Molecular patterning during the development of Phoronopsis harmeri reveals similarities to rhynchonelliform brachiopods

Carmen Andrikou,Mark Q Martindale,Chris J Lowe,Andreas Hejnol,Yale J Passamaneck

doi:10.1186/s13227-019-0146-1

Carmen Andrikou, Mark Q Martindale + Show 3 more

Open Access

https://doi.org/10.1186/s13227-019-0146-1

Copy DOI

Abstract

BackgroundPhoronids, rhynchonelliform and linguliform brachiopods show striking similarities in their embryonic fate maps, in particular in their axis specification and regionalization. However, although brachiopod development has been studied in detail and demonstrated embryonic patterning as a causal factor of the gastrulation mode (protostomy vs deuterostomy), molecular descriptions are still missing in phoronids. To understand whether phoronids display underlying embryonic molecular mechanisms similar to those of brachiopods, here we report the expression patterns of anterior (otx, gsc, six3/6, nk2.1), posterior (cdx, bra) and endomesodermal (foxA, gata4/5/6, twist) markers during the development of the protostomic phoronid Phoronopsis harmeri.ResultsThe transcription factors foxA, gata4/5/6 and cdx show conserved expression in patterning the development and regionalization of the phoronid embryonic gut, with foxA expressed in the presumptive foregut, gata4/5/6 demarcating the midgut and cdx confined to the hindgut. Furthermore, six3/6, usually a well-conserved anterior marker, shows a remarkably dynamic expression, demarcating not only the apical organ and the oral ectoderm, but also clusters of cells of the developing midgut and the anterior mesoderm, similar to what has been reported for brachiopods, bryozoans and some deuterostome Bilateria. Surprisingly, brachyury, a transcription factor often associated with gastrulation movements and mouth and hindgut development, seems not to be involved with these patterning events in phoronids.ConclusionsOur description and comparison of gene expression patterns with other studied Bilateria reveals that the timing of axis determination and cell fate distribution of the phoronid shows highest similarity to that of rhynchonelliform brachiopods, which is likely related to their shared protostomic mode of development. Despite these similarities, the phoronid Ph. harmeri also shows particularities in its development, which hint to divergences in the arrangement of gene regulatory networks responsible for germ layer formation and axis specification.

Highlights

Phoronids, rhynchonelliform and linguliform brachiopods show striking similarities in their embryonic fate maps, in particular in their axis specification and regionalization
To identify the appearance and segregation of the primary embryonic fates in Ph. harmeri, we identified orthologs of evolutionary conserved developmental genes often associated with anterior [38,39,40,41,42], posterior [43, 44] and endomesodermal identities [45,46,47,48,49,50], and revealed their spatial expression during embryonic development by whole mount in situ hybridization (WMISH)
Brachyury seems to be unrelated with gastrulation, hindgut and mouth patterning in phoronids Comparison of embryos from different evolutionary lineages has shown that the molecular interplay of axial and cellular specification is sometimes characterized by a remarkable conservation of expression patterns for many genes, and by important lineage-specific novelties [51,52,53,54,55]

Summary

Introduction

Rhynchonelliform and linguliform brachiopods show striking similarities in their embryonic fate maps, in particular in their axis specification and regionalization. To understand whether phoronids display underlying embryonic molecular mechanisms similar to those of brachiopods, here we report the expression patterns of anterior (otx, gsc, six3/6, nk2.1), posterior (cdx, bra) and endomesodermal (foxA, gata4/5/6, twist) markers during the development of the protostomic phoronid Phoronopsis harmeri. With the exception of Hox genes [5], molecular studies on embryonic development of phoronids are still lacking and are important to understand the precise timing of germ layer segregation and cell specification. Due to their informative phylogenetic position (as sister group, together with Ectoprocta, to Brachiopoda), phoronids can shed light on whether a similar developmental mode is shaped by conserved molecular mechanisms in closely related taxa. Most phoronids are characterized by a planktotrophic actinotroch larva (Fig. 1b), which undergoes a rapid, catastrophic metamorphosis to give rise to the adult body plan [12, 13]

Methods

Results

Discussion

Conclusion