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

Abstract

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.

Keywords: chordates; hemichordates; notochord; pharyngeal organs; stomochord.

FIG. 1

Development of the stomochord in hemichordates and the notochord in amphioxus and ascidians. (a–c) A schematic drawing of development of the stomochord in Saccoglossus kowalevskii. (a) A late gastrula (36 hrs postfertilization) shown in longitudinal section. Anterior is to the top left. Ectoderm shown in green, mesoderm in red, and endoderm in yellow. (b) A late neurula embryo (3 days post-fertilization) shown in sagittal section. Anterior is to the top left. Dorsal is to the top right. (c) The two gill slit embryo (14 days post-fertilization) in sagittal section. Note the extended stomochord protruding into the prosome, two paired gill-slits, and ventral post-anal tail (redrawn from Lowe et al., 2006). (d) The stomochord in the proboscis of Ptychodera adult (redrawn from Peterson et al., 1999). (e–j) A schematic drawing of development of the notochord in amphioxus embryos (based on Hatschek, 1893; Conklin, 1932; Hirakow and Kajita, 1994). (e, f) Mid neurula, (g, h) mid-to-late neurula, and (I, j) late neurula. (e, g, i) Mid-sagittal sectioned, (f, h, j) cross-sectioned. During the time of neural tube formation, the notochord develops from the adjacent chordamesodermal plate that constitutes the roof of the archenteron. Namely, the notochord is formed by an upward pouching off of midline cells along of the chordamesodermal plate. (k–n) Ascidian notochord development from the 64-cell stage embryo. (k) The 64-cell stage embryo, (l) 110-cell stage embryo, and (m, n) late tailbud embryo. Infolding and convergent extension transform notochord precursor into a column of 40 stacked cells.

FIG. 2

Expression of genes in the stomochord-forming region in S. kowalevskii juveniles. (a) A schematic drawing of the stomochord-forming region, (b) bra, (c) chordin, (d) noggin, (e) admp, (f) foxA, (g) hh, (h) ptch, (i) frzb, (j) gsc, (k) hex, (l) dmbx, (m) otx, (n) pitx, (o) dkk1/2/4, and (p) leprecan (Lowe et al., 2003, ; Pani and Lowe, 2013) Black arrows indicate the stomochord-forming region and white arrow dorsal neural pit region.

FIG. 3

Comparison of the expression of foxE among hemichordates, cephalochordates, and urochordates. (a, b) Expression of foxE in the stomochord-forming region of Saccoglossus kowalevskii juveniles. Arrows indicate the gene expression, and white arrowhead the ciliated band positions. (c, d) Expression of foxE in the forming region of the club-shaped gland and endostyle of amphioxus embryo (c) and juvenile (d), and (e, f) in the endostyle of ascidian juveniles, whole juvenile (e) and section of the endostyle (f).