Retinoic acid signaling acts via Hox1 to establish the posterior limit of the pharynx in the chordate amphioxus

Abstract

expression of these endodermal genes in embryos treated with RA or the RA antagonist BMS009 indicates that Pax1/9, Pitx and Notch are probably more upstream than Otx and Nodal in the hierarchy of genes repressed by RA signaling. This work highlights the potential of amphioxus, a genomically simple, vertebrate-like invertebrate chordate, as a paradigm for understanding gene hierarchies similar to the more complex ones of vertebrates.

Evolution of the thyroid: Anterior–posterior regionalization of theOikopleuraendostyle revealed byOtx,Pax2/5/8, andHox1expression

“…Of interest, in later developmental stages, Pax2/5/8 expression diminishes in the most anterior part of the amphioxus endostyle at the time and location predicted from our observations in Oikopleura, corresponding to the stage at which Pax2/5/8 expression becomes restricted to the central part of the endostyle (Kozmik et al, 1999). Although Otx and Hox1 expression have not yet been investigated in the differentiated endostyle of amphioxus, Otx and Hox1 are expressed early in the pharyngeal endoderm from which the endostyle differentiates (Williams and Holland, 1996;Schubert et al, 2005). In the pharynx of 30-hpf amphioxus embryos, Otx is expressed anteriorly, and Hox1 is expressed posteriorly (Schubert et al, 2005), following the same order that we observed in the expression of the orthologs in Oikopleura when endostyle precursors differentiate from the pharyngeal primordium.…”

“…Although Otx and Hox1 expression have not yet been investigated in the differentiated endostyle of amphioxus, Otx and Hox1 are expressed early in the pharyngeal endoderm from which the endostyle differentiates (Williams and Holland, 1996;Schubert et al, 2005). In the pharynx of 30-hpf amphioxus embryos, Otx is expressed anteriorly, and Hox1 is expressed posteriorly (Schubert et al, 2005), following the same order that we observed in the expression of the orthologs in Oikopleura when endostyle precursors differentiate from the pharyngeal primordium. It is thus possible that the genetic mechanisms that pattern the AP axis of the pharyngeal endoderm from which the endostyle derives also pattern the endostyle.…”

“…It is thus possible that the genetic mechanisms that pattern the AP axis of the pharyngeal endoderm from which the endostyle derives also pattern the endostyle. The mechanism of AP patterning of the pharyngeal endoderm in amphioxus is shared with urochordates and vertebrates, which also express Otx in stomodeal and anterior pharyngeal endoderm (Simeone et al, 1993;Williams and Holland, 1996;, and express a combinatorial code of Hox genes to define AP identity in posterior pharyngeal endoderm (Hunt et al, 1991;Holland and Holland, 1996;Couly et al, 2002;Miller et al, 2004;Schubert et al, 2005;Crump et al, 2006). Thus, expression of Otx and Hox genes in anterior and posterior endostyle regions in Oikopleura suggests the hypothesis that the endostyle uses genetic mechanisms that regionalize the anterior endoderm in the pharynx (GrapinBotton and Melton, 2000;Shivdasani, 2002).…”

Retinoic acid signaling in development: Tissue‐specific functions and evolutionary origins

“…In invertebrate chordates, as in other invertebrate deuterostomes, the establishment of left/right asymmetry probably involves the same gene hierarchy as in vertebrates (Chea et al, 2005;Duboc et al, 2004Duboc et al, , 2005. For example, as in vertebrates, homologs of shh, pitx, and nodal are all expressed asymmetrically during amphioxus development (Schubert et al, 2005;Yu et al, 2007). However, both in amphioxus (Schubert et al, 2005) and ascidians (Hinman and Degnan, 1998), treatments with exogenous RA do not obviously alter the establishment of the left/right body axis suggesting that a role for RA signaling in establishing global left/ right asymmetry in the embryo is a vertebrate innovation (Schubert et al, 2005).…”

“…In the cephalochordate amphioxus, which lacks migrating NCCs, patterning of the pharyngeal endoderm is also RA-dependent (Escrivà et al, 2002;Holland and Holland, 1996;Schubert et al, 2005). Treatments with exogenous RA lead to a loss of pharyngeal structures (e.g.…”