Ptc, Smo, Sufu, and the Hedgehog signaling pathway in amphioxus

Abstract

The Hedgehog (Hh) signaling pathway regulates many developmental processes both in vertebrates and in invertebrates. However, little is known about this pathway in the cephalochordate amphioxus. In this paper, we focus on the Ptc, Smo, and Sufu homologs in amphioxus, which are the key members of the Hh signaling pathway. Their genomic structures show their comparability with homologs in vertebrates. In situ hybridization reveals that amphioxus Ptc, Smo, and Sufu have similar expression patterns in embryogenesis. They are expressed in the neural plate at early neurula stage, and then down-regulated in dorsal neural ectoderm. During development, their transcripts appear and persist in the notochord, the wall of the head cavity, the epithelium of the pharynx, and the gut. The data show that the expression patterns of these three genes are overlapping with Hh and Gli during the embryonic development in amphioxus. Moreover, injection of amphioxus Hh RNA into zebrafish-fertilized eggs can expand the expression domains of Ptc1 and Nk2.2a, the target genes of the Hh signaling pathway, which is similar to the injection of zebrafish Sonic hh a (zShha) and Sonic hh b (zShhb). Our results suggest that amphioxus may possess a conserved and functional Hh signaling pathway similar to that of vertebrates.

Developmental cell-cell communication pathways in the cephalochordate amphioxus: actors and functions

“…In neurula stage embryos and in larvae, Hh is expressed in the notochord, the tailbud, the endostyle and the pre-oral pit (Shimeld, 1999, Shimeld et al, 2007, Somorjai et al, 2008, as well as transiently in some ventral neural tube cells (Shimeld, 1999). The expression of both Ptc, orthologous to Ptc1 and Ptc2 in vertebrates, and Smo was analyzed in B. belcheri (Lin et al, 2009). The Ptc transcripts are first detected in the dorsal region of gastrula stage embryos.…”

“…In neurulae, Ptc is expressed in newly formed somites and in the anterior endoderm (Lin et al, 2009). As the embryo elongates, expression is also detected in the notochord, the presumptive gill slit and the pre-oral pit.…”

“…As the embryo elongates, expression is also detected in the notochord, the presumptive gill slit and the pre-oral pit. Finally, at the larval stage, Ptc is expressed in the cerebral vesicle, the somites, the gill slits, the pre-oral pit, the club-shaped gland and in the gut and pharynx epithelium (Lin et al, 2009). Smo has a similar expression pattern.…”

“…Smo has a similar expression pattern. It is first expressed later than Ptc in the newly formed somites and anterior endoderm in early neurula stage embryos (Lin et al, 2009). Expression is observed at later stages in the somites, the gut and the anterior notochord (Lin et al, 2009).…”

Phylogenetic Origins of Brain Organisers

“…In amphioxus, the floor plate expresses hh , hnf3 , and netrin , but it remains to be established whether the cephalochordate floor plate exerts any signalling and/or axon guidance functions (Figures 1(c) and 2) [108, 134, 145]. Various components of the Hh signalling pathway are expressed in the nerve cord of amphioxus and in particular the Hh target gene patched becomes downregulated dorsally, possibly reflecting an involvement of this signalling pathway in neural ventralisation comparable to vertebrates [146]. Unlike vertebrates that transduce Shh signals via the combinatorial activity of three Gli genes, amphioxus only has a single gli gene that produces two transcripts with opposing activities and is expressed in the floor plate, but not in the notochord, consistent with a unidirectional induction of the lancelet's floor plate by notochord-derived Hh [147].…”