Isolation and developmental expression of the amphioxusPax-6gene(AmphiPax-6): insights into eye and photoreceptor evolution

Abstract

Pax-6 genes have been identified from a broad range of invertebrate and vertebrate animals and shown to be always involved in early eye development. Therefore, it has been proposed that the various types of eyes evolved from a single eye prototype, by a Pax-6-dependent mechanism. Here we describe the characterization of a cephalochordate Pax-6 gene. The single amphioxus Pax-6 gene (AmphiPax-6) can produce several alternatively spliced transcripts, resulting in proteins with markedly different amino and carboxy termini. The amphioxus Pax-6 proteins are 92% identical to mammalian Pax-6 proteins in the paired domain and 100% identical in the homeodomain. Expression of AmphiPax-6 in the anterior epidermis of embryos may be related to development of an olfactory epithelium. Expression is also detectable in Hatschek's left diverticulum as it forms the preoral ciliated pit, part of which gives rise to the homolog of the vertebrate anterior pituitary. A zone of expression in the anterior neural plate of early embryos is carried into the cerebral vesicle (a probable diencephalic homolog) during neurulation. This zone includes cells that will differentiate into the lamellar body, a presumed homolog of the vertebrate pineal eye. In neurulae, AmphiPax-6 is also expressed in ventral cells at the anterior tip of the nerve cord; these cells are precursors of the photoreceptive neurons of the frontal eye, the presumed homolog of the vertebrate paired eyes. However, AmphiPax-6 expression was not detected in two additional types of photoreceptors, the Joseph cells or the organs of Hesse, which are evidently relatively recent adaptations (ganglionic photoreceptors) and appear to be rare exceptions to the general rule that animal photoreceptors develop from a genetic program triggered by Pax-6.

The Origination of Growth Hormone/Insulin-Like Growth Factor System: A Story From Ancient Basal Chordate Amphioxus

“…A series of immunohistochemical studies further detected positive signals of vertebrate pituitary hormones including luteinizing hormone (LH), follicle stimulating hormone (FSH), and luteinizing hormone-releasing hormone (LHRH) from Hatschek's pit (6)(7)(8)(9). Transcriptions of the pituitary-specific transcription factor Pit-1 and Pax6 have also been detected in the primordium of Hatschek's pit (10,11). These results suggest that Hatschek's pit and the vertebrate pituitary gland are homologous.…”

Gene Regulatory Networks of Epidermal and Neural Fate Choice in a Chordate

“…Among the downstream TFs, Rfx1/2/4 and FoxJ1 are orthologues of known ciliogenesis regulators in vertebrates ( Thomas et al 2010 ) consistent with the appearance of cilia in ectodermal cells of the amphioxus embryo during gastrulation. Although Pax4/6 and Six3/6 are referred to as typical neural genes, in amphioxus, they are expressed in the anterior epidermis together with Arpd2 ( Glardon et al 1998 ; Kozmik et al 2007 ; Albuixech-Crespo et al 2017 ), and their presence in the epidermal putative GRN might reflect the fact that the epidermal explants adopt an anterior fate, consistent with the absence of the organizer. Finally, concerning Gata1/2/3, it has been shown that Gata3 interacts with Tfap2a, Tfap2c, and Grhl2 during embryonic stem cells differentiation into committed surface ectoderm in vertebrates ( Li et al 2019 ).…”

Functional Conservation and Genetic Divergence of Chordate Glycinergic Neurotransmission: Insights from Amphioxus Glycine Transporters

“…In N4 neurulae, GlyT2.1 was faintly expressed in the dorsal part of the prospective posterior cerebral vesicle, where the lamellar body will develop. Interestingly, this stage corresponds to the initiation of lamellar body differentiation [ 80 , 82 ]. During subsequent development (at T0 and T1 stages), GlyT2.1 expression remained conspicuous in this region of the cerebral vesicle and, in L1 larvae, in which the first lamellate cells have already differentiated [ 83 ], GlyT2.1 expression was still detectable in the lamellar body, extending also to the dorsal part of the anterior cerebral vesicle.…”