nervous System of the LeechHelobdella

Abstract

Molecular developmental studies of fly and mouse embryos have shown that the identity of individual body segments is controlled by a suite of homeobox-containing genes called the Hox cluster. To examine the conservation of this patterning mechanism in other segmented phyla, we here describe four Hox gene homologs isolated from glossiphoniid leeches of the genus Helobdella. Based on sequence similarity and phylogenetic analysis, the leech genes Lox7, Lox6, Lox20, and Lox5 are deemed to be orthologs of the Drosophila genes lab, Dfd, Scr, and Antp, respectively. Sequence similarities between Lox5 and Antp outside the homeodomain and phylogenetic reconstructions suggest that the Antennapedia family of Hox genes (as defined by Bürglin, 1994) had already expanded to include at least two discrete Antp and Ubx/abdA precursors prior to the annelid/arthropod divergence. In situ hybridization reveals that the four Lox genes described in this study are all expressed at high levels within the segmented portion of the central nervous system (CNS), with variable levels of expression in the segmental mesoderm. Little or no expression was seen in peripheral ectoderm or endoderm, or in the unsegmented head region (prostomium). Each Lox gene has a distinct anterior expression boundary within one of the four rostral segments, and the anterior-posterior (AP) order of these expression boundaries is identical to that reported for the orthologous Hox gene products in fly and mouse. This finding supports the idea that the process of AP axis differentiation is conserved among the higher metazoan phyla with respect to the regional expression of individual Hox genes along that axis. One unusual feature of leech Hox genes is the observation that some genes are only expressed during later development -- beginning at the time of terminal cell differentiation -- whereas others begin expression at a much earlier stage, and their RNA ceases to be detectable shortly after the onset of expression of the 'late' Hox genes. The functional significance of this temporal disparity is unknown, but it is noteworthy that only the two 'early' Hox genes display high levels of mesodermal expression.

HOX genes in the sepiolid squid Euprymna scolopes : Implications for the evolution of complex body plans

“…It is most similar to HruHox5 from the archaegastropod Haliotis (46) and additional Lophotrochozoan Hox genes, including the brachiopod Lingula and the polychaete Nereis (14). It also shows significant sequence similarity to Amphi-Hox5 (17), and the leech Hox genes Lox20 and Lox6 (47).…”

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Consistent with their disintegrated Hox clusters, H. robusta and S. mediterranea show no temporal collinearity and only remnants of spatial collinearity (41,51,52). Conversely, C. teleta, which apparently has a split cluster, does exhibit these features (43).…”

“…Although Hox gene expression is known for a handful of spiralian species (26,41,43,(45)(46)(47)(48)(49)(50)(51)(52)(53)(54), the relationship between genomic organization and expression domains is known for only three of these species, namely the annelids C. teleta and H. robusta and the planarian S. mediterranea. Consistent with their disintegrated Hox clusters, H. robusta and S. mediterranea show no temporal collinearity and only remnants of spatial collinearity (41,51,52).…”

Testing the vulnerability of the phylotypic stage: On modularity and evolutionary conservation

“…Slack et al (1993) made the intriguing observation that the most conserved developmental stage within vertebrates is also the stage during which the Hox genes are sequentially activated in the order that they have in the Hox cluster on the chromosomes (temporal and spatial colinearity). Comparison with other taxa suggests that this sequential gene expression is a highly conserved plesiomorph character (McGinnis and Krumlauf, 1992;Kourakis et al, 1997;Brooke et al, 1998). Duboule (1994) hypothesized that the nature of the precise regulation of Hox genes is the cause of the conservation of the phylotypic stage.…”