Abstract
BackgroundAlthough chordates descend from a segmented ancestor, the evolution of head segmentation has been very controversial for over 150 years. Chordates generally possess a segmented pharynx, but even though anatomical evidence and gene expression analyses suggest homologies between the pharyngeal apparatus of invertebrate chordates, such as the cephalochordate amphioxus, and vertebrates, these homologies remain contested. We, therefore, decided to study the evolution of the chordate head by examining the molecular mechanisms underlying pharyngeal morphogenesis in amphioxus, an animal lacking definitive neural crest.ResultsFocusing on the role of retinoic acid (RA) in post-gastrulation pharyngeal morphogenesis, we found that during gastrulation, RA signaling in the endoderm is required for defining pharyngeal and non-pharyngeal domains and that this process involves active degradation of RA anteriorly in the embryo. Subsequent extension of the pharyngeal territory depends on the creation of a low RA environment and is coupled to body elongation. RA further functions in pharyngeal segmentation in a regulatory network involving the mutual inhibition of RA- and Tbx1/10-dependent signaling.ConclusionsThese results indicate that the involvement of RA signaling and its interactions with Tbx1/10 in head segmentation preceded the evolution of neural crest and were thus likely present in the ancestral chordate. Furthermore, developmental comparisons between different deuterostome models suggest that the genetic mechanisms for pharyngeal segmentation are evolutionary ancient and very likely predate the origin of chordates.Electronic supplementary materialThe online version of this article (doi:10.1186/2041-9139-5-36) contains supplementary material, which is available to authorized users.
Highlights
Chordates descend from a segmented ancestor, the evolution of head segmentation has been very controversial for over 150 years
RA, a natural morphogen synthesized from vitamin A, binds to heterodimers of the retinoic acid receptor (RAR) and retinoid X receptor (RXR), allowing the complex to bind to regulatory regions of target genes and thereby activate transcription
RA signaling is required for both regional specification and morphogenesis of the pharynx To determine if RA regulates development of the pharynx once it is initially specified, embryos were treated with either RA or the RAR antagonist BMS009 at the early/mid neurula (16 hpf), mid neurula (20 hpf) and late neurula (24 hpf) stage and subsequently fixed at the early larval stage (36 hpf)
Summary
Chordates descend from a segmented ancestor, the evolution of head segmentation has been very controversial for over 150 years. The gene is expressed in the mesenchyme of the upper lip, velar muscles and pharyngeal arches, while, in gnathostomes, Tbx1/ 10 is detectable both in neural crest and head mesenchyme derivatives [9,10]. In both amphioxus and aquatic vertebrates, Pax2/5/8 is expressed where the gill slits are forming as well as in the endostyle or its vertebrate homolog, the thyroid gland, and in the central nervous system (CNS), while Pax1/9 genes are broadly expressed in the pharyngeal endoderm of all chordates [11,12,13]. Excess RA leads to a compression of the pharynx in lampreys [23,24] and to a fusion of the first two pharyngeal arches in gnathostomes, while the inhibition of RA signaling in gnathostomes, either genetically or by vitamin A deficiency, results in a loss of posterior pharyngeal structures [19,20,21,22,25,26,27]
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