On a possible evolutionary link of the stomochord of hemichordates to pharyngeal organs of chordates

Abstract

Summary As a group closely related to chordates, hemichordate acorn worms are in a key phylogenic position for addressing hypotheses of chordate origins. The stomochord of acorn worms is an anterior outgrowth of the pharynx endoderm into the proboscis. In 1886 Bateson proposed homology of this organ to the chordate notochord, crowning this animal group “hemichordates.” Although this proposal has been debated for over a century, the question still remains unresolved. Here we review recent progress related to this question. First, the developmental mode of the stomochord completely differs from that of the notochord. Second, comparison of expression profiles of genes including Brachyury, a key regulator of notochord formation in chordates, does not support the stomochord/notochord homology. Third, FoxE that is expressed in the stomochord-forming region in acorn worm juveniles is expressed in the club-shaped gland and in the endostyle of amphioxus, in the endostyle of ascidians, and in the thyroid gland of vertebrates. Based on these findings, together with the anterior endodermal location of the stomochord, we propose that the stomochord has evolutionary relatedness to chordate organs deriving from the anterior pharynx rather than to the notochord.

Hemichordate models

“…These morphological features gave rise to the name, 'HemiChordates' [9,10 ,11 ]. Recent molecular developmental studies, however, have refuted the presumed homology of the stomochord and notochord [35 ]. The notochord is a key source of secreted factors, including Shh and the BMP antagonists Chordin, Noggin, and Follistatin, essential for neural patterning in vertebrates.…”

“…Moreover, the Brachyury gene, a key transcription factor for notochord formation in chordates, is not expressed in the developing stomochord [5,35 ,36 ]. On the other hand, vertebrate prechordal endomesoderm genes, otx, dmbx, and hex, are expressed in the stomochord-forming region and in endoderm [35 ]. Another transcription factor, FoxE, which is thyroidspecific in vertebrates, endostyle-specific in ascidians, and specific to the club-shaped gland in amphioxus, is expressed in the stomochord [3,35 ].…”

“…On the other hand, vertebrate prechordal endomesoderm genes, otx, dmbx, and hex, are expressed in the stomochord-forming region and in endoderm [35 ]. Another transcription factor, FoxE, which is thyroidspecific in vertebrates, endostyle-specific in ascidians, and specific to the club-shaped gland in amphioxus, is expressed in the stomochord [3,35 ]. Our current understanding of the stomochord is that it is a pharynx-derived organ, homologous to chordate counterparts [3,14 ,35 ].…”

Chordate evolution and the three-phylum system

“…'half-chord') to the chordate notochord, crowning this animal group 'hemichordates'. A recent evodevo study has demonstrated that FoxE is commonly expressed in the stomochord and the chordate endostyle, suggesting that the stomochord is evolutionarily related to the endostyle, rather than the notochord [71]. That is, the two digestive-system-associated structures evolved prior to divergence of chordates from non-chordate deuterostomes [17,18], although the system developed more complex functions in chordates.…”

The chordate ancestor possessed a single copy of the Brachyury gene for notochord acquisition

“…Chordates comprise three taxa, cephalochordates, urochordates or tunicates, and vertebrates [2]. These are thought to have originated from a common ancestor of the deuterostomes, together with ambulacrarians, a clade containing echinoderms and hemichordates.…”