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.2010 Nov 22;277(1699):3381-9.
doi: 10.1098/rspb.2010.0647. Epub 2010 Jun 16.

Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression

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Ancient homeobox gene loss and the evolution of chordate brain and pharynx development: deductions from amphioxus gene expression

Thomas Butts et al. Proc Biol Sci..

Abstract

Homeobox genes encode a large superclass of transcription factors with widespread roles in animal development. Within chordates there are over 100 homeobox genes in the invertebrate cephalochordate amphioxus and over 200 in humans. Set against this general trend of increasing gene number in vertebrate evolution, some ancient homeobox genes that were present in the last common ancestor of chordates have been lost from vertebrates. Here, we describe the embryonic expression of four amphioxus descendants of these genes--AmphiNedxa, AmphiNedxb, AmphiMsxlx and AmphiNKx7. All four genes are expressed with a striking asymmetry about the left-right axis in the pharyngeal region of neurula embryos, mirroring the pronounced asymmetry of amphioxus embryogenesis. AmphiMsxlx and AmphiNKx7 are also transiently expressed in an anterior neural tube region destined to become the cerebral vesicle. These findings suggest significant rewiring of developmental gene regulatory networks occurred during chordate evolution, coincident with homeobox gene loss. We propose that loss of otherwise widely conserved genes is possible when these genes function in a confined role in development that is subsequently lost or significantly modified during evolution. In the case of these homeobox genes, we propose that this has occurred in relation to the evolution of the chordate pharynx and brain.

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Figures

Figure 1.
Figure 1.
Homeodomain alignment of ancient gene families lost in vertebrates. The gene families Nedx, Msxlx and NK7 are aligned to theDrosophila Antennapedia homeodomain. As with other homeobox gene families, diagnostic family-specific residues are found throughout the homeodomain. Species abbreviations are as follows: Dme,Drosophila melanogaster; Amphi,Branchiostoma floridae; Tca,Tribolium castaneum and Odi,Oikopleura dioica.
Figure 2.
Figure 2.
Nedx expression. (a,b)AmphiNedxa and (c,d)AmphiNedxb are both expressed at the mid-neurula stage in ventrolateral pharyngeal epidermis on the left-hand side, though the expression ofAmphiNedxb is considerably stronger and covers a much broader area. (a,c) Lateral views, (b,d) ventral views. Anterior is to the left in all panels; scale bar, 50 µm.
Figure 3.
Figure 3.
AmphiMsxlx expression.AmphiMsxlx is expressed at the mid-neurula stage in the left anterior gut diverticulum (asterisks) and in bilateral spots in the ventral anterior neural plate (arrowheads). (a) Lateral view; (b) dorsal view; (c) is rotated slightly laterally, off dorsal, to reveal these bilateral spots more clearly. Anterior is to the left in all panels; scale bar, 50 µm.
Figure 4.
Figure 4.
AmphiNKx7 expression.AmphiNKx7 is expressed at the (a–c) mid- (nine somites) and (d–f) late (12 somites) neurula stages in the anterior neural plate (arrowheads) and in the left side of the pharyngeal endoderm (arrows). (a,d) Lateral views; (b,e) dorsal views; (c,f) ventral views. Anterior is to the left in all panels; scale bar = 50 µm.
Figure 5.
Figure 5.
A hypothesis for the evolution of pharynx development. The evolution of chordates was marked by the relocation of the mouth to aPitx-expressing territory, the expression of which may have been controlled by BMP signalling (Olfactores) or Nodal signalling (amphioxus). In the Olfactores lineage, the pharynx has undergone significant modification with the oral function ofPitx being controlled independently of the asymmetry function (blue).Msxlx,Nedx andNK7, which in amphioxus are putatively downstream ofPitx have been lost from Olfactores (red), except two Nedx paralogues in the appendicularianOikopleura (*). The expression ofMsxlx,Nedx andNK7 in non-chordate bilaterians is unexplored (green).
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