Hox gene expression during development of the phoronid Phoronopsis harmeri

Abstract

Background: Phoronida is a small group of marine worm-like suspension feeders, which together with brachiopods and bryozoans form the clade Lophophorata. Although their development is well studied on the morphological level, data regarding gene expression during this process are scarce and restricted to the analysis of relatively few transcription factors. Here we present a description of the expression patterns of Hox genes during the embryonic and larval development of the phoronid Phoronopsis harmeri. Results: We identified sequences of eight Hox genes in the transcriptome of Ph. harmeri and determined their expression pattern during embryonic and larval development using whole mount in situ hybridization. We found that none of the Hox genes is expressed during embryonic development. Instead their expression is initiated in the later developmental stages, when the larval body is already formed. In the investigated initial larval stages the Hox genes are expressed in the non-collinear manner in the posterior body of the larvae: in the telotroch and the structures that represent rudiments of the adult worm. Additionally, we found that certain head-specific transcription factors are expressed in the oral hood, apical organ, preoral coelom, anterior digestive system and developing larval tentacles, anterior to the Hox-expressing territories. Conclusions: The lack of Hox gene expression during early development of Ph. harmeri indicates that the larval body develops without positional information from the Hox patterning system. Such phenomenon might be a consequence of the evolutionary intercalation of the larval form into an ancestral life cycle of phoronids. The observed Hox gene expression can also be a consequence of the actinotrocha representing a “head larva”, which is composed of the most anterior body region that is devoid of Hox gene expression. Such interpretation is further supported by the expression of head-specific transcription factors. This implies that the Hox patterning system is used for the positional information of the trunk rudiments and is, therefore, delayed to the later larval stages. We propose that a new body form was intercalated to the phoronid life cycle by precocious development of the anterior structures or by delayed development of the trunk rudiment in the ancestral phoronid larva.

The Evolution of Hox Genes in Spiralia

“…[29] (Figure 1). The absence of Lox2 is shared with Phoronida and Brachiopoda [7,[30][31][32] (Figure 1), however it remains unclear whether the gene was lost in the common ancestor of Lophophorates, or originated after split of them from the remaining Lophotrochozoa [32]. Phoronids seem to have lost Post1 and Scr [30,32].…”

“…The absence of Lox2 is shared with Phoronida and Brachiopoda [7,[30][31][32] (Figure 1), however it remains unclear whether the gene was lost in the common ancestor of Lophophorates, or originated after split of them from the remaining Lophotrochozoa [32]. Phoronids seem to have lost Post1 and Scr [30,32]. Regardless of these losses, an ordered Hox cluster appears ancestral for both Brachiopoda and Phoronida, with the lineage of the brachiopod Lingula having experienced a genomic inversion of the cluster [7,30,31].…”

“…Hox genes represent one of the most comprehensively studied families of animal transcription factors and their expression has been investigated in numerous Spiralia [25], representing diverse evolutionary lineages, such as flatworms [23, 51, 52], rotifers [12], chaetognaths [13], dicyemids [53], nemerteans [34,35], lophophorates [7,32,36,54], annelids [40,41,43,45,[55][56][57][58] and mollusks [37,38,[59][60][61][62][63][64][65][66]. However, the function of particular Hox genes in those studied species is inferred only from expression patterns, since among spiralians the functional studies of Hox genes has been conducted thus far only on adult planarians [52].…”

“…The Hox genes seem to not be Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 26 November 2021 expressed in any neural structures neither in phoronids nor brachiopods (which probably correlates with the extensive reduction of the central nervous system in those sessile animals) and instead they are expressed in various ectodermal and mesodermal domains in the non-colinear manner (Fig. 2; [7,32,36]). Interestingly, three Hox genes -pb, Hox3 and Dfd, show staggered mesodermal expression along the A-P axis in larval brachiopods [7], while after metamorphosis they are expressed in specific muscles [36], indicating cooption of a subset of the Hox gene system into mesodermal A-P specification in this clade.…”

“…Interestingly, three Hox genes -pb, Hox3 and Dfd, show staggered mesodermal expression along the A-P axis in larval brachiopods [7], while after metamorphosis they are expressed in specific muscles [36], indicating cooption of a subset of the Hox gene system into mesodermal A-P specification in this clade. Additionally, several of the Hox genes are expressed in specific morphological structures of both brachiopods (lab and Post1 in chaetal sacs, Scr in shell field [7,36]) and phoronids (pb in protonephridia and Lox4 at the junction between midgut and proctodeum [32]) suggesting that the Hox genes, released from their putative ancestral function in the patterning of neuroectoderm, became widely and independently coopted into morphogenesis of various organs in Lophophorata. Another interesting example of the evolution of new function for Hox genes can be found in planarians.…”