Hox gene expression during postlarval development of the polychaete Alitta virens

Abstract

BackgroundHox genes are the family of transcription factors that play a key role in the patterning of the anterior-posterior axis of all bilaterian animals. These genes display clustered organization and colinear expression. Expression boundaries of individual Hox genes usually correspond with morphological boundaries of the body. Previously, we studied Hox gene expression during larval development of the polychaete Alitta virens (formerly Nereis virens) and discovered that Hox genes are expressed in nereid larva according to the spatial colinearity principle. Adult Alitta virens consist of multiple morphologically similar segments, which are formed sequentially in the growth zone. Since the worm grows for most of its life, postlarval segments constantly change their position along the anterior-posterior axis.ResultsWe studied the expression dynamics of the Hox cluster during postlarval development of the nereid Alitta virens and found that 8 out of 11 Hox genes are transcribed as wide gene-specific gradients in the ventral nerve cord, ectoderm, and mesoderm. The expression domains constantly shift in accordance with the changing proportions of the growing worm, so expression domains of most Hox genes do not have stable anterior or/and posterior boundaries.In the course of our study, we revealed long antisense RNA (asRNA) for some Hox genes. Expression patterns of two of these genes were analyzed using whole-mount in-situ hybridization. This is the first discovery of antisense RNA for Hox genes in Lophotrochozoa.ConclusionHox gene expression in juvenile A. virens differs significantly from Hox gene expression patterns both in A. virens larva and in other Bilateria.We suppose that the postlarval function of the Hox genes in this polychaete is to establish and maintain positional coordinates in a constantly growing body, as opposed to creating morphological difference between segments.

Segment formation in Annelids: patterns, processes and evolution

“…By contrast, in Platynereis and Alitta, collinearity is less clear and only anterior Hox genes are expressed in the three segments of the larva. Interestingly, Bakalenko et al, (2013) found a much more regular collinear expression of Hox genes in a more advanced developmental stage of A. virens, a 15-segment juvenile. One could argue therefore that this juvenile stage of A. virens is the temporal homologue of the late Capitella metatrochophore and that the derived expression of Hox genes in the three-segment, early-settling larva of nereidids is an indication that this larva is itself a derived characteristic within annelids.…”

“…their expressions are organized in overlapping domains in the same order as the genes are found in their chromosomal cluster. Hox expression profiles have been extensively studied in species with different modes of development: the closely related Nereidids Platynereis dumerilii and Alitta virens on one side and the Capitellid Capitella teleta on the other (Kulakova et al, 2007;Fröbius et al, 2008;Bakalenko et al, 2013). Capitella broods larvae that make thirteen segments before being released.…”

Hox and ParaHox gene expression in early body plan patterning of polyplacophoran mollusks

“…In bilaterians, studies on the spatial and temporal expression pattern of Hox and ParaHox genes are mainly available for two of the three major clades, namely Deuterostomia (e.g., Prince et al., ; Lowe et al., ; Garcia‐Fernàndez, ; Aronowicz and Lowe, ) and Ecdysozoa (e.g., Wang et al., ; Averof and Akam, ; Averof and Patel, ; Orii et al., ; Peterson et al., ). Detailed Hox and ParaHox gene expression data within the third bilaterian superclade, Lophotrochozoa, are available to a much lesser degree such as for various annelid and two nemertean species (Nardelli‐Haefliger and Shankland, ; Nardelli‐Haefliger et al., ; Wong et al., ; Kourakis et al., ; Irvine and Martindale, ; Kulakova et al., ; Fröbius et al., ; Bakalenko et al., ; Gharbaran et al., ; Hiebert and Maslakova, ,b).…”

Demonstration of the preoral coelom in the brachiopod Lingula anatina with consideration of its phylogenetic significance

“…The prostomium lacks a coelom in most annelids, but the anlage of this coelom was described in the embryonic development of some polychaetes (Anderson, 1959). The specialization of the first two segments of body can be suggested by gene expression: most Hox genes are never expressed in the protostomium or peristomium of annelids (Fröbius et al, 2008;Bakalenko et al, 2013).…”