Hox gene expression in postmetamorphic juveniles of the brachiopod Terebratalia transversa

Abstract

Background: Hox genes encode a family of homeodomain containing transcription factors that are clustered together on chromosomes of many Bilateria. Some bilaterian lineages express these genes during embryogenesis in spatial and/or temporal order according to their arrangement in the cluster, a phenomenon referred to as collinearity. Expression of Hox genes is well studied during embryonic and larval development of numerous species; however, relatively few studies focus on the comparison of pre- and postmetamorphic expression of Hox genes in animals with biphasic life cycle. Recently, the expression of Hox genes was described for embryos and larvae of Terebratalia transversa, a rhynchonelliformean brachiopod, which possesses distinct metamorphosis from planktonic larvae to sessile juvenile. During premetamorphic development, T. transversa does not exhibit spatial collinearity and several of its Hox genes are recruited for the morphogenesis of novel structures. In our study we determined expression of Hox genes in post-metamorphic juveniles of T. transversa in order to examine metamorphosis-related changes of expression patterns and to test if Hox genes are expressed in the spatially collinear way in the postmetamorphic juveniles. Results: Hox genes are expressed in a spatially non-collinear manner in juveniles, generally showing similar patterns as ones observed in competent larvae: genes labial and Post1 are expressed in chaetae-related structures, sex comb reduced in the shell forming epithelium, whereas Lox5 and Lox4 in dorso-posterior epidermis. After metamorphosis expression of genes proboscipedia, Hox3, Deformed and Antennapedia becomes restricted to, respectively, shell musculature, prospective hinge rudiments, and pedicle musculature and epidermis. Conclusions: All developmental stages of T. transversa, including postmetamorphic juveniles, exhibit a spatial non-collinear Hox genes expression with only minor changes observed between pre- and postmetamorphic stages. Our results are concordant with morphological observation that metamorphosis in rhynchonelliformean brachiopods, despite being rapid, is rather gradual. The most drastic changes in Hox genes expression patterns observed during metamorphosis could be explained by the inversion of the mantle lobe, which relocates some of the more posterior larval structures into the anterior edge of the juveniles. Cooption of Hox genes for the morphogenesis of novel structures is even more pronounced in post-metamorphic brachiopods when compared to larvae.

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…This is in contrast to brachiopods, the putative close relatives of Phoronida, where various level of Hox cluster disorganization is shown ( Fig. 1A) and temporal and spatial collinearity is missing (16,40,89,90). Therefore, it remains important to examine whether phoronid Hox genes are also expressed in the spatio-temporally collinear manner during development, which would correspond with the retention of the organized Hox cluster shown in this clade.…”

“…Similarly, in rhynchonelliformean and craniiformean brachiopods none of the Hox genes are expressed in the larval anterior lobe (16,40), which contributes to the lophophore after metamorphosis (112). A lack of Hox expression in the adult lophophore tissue (as opposed to the remaining body regions) was shown for the linguliformean Lingula anatina, based on the tissue specific transcriptomics (89).…”

“…On the other hand, in animals with more gradual metamorphosis (e.g. cephalochordates, mollusks, annelids or brachiopods), the Hox genes seem to pattern both the larval and adult body plans in a relatively similar way (31,39,40,46,48). However, studies focusing on metamorphosis-related differences of Hox gene expression in Bilateria are still limited to a relatively few evolutionary lineages (40,92).…”

“…Luo et al (89) reported that Ph. australis lacks scr and post1 orthologues and suggested that those two genes, which are expressed in the shell forming tissues of brachiopods (16,40), might be lost in Phoronida due to the evolutionary reduction of the shell in this clade. Accordingly, we also did not identify orthologues of scr and post1 in P.…”

“…However, information about the molecular patterning is limited to the single study of 9 transcription factors (which include anterior, posterior and endomesodermal markers) during the development of Phoronopsis harmeri (85). Importantly, information about expression of Hox genes during development of any phoronid species is still lacking (40,59).…”